Abstract
Within eukaryotic cells, biochemical reactions need to be organized on the surface of membrane compartments that use distinct lipid constituents to dynamically modulate the functions of integral proteins or influence the selective recruitment of peripheral membrane effectors. As a result of these complex interactions, a variety of human pathologies can be traced back to improper communication between proteins and membrane surfaces; either due to mutations that directly alter protein structure or as a result of changes in membrane lipid composition. Among the known structural lipids found in cellular membranes, phosphatidylinositol (PtdIns) is unique in that it also serves as the membrane-anchored precursor of low-abundance regulatory lipids, the polyphosphoinositides (PPIn), which have restricted distributions within specific subcellular compartments. The ability of PPIn lipids to function as signaling platforms relies on both non-specific electrostatic interactions and the selective stereospecific recognition of PPIn headgroups by specialized protein folds. In this chapter, we will attempt to summarize the structural diversity of modular PPIn-interacting domains that facilitate the reversible recruitment and conformational regulation of peripheral membrane proteins. Outside of protein folds capable of capturing PPIn headgroups at the membrane interface, recent studies detailing the selective binding and bilayer extraction of PPIn species by unique functional domains within specific families of lipid-transfer proteins will also be highlighted. Overall, this overview will help to outline the fundamental physiochemical mechanisms that facilitate localized interactions between PPIn lipids and the wide-variety of PPIn-binding proteins that are essential for the coordinate regulation of cellular metabolism and membrane dynamics.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Change history
19 July 2019
This chapter was inadvertently published with an incorrect copyright holder. It has now been updated as below
References
Ago T, Takeya R, Hiroaki H, Kuribayashi F, Ito T, Kohda D, Sumimoto H (2001) The PX domain as a novel phosphoinositide- binding module. Biochem Biophys Res Commun 287(3):733–738. https://doi.org/10.1006/bbrc.2001.5629
Agranoff BW (2009) Turtles all the way: reflections on myo-Inositol. J Biol Chem 284(32):21121–21126. https://doi.org/10.1074/jbc.X109.004747
Agranoff BW, Bradley RM, Brady RO (1958) The enzymatic synthesis of inositol phosphatide. J Biol Chem 233(5):1077–1083
Agranoff BW, Benjamin JA, Hajra AK (1969) Biosynthesis of phosphatidylinositol. Ann N Y Acad Sci 165(2):755–760
Alam SL, Langelier C, Whitby FG, Koirala S, Robinson H, Hill CP, Sundquist WI (2006) Structural basis for ubiquitin recognition by the human ESCRT-II EAP45 GLUE domain. Nat Struct Mol Biol 13(11):1029–1030. https://doi.org/10.1038/nsmb1160
Altan-Bonnet N (2017) Lipid tales of viral replication and transmission. Trends Cell Biol 27(3):201–213. https://doi.org/10.1016/j.tcb.2016.09.011
Altan-Bonnet N, Balla T (2012) Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem Sci 37(7):293–302. https://doi.org/10.1016/j.tibs.2012.03.004
Alto NM, Shao F, Lazar CS, Brost RL, Chua G, Mattoo S, McMahon SA, Ghosh P, Hughes TR, Boone C, Dixon JE (2006) Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124(1):133–145. https://doi.org/10.1016/j.cell.2005.10.031
Alwarawrah M, Wereszczynski J (2017) Investigation of the effect of bilayer composition on PKCalpha-C2 domain docking using molecular dynamics simulations. J Phys Chem B 121(1):78–88. https://doi.org/10.1021/acs.jpcb.6b10188
Amarilio R, Ramachandran S, Sabanay H, Lev S (2005) Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J Biol Chem 280(7):5934–5944. https://doi.org/10.1074/jbc.M409566200
Anand K, Maeda K, Gavin AC (2012) Structural analyses of the Slm1-PH domain demonstrate ligand binding in the non-canonical site. PLoS One 7(5):e36526. https://doi.org/10.1371/journal.pone.0036526
Antonny B (2011) Mechanisms of membrane curvature sensing. Annu Rev Biochem 80:101–123. https://doi.org/10.1146/annurev-biochem-052809-155121
Arcaro A (1998) The small GTP-binding protein Rac promotes the dissociation of gelsolin from actin filaments in neutrophils. J Biol Chem 273(2):805–813
Baines AJ, Lu HC, Bennett PM (2014) The Protein 4.1 family: hub proteins in animals for organizing membrane proteins. Biochim Biophys Acta 1838(2):605–619. https://doi.org/10.1016/j.bbamem.2013.05.030
Balla T (2005) Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci 118(Pt 10):2093–2104. https://doi.org/10.1242/jcs.02387
Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93(3):1019–1137. https://doi.org/10.1152/physrev.00028.2012
Balla A, Balla T (2006) Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol 16(7):351–361. https://doi.org/10.1016/j.tcb.2006.05.003
Balla T, Baukal AJ, Guillemette G, Catt KJ (1988) Multiple pathways of inositol polyphosphate metabolism in angiotensin-stimulated adrenal glomerulosa cells. J Biol Chem 263(9):4083–4091
Balla A, Kim YJ, Varnai P, Szentpetery Z, Knight Z, Shokat KM, Balla T (2008) Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIalpha. Mol Biol Cell 19(2):711–721. https://doi.org/10.1091/mbc.E07-07-0713
Bankaitis VA, Malehorn DE, Emr SD, Greene R (1989) The Saccharomyces cerevisiae SEC14 gene encodes a cytosolic factor that is required for transport of secretory proteins from the yeast Golgi complex. J Cell Biol 108(4):1271–1281
Bankaitis VA, Aitken JR, Cleves AE, Dowhan W (1990) An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347(6293):561–562. https://doi.org/10.1083/347561a0
Bankaitis VA, Mousley CJ, Schaaf G (2010) The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem Sci 35(3):150–160. https://doi.org/10.1016/j.tibs.2009.10.008
Baraldi E, Djinovic Carugo K, Hyvonen M, Surdo PL, Riley AM, Potter BV, O’Brien R, Ladbury JE, Saraste M (1999) Structure of the PH domain from Bruton’s tyrosine kinase in complex with inositol 1,3,4,5-tetrakisphosphate. Structure 7(4):449–460
Barelli H, Antonny B (2016) Lipid unsaturation and organelle dynamics. Curr Opin Cell Biol 41:25–32. https://doi.org/10.1016/j.ceb.2016.03.012
Barlow CA, Laishram RS, Anderson RA (2010) Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol 20(1):25–35. https://doi.org/10.1016/j.tcb.2009.09.009
Barrera NP, Zhou M, Robinson CV (2013) The role of lipids in defining membrane protein interactions: insights from mass spectrometry. Trends Cell Biol 23(1):1–8. https://doi.org/10.1016/j.tcb.2012.08.007
Baskaran S, Ragusa MJ, Boura E, Hurley JH (2012) Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol Cell 47(3):339–348. https://doi.org/10.1016/j.molcel.2012.05.027
Baumgart T, Capraro BR, Zhu C, Das SL (2011) Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu Rev Phys Chem 62:483–506. https://doi.org/10.1146/annurev.physchem.012809.103450
Begley MJ, Dixon JE (2005) The structure and regulation of myotubularin phosphatases. Curr Opin Struct Biol 15(6):614–620. https://doi.org/10.1016/j.sbi.2005.10.016
Begley MJ, Taylor GS, Kim SA, Veine DM, Dixon JE, Stuckey JA (2003) Crystal structure of a phosphoinositide phosphatase, MTMR2: insights into myotubular myopathy and Charcot-Marie-Tooth syndrome. Mol Cell 12(6):1391–1402
Begley MJ, Taylor GS, Brock MA, Ghosh P, Woods VL, Dixon JE (2006) Molecular basis for substrate recognition by MTMR2, a myotubularin family phosphoinositide phosphatase. Proc Natl Acad Sci U S A 103(4):927–932. https://doi.org/10.1073/pnas.0510006103
Berger P, Schaffitzel C, Berger I, Ban N, Suter U (2003) Membrane association of myotubularin-related protein 2 is mediated by a pleckstrin homology-GRAM domain and a coiled-coil dimerization module. Proc Natl Acad Sci U S A 100(21):12177–12182. https://doi.org/10.1073/pnas.2132732100
Bezanilla M, Gladfelter AS, Kovar DR, Lee WL (2015) Cytoskeletal dynamics: a view from the membrane. J Cell Biol 209(3):329–337. https://doi.org/10.1083/jcb.201502062
Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23(5):886–895. https://doi.org/10.1016/j.devcel.2012.10.009
Bittova L, Sumandea M, Cho W (1999) A structure-function study of the C2 domain of cytosolic phospholipase A2. Identification of essential calcium ligands and hydrophobic membrane binding residues. J Biol Chem 274(14):9665–9672
Blomberg N, Nilges M (1997) Functional diversity of PH domains: an exhaustive modelling study. Fold Des 2(6):343–355. https://doi.org/10.1016/S1359-0278(97)00048-5
Blomberg N, Baraldi E, Nilges M, Saraste M (1999) The PH superfold: a structural scaffold for multiple functions. Trends Biochem Sci 24(11):441–445
Boggon TJ, Shan WS, Santagata S, Myers SC, Shapiro L (1999) Implication of tubby proteins as transcription factors by structure-based functional analysis. Science 286(5447):2119–2125
Bojjireddy N, Botyanszki J, Hammond G, Creech D, Peterson R, Kemp DC, Snead M, Brown R, Morrison A, Wilson S, Harrison S, Moore C, Balla T (2014) Pharmacological and genetic targeting of the PI4KA enzyme reveals its important role in maintaining plasma membrane phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate levels. J Biol Chem 289(9):6120–6132. https://doi.org/10.1074/jbc.M113.531426
Bompard G, Martin M, Roy C, Vignon F, Freiss G (2003) Membrane targeting of protein tyrosine phosphatase PTPL1 through its FERM domain via binding to phosphatidylinositol 4,5-biphosphate. J Cell Sci 116(Pt 12):2519–2530. https://doi.org/10.1242/jcs.00448
Bonangelino CJ, Nau JJ, Duex JE, Brinkman M, Wurmser AE, Gary JD, Emr SD, Weisman LS (2002) Osmotic stress-induced increase of phosphatidylinositol 3,5-bisphosphate requires Vac14p, an activator of the lipid kinase Fab1p. J Cell Biol 156(6):1015–1028. https://doi.org/10.1083/jcb.200201002
Botelho RJ (2009) Changing phosphoinositides “on the fly”: how trafficking vesicles avoid an identity crisis. BioEssays 31(10):1127–1136. https://doi.org/10.1002/bies.200900060
Boucrot E, Ferreira AP, Almeida-Souza L, Debard S, Vallis Y, Howard G, Bertot L, Sauvonnet N, McMahon HT (2015) Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517(7535):460–465. https://doi.org/10.1038/nature14067
Boura E, Nencka R (2015) Phosphatidylinositol 4-kinases: function, structure, and inhibition. Exp Cell Res 337(2):136–145. https://doi.org/10.1016/j.yexcr.2015.03.028
Braccini L, Ciraolo E, Campa CC, Perino A, Longo DL, Tibolla G, Pregnolato M, Cao Y, Tassone B, Damilano F, Laffargue M, Calautti E, Falasca M, Norata GD, Backer JM, Hirsch E (2015) PI3K-C2gamma is a Rab5 effector selectively controlling endosomal Akt2 activation downstream of insulin signalling. Nat Commun 6:7400. https://doi.org/10.1038/ncomms8400
Bravo J, Karathanassis D, Pacold CM, Pacold ME, Ellson CD, Anderson KE, Butler PJ, Lavenir I, Perisic O, Hawkins PT, Stephens L, Williams RL (2001) The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol Cell 8(4):829–839
Brombacher E, Urwyler S, Ragaz C, Weber SS, Kami K, Overduin M, Hilbi H (2009) Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J Biol Chem 284(8):4846–4856. https://doi.org/10.1074/jbc.M807505200
Brunecky R, Lee S, Rzepecki PW, Overduin M, Prestwich GD, Kutateladze AG, Kutateladze TG (2005) Investigation of the binding geometry of a peripheral membrane protein. Biochemistry 44(49):16064–16071. https://doi.org/10.1021/bi051127+
Bunney TD, Katan M (2010) Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 10(5):342–352. https://doi.org/10.1038/nrc2842
Burd CG, Emr SD (1998) Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 2(1):157–162
Burke JE, Williams RL (2015) Synergy in activating class I PI3Ks. Trends Biochem Sci 40(2):88–100. https://doi.org/10.1016/j.tibs.2014.12.003
Busse RA, Scacioc A, Krick R, Perez-Lara A, Thumm M, Kuhnel K (2015) Characterization of PROPPIN-Phosphoinositide binding and role of loop 6CD in PROPPIN-Membrane binding. Biophys J 108(9):2223–2234. https://doi.org/10.1016/j.bpj.2015.03.045
Callaghan J, Simonsen A, Gaullier JM, Toh BH, Stenmark H (1999) The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer. Biochem J 338(Pt 2):539–543
Calleja V, Alcor D, Laguerre M, Park J, Vojnovic B, Hemmings BA, Downward J, Parker PJ, Larijani B (2007) Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS Biol 5(4):e95. https://doi.org/10.1371/journal.pbio.0050095
Calleja V, Laguerre M, Larijani B (2009a) 3-D structure and dynamics of protein kinase B-new mechanism for the allosteric regulation of an AGC kinase. J Chem Biol 2(1):11–25. https://doi.org/10.1007/s12154-009-0016-8
Calleja V, Laguerre M, Parker PJ, Larijani B (2009b) Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition. PLoS Biol 7(1):e17. https://doi.org/10.1371/journal.pbio.1000017
Calleja V, Laguerre M, Larijani B (2012) Role of the C-terminal regulatory domain in the allosteric inhibition of PKB/Akt. Adv Biol Regul 52(1):46–57. https://doi.org/10.1016/j.advenzreg.2011.09.009
Campa F, Yoon HY, Ha VL, Szentpetery Z, Balla T, Randazzo PA (2009) A PH domain in the Arf GTPase-activating protein (GAP) ARAP1 binds phosphatidylinositol 3,4,5-trisphosphate and regulates Arf GAP activity independently of recruitment to the plasma membranes. J Biol Chem 284(41):28069–28083. https://doi.org/10.1074/jbc.M109.028266
Campbell RB, Liu F, Ross AH (2003) Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 278(36):33617–33620. https://doi.org/10.1074/jbc.C300296200
Carlton JG, Cullen PJ (2005) Coincidence detection in phosphoinositide signaling. Trends Cell Biol 15(10):540–547. https://doi.org/10.1016/j.tcb.2005.08.005
Carroll K, Gomez C, Shapiro L (2004) Tubby proteins: the plot thickens. Nat Rev Mol Cell Biol 5(1):55–63. https://doi.org/10.1038/nrm1278
Cash JN, Davis EM, Tesmer JJG (2016) Structural and biochemical characterization of the catalytic core of the metastatic factor P-Rex1 and its regulation by Ptdins(3,4,5)P3. Structure 24(5):730–740. https://doi.org/10.1016/j.str.2016.02.022
Ceccarelli DF, Song HK, Poy F, Schaller MD, Eck MJ (2006) Crystal structure of the FERM domain of focal adhesion kinase. J Biol Chem 281(1):252–259. https://doi.org/10.1074/jbc.M509188200
Ceccarelli DF, Blasutig IM, Goudreault M, Li Z, Ruston J, Pawson T, Sicheri F (2007) Non-canonical interaction of phosphoinositides with pleckstrin homology domains of Tiam1 and ArhGAP9. J Biol Chem 282(18):13864–13874. https://doi.org/10.1074/jbc.M700505200
Chan KC, Lu L, Sun F, Fan J (2017) Molecular details of the PH domain of ACAP1(BAR-PH) protein binding to PIP-containing membrane. J Phys Chem B 121(15):3586–3596. https://doi.org/10.1021/acs.jpcb.6b09563
Chang CL, Liou J (2015) Phosphatidylinositol 4,5-bisphosphate homeostasis regulated by Nir2 and Nir3 proteins at endoplasmic reticulum-plasma membrane junctions. J Biol Chem 290(23):14289–14301. https://doi.org/10.1074/jbc.M114.621375
Chang BH, Gujral TS, Karp ES, BuKhalid R, Grantcharova VP, MacBeath G (2011) A systematic family-wide investigation reveals that ~30% of mammalian PDZ domains engage in PDZ-PDZ interactions. Chem Biol 18(9):1143–1152. https://doi.org/10.1016/j.chembiol.2011.06.013
Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB, Volk E, Liao JC, Liou J (2013) Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5(3):813–825. https://doi.org/10.1016/j.celrep.2013.09.038
Charman M, Colbourne TR, Pietrangelo A, Kreplak L, Ridgway ND (2014) Oxysterol-binding protein (OSBP)-related protein 4 (ORP4) is essential for cell proliferation and survival. J Biol Chem 289(22):15705–15717. https://doi.org/10.1074/jbc.M114.571216
Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M (2001) Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat Cell Biol 3(7):613–618. https://doi.org/10.1038/35083000
Cheever ML, Kutateladze TG, Overduin M (2006) Increased mobility in the membrane targeting PX domain induced by phosphatidylinositol 3-phosphate. Protein Sci 15(8):1873–1882. https://doi.org/10.1110/ps.062194906
Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394(6695):793–797. https://doi.org/10.1038/29555
Chen Y, Sheng R, Kallberg M, Silkov A, Tun MP, Bhardwaj N, Kurilova S, Hall RA, Honig B, Lu H, Cho W (2012) Genome-wide functional annotation of dual-specificity protein- and lipid-binding modules that regulate protein interactions. Mol Cell 46(2):226–237. https://doi.org/10.1016/j.molcel.2012.02.012
Chergui M (2016) Time-resolved X-ray spectroscopies of chemical systems: new perspectives. Struct Dyn 3(3):031001. https://doi.org/10.1063/1.4953104
Chiapparino A, Maeda K, Turei D, Saez-Rodriguez J, Gavin AC (2016) The orchestra of lipid-transfer proteins at the crossroads between metabolism and signaling. Prog Lipid Res 61:30–39. https://doi.org/10.1016/j.plipres.2015.10.004
Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M, Jindal H, Liu SC, Low PS, Rouleau GA, Mohandas N, Chasis JA, Conboy JG, Gascard P, Takakuwa Y, Huang SC, Benz EJ Jr, Bretscher A, Fehon RG, Gusella JF, Ramesh V, Solomon F, Marchesi VT, Tsukita S, Tsukita S, Hoover KB et al (1998) The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23(8):281–282
Cho W, Stahelin RV (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 34:119–151. https://doi.org/10.1146/annurev.biophys.33.110502.133337
Cho W, Stahelin RV (2006) Membrane binding and subcellular targeting of C2 domains. Biochim Biophys Acta 1761(8):838–849. https://doi.org/10.1016/j.bbalip.2006.06.014
Choi S, Thapa N, Tan X, Hedman AC, Anderson RA (2015) PIP kinases define PI4,5P(2)signaling specificity by association with effectors. Biochim Biophys Acta 1851(6):711–723. https://doi.org/10.1016/j.bbalip.2015.01.009
Choi S, Hedman AC, Sayedyahossein S, Thapa N, Sacks DB, Anderson RA (2016) Agonist-stimulated phosphatidylinositol-3,4,5-trisphosphate generation by scaffolded phosphoinositide kinases. Nat Cell Biol 18(12):1324–1335. https://doi.org/10.1038/ncb3441
Choy CH, Han BK, Botelho RJ (2017) Phosphoinositide diversity, distribution, and effector function: stepping out of the box. BioEssays 39(12). https://doi.org/10.1002/bies.201700121
Chung SH, Song WJ, Kim K, Bednarski JJ, Chen J, Prestwich GD, Holz RW (1998) The C2 domains of Rabphilin3A specifically bind phosphatidylinositol 4,5-bisphosphate containing vesicles in a Ca2+−dependent manner. In vitro characteristics and possible significance. J Biol Chem 273(17):10240–10248
Chung J, Torta F, Masai K, Lucast L, Czapla H, Tanner LB, Narayanaswamy P, Wenk MR, Nakatsu F, De Camilli P (2015) Intracellular transport. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349(6246):428–432. https://doi.org/10.1126/science.aab1370
Cicchetti G, Maurer P, Wagener P, Kocks C (1999) Actin and phosphoinositide binding by the ActA protein of the bacterial pathogen Listeria monocytogenes. J Biol Chem 274(47):33616–33626
Clague MJ, Lorenzo O (2005) The myotubularin family of lipid phosphatases. Traffic 6(12):1063–1069. https://doi.org/10.1111/j.1600-0854.2005.00338.x
Cleves A, McGee T, Bankaitis V (1991) Phospholipid transfer proteins: a biological debut. Trends Cell Biol 1(1):30–34
Cockcroft S (1999) Mammalian phosphatidylinositol transfer proteins: emerging roles in signal transduction and vesicular traffic. Chem Phys Lipids 98(1–2):23–33
Cockcroft S (2012) The diverse functions of phosphatidylinositol transfer proteins. Curr Top Microbiol Immunol 362:185–208. https://doi.org/10.1007/978-94-007-5025-8_9
Cockcroft S, Carvou N (2007) Biochemical and biological functions of class I phosphatidylinositol transfer proteins. Biochim Biophys Acta 1771(6):677–691. https://doi.org/10.1016/j.bbalip.2007.03.009
Corbalan-Garcia S, Gomez-Fernandez JC (2014a) Classical protein kinases C are regulated by concerted interaction with lipids: the importance of phosphatidylinositol-4,5-bisphosphate. Biophys Rev 6(1):3–14. https://doi.org/10.1007/s12551-013-0125-z
Corbalan-Garcia S, Gomez-Fernandez JC (2014b) Signaling through C2 domains: more than one lipid target. Biochim Biophys Acta 1838(6):1536–1547. https://doi.org/10.1016/j.bbamem.2014.01.008
Coudevylle N, Montaville P, Leonov A, Zweckstetter M, Becker S (2008) Structural determinants for Ca2+ and phosphatidylinositol 4,5-bisphosphate binding by the C2A domain of rabphilin-3A. J Biol Chem 283(51):35918–35928. https://doi.org/10.1074/jbc.M804094200
Cozier GE, Carlton J, Bouyoucef D, Cullen PJ (2004) Membrane targeting by pleckstrin homology domains. Curr Top Microbiol Immunol 282:49–88
Crowder MK, Seacrist CD, Blind RD (2017) Phospholipid regulation of the nuclear receptor superfamily. Adv Biol Regul 63:6–14. https://doi.org/10.1016/j.jbior.2016.10.006
Cullen PJ, Cozier GE, Banting G, Mellor H (2001) Modular phosphoinositide-binding domains--their role in signalling and membrane trafficking. Curr Biol 11(21):R882–R893
Daste F, Walrant A, Holst MR, Gadsby JR, Mason J, Lee JE, Brook D, Mettlen M, Larsson E, Lee SF, Lundmark R, Gallop JL (2017) Control of actin polymerization via the coincidence of phosphoinositides and high membrane curvature. J Cell Biol 216(11):3745–3765. https://doi.org/10.1083/jcb.201704061
Davletov B, Perisic O, Williams RL (1998) Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically. J Biol Chem 273(30):19093–19096. https://doi.org/10.1074/jbc.273.30.19093
De Camilli P, Chen H, Hyman J, Panepucci E, Bateman A, Brunger AT (2002) The ENTH domain. FEBS Lett 513(1):11–18
De Matteis M, Godi A, Corda D (2002) Phosphoinositides and the golgi complex. Curr Opin Cell Biol 14(4):434–447
de Saint-Jean M, Delfosse V, Douguet D, Chicanne G, Payrastre B, Bourguet W, Antonny B, Drin G (2011) Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers. J Cell Biol 195(6):965–978. https://doi.org/10.1083/jcb.201104062
de Vries KJ, Heinrichs AA, Cunningham E, Brunink F, Westerman J, Somerharju PJ, Cockcroft S, Wirtz KW, Snoek GT (1995) An isoform of the phosphatidylinositol-transfer protein transfers sphingomyelin and is associated with the Golgi system. Biochem J 310(Pt 2):643–649
De Vries KJ, Westerman J, Bastiaens PI, Jovin TM, Wirtz KW, Snoek GT (1996) Fluorescently labeled phosphatidylinositol transfer protein isoforms (alpha and beta), microinjected into fetal bovine heart endothelial cells, are targeted to distinct intracellular sites. Exp Cell Res 227(1):33–39. https://doi.org/10.1006/excr.1996.0246
Del Campo CM, Mishra AK, Wang YH, Roy CR, Janmey PA, Lambright DG (2014) Structural basis for PI(4)P-specific membrane recruitment of the Legionella pneumophila effector DrrA/SidM. Structure 22(3):397–408. https://doi.org/10.1016/j.str.2013.12.018
Dhe-Paganon S, Ottinger EA, Nolte RT, Eck MJ, Shoelson SE (1999) Crystal structure of the pleckstrin homology-phosphotyrosine binding (PH-PTB) targeting region of insulin receptor substrate 1. Proc Natl Acad Sci U S A 96(15):8378–8383
Di Lello P, Nguyen BD, Jones TN, Potempa K, Kobor MS, Legault P, Omichinski JG (2005) NMR structure of the amino-terminal domain from the Tfb1 subunit of TFIIH and characterization of its phosphoinositide and VP16 binding sites. Biochemistry 44(21):7678–7686. https://doi.org/10.1021/bi050099s
DiNitto JP, Lambright DG (2006) Membrane and juxtamembrane targeting by PH and PTB domains. Biochim Biophys Acta 1761(8):850–867. https://doi.org/10.1016/j.bbalip.2006.04.008
DiNitto JP, Delprato A, Gabe Lee MT, Cronin TC, Huang S, Guilherme A, Czech MP, Lambright DG (2007) Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. Mol Cell 28(4):569–583. https://doi.org/10.1016/j.molcel.2007.09.017
Diraviyam K, Stahelin RV, Cho W, Murray D (2003) Computer modeling of the membrane interaction of FYVE domains. J Mol Biol 328(3):721–736
Doerks T, Strauss M, Brendel M, Bork P (2000) GRAM, a novel domain in glucosyltransferases, myotubularins and other putative membrane-associated proteins. Trends Biochem Sci 25(10):483–485
Dornan GL, McPhail JA, Burke JE (2016) Type III phosphatidylinositol 4 kinases: structure, function, regulation, signalling and involvement in disease. Biochem Soc Trans 44(1):260–266. https://doi.org/10.1042/BST20150219
Dove SK, Piper RC, McEwen RK, Yu JW, King MC, Hughes DC, Thuring J, Holmes AB, Cooke FT, Michell RH, Parker PJ, Lemmon MA (2004) Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J 23(9):1922–1933. https://doi.org/10.1038/sj.emboj.7600203
Drin G (2014) Topological regulation of lipid balance in cells. Annu Rev Biochem 83:51–77. https://doi.org/10.1146/annurev-biochem-060713-035307
Dror RO, Dirks RM, Grossman JP, Xu H, Shaw DE (2012) Biomolecular simulation: a computational microscope for molecular biology. Annu Rev Biophys 41:429–452. https://doi.org/10.1146/annurev-biophys-042910-155245
Du X, Kumar J, Ferguson C, Schulz TA, Ong YS, Hong W, Prinz WA, Parton RG, Brown AJ, Yang H (2011) A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J Cell Biol 192(1):121–135. https://doi.org/10.1083/jcb.201004142
Dumas JJ, Merithew E, Sudharshan E, Rajamani D, Hayes S, Lawe D, Corvera S, Lambright DG (2001) Multivalent endosome targeting by homodimeric EEA1. Mol Cell 8(5):947–958
Duning K, Wennmann DO, Bokemeyer A, Reissner C, Wersching H, Thomas C, Buschert J, Guske K, Franzke V, Floel A, Lohmann H, Knecht S, Brand SM, Poter M, Rescher U, Missler M, Seelheim P, Propper C, Boeckers TM, Makuch L, Huganir R, Weide T, Brand E, Pavenstadt H, Kremerskothen J (2013) Common exonic missense variants in the C2 domain of the human KIBRA protein modify lipid binding and cognitive performance. Transl Psychiatry 3:e272. https://doi.org/10.1038/tp.2013.49
Dyson JM, Fedele CG, Davies EM, Becanovic J, Mitchell CA (2012) Phosphoinositide phosphatases: just as important as the kinases. Subcell Biochem 58:215–279. https://doi.org/10.1007/978-94-007-3012-0_7
Ebner M, Lucic I, Leonard TA, Yudushkin I (2017) PI(3,4,5)P3 engagement restricts Akt activity to cellular membranes. Mol Cell 65(3):416–431 e416. https://doi.org/10.1016/j.molcel.2016.12.028
Edwards SD, Keep NH (2001) The 2.7 A crystal structure of the activated FERM domain of moesin: an analysis of structural changes on activation. Biochemistry 40(24):7061–7068
Egea-Jimenez AL, Gallardo R, Garcia-Pino A, Ivarsson Y, Wawrzyniak AM, Kashyap R, Loris R, Schymkowitz J, Rousseau F, Zimmermann P (2016) Frizzled 7 and PIP2 binding by syntenin PDZ2 domain supports Frizzled 7 trafficking and signalling. Nat Commun 7:12101. https://doi.org/10.1038/ncomms12101
Eisenberg-Bord M, Shai N, Schuldiner M, Bohnert M (2016) A tether is a tether is a tether: tethering at membrane contact sites. Dev Cell 39(4):395–409. https://doi.org/10.1016/j.devcel.2016.10.022
Ellson CD, Gobert-Gosse S, Anderson KE, Davidson K, Erdjument-Bromage H, Tempst P, Thuring JW, Cooper MA, Lim ZY, Holmes AB, Gaffney PR, Coadwell J, Chilvers ER, Hawkins PT, Stephens LR (2001) PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox). Nat Cell Biol 3(7):679–682. https://doi.org/10.1038/35083076
Emptage RP, Lemmon MA, Ferguson KM (2017a) Molecular determinants of KA1 domain-mediated autoinhibition and phospholipid activation of MARK1 kinase. Biochem J 474(3):385–398. https://doi.org/10.1042/BCJ20160792
Emptage RP, Schoenberger MJ, Ferguson KM, Marmorstein R (2017b) Intramolecular autoinhibition of checkpoint kinase 1 is mediated by conserved basic motifs of the C-terminal kinase associated-1 domain. J Biol Chem 292(46):19024–19033. https://doi.org/10.1074/jbc.M117.811265
Endo M, Shirouzu M, Yokoyama S (2003) The Cdc42 binding and scaffolding activities of the fission yeast adaptor protein Scd2. J Biol Chem 278(2):843–852. https://doi.org/10.1074/jbc.M209714200
Erneux C, Edimo WE, Deneubourg L, Pirson I (2011) SHIP2 multiple functions: a balance between a negative control of PtdIns(3,4,5)P(3) level, a positive control of PtdIns(3,4)P(2) production, and intrinsic docking properties. J Cell Biochem 112(9):2203–2209. https://doi.org/10.1002/jcb.23146
Ernst A, Appleton BA, Ivarsson Y, Zhang Y, Gfeller D, Wiesmann C, Sidhu SS (2014) A structural portrait of the PDZ domain family. J Mol Biol 426(21):3509–3519. https://doi.org/10.1016/j.jmb.2014.08.012
Falasca M, Hughes WE, Dominguez V, Sala G, Fostira F, Fang MQ, Cazzolli R, Shepherd PR, James DE, Maffucci T (2007) The role of phosphoinositide 3-kinase C2alpha in insulin signaling. J Biol Chem 282(38):28226–28236. https://doi.org/10.1074/jbc.M704357200
Ferguson KM, Lemmon MA, Schlessinger J, Sigler PB (1994) Crystal structure at 2.2 A resolution of the pleckstrin homology domain from human dynamin. Cell 79(2):199–209
Ferguson KM, Lemmon MA, Schlessinger J, Sigler PB (1995) Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell 83(6):1037–1046
Ferguson KM, Kavran JM, Sankaran VG, Fournier E, Isakoff SJ, Skolnik EY, Lemmon MA (2000) Structural basis for discrimination of 3-phosphoinositides by pleckstrin homology domains. Mol Cell 6(2):373–384
Fernandes F, Coutinho A, Prieto M, Loura LM (2015) Electrostatically driven lipid-protein interaction: answers from FRET. Biochim Biophys Acta 1848(9):1837–1848. https://doi.org/10.1016/j.bbamem.2015.02.023
Flesch FM, Yu JW, Lemmon MA, Burger KN (2005) Membrane activity of the phospholipase C-delta1 pleckstrin homology (PH) domain. Biochem J 389(Pt 2):435–441. https://doi.org/10.1042/BJ20041721
Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ, Gibson A, Hopkins CR, Evans PR, McMahon HT (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291(5506):1051–1055. https://doi.org/10.1126/science.291.5506.1051
Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, Evans PR, McMahon HT (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419(6905):361–366. https://doi.org/10.1038/nature01020
Frame MC, Patel H, Serrels B, Lietha D, Eck MJ (2010) The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 11(11):802–814. https://doi.org/10.1038/nrm2996
Franco I, Gulluni F, Campa CC, Costa C, Margaria JP, Ciraolo E, Martini M, Monteyne D, De Luca E, Germena G, Posor Y, Maffucci T, Marengo S, Haucke V, Falasca M, Perez-Morga D, Boletta A, Merlo GR, Hirsch E (2014) PI3K class II alpha controls spatially restricted endosomal PtdIns3P and Rab11 activation to promote primary cilium function. Dev Cell 28(6):647–658. https://doi.org/10.1016/j.devcel.2014.01.022
Frazier AA, Wisner MA, Malmberg NJ, Victor KG, Fanucci GE, Nalefski EA, Falke JJ, Cafiso DS (2002) Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry 41(20):6282–6292
Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137(2):191–196. https://doi.org/10.1016/j.cell.2009.04.010
Funderburk SF, Wang QJ, Yue Z (2010) The Beclin 1-VPS34 complex--at the crossroads of autophagy and beyond. Trends Cell Biol 20(6):355–362. https://doi.org/10.1016/j.tcb.2010.03.002
Gallardo R, Ivarsson Y, Schymkowitz J, Rousseau F, Zimmermann P (2010) Structural diversity of PDZ-lipid interactions. Chembiochem 11(4):456–467. https://doi.org/10.1002/cbic.200900616
Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, Langen R, McMahon HT (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25(12):2898–2910. https://doi.org/10.1038/sj.emboj.7601174
Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Cafiso DS, Wang J, Murray D, Pentyala SN, Smith SO, McLaughlin S (2004) Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86(4):2188–2207. https://doi.org/10.1016/S0006-3495(04)74278-2
Gamper N, Shapiro MS (2007) Regulation of ion transport proteins by membrane phosphoinositides. Nat Rev Neurosci 8(12):921–934. https://doi.org/10.1038/nrn2257
Garner K, Hunt AN, Koster G, Somerharju P, Groves E, Li M, Raghu P, Holic R, Cockcroft S (2012) Phosphatidylinositol transfer protein, cytoplasmic 1 (PITPNC1) binds and transfers phosphatidic acid. J Biol Chem 287(38):32263–32276. https://doi.org/10.1074/jbc.M112.375840
Gary JD, Wurmser AE, Bonangelino CJ, Weisman LS, Emr SD (1998) Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 143(1):65–79
Gaullier JM, Simonsen A, D’Arrigo A, Bremnes B, Stenmark H, Aasland R (1998) FYVE fingers bind PtdIns(3)P. Nature 394(6692):432–433. https://doi.org/10.1038/28767
Ghai R, Du X, Wang H, Dong J, Ferguson C, Brown AJ, Parton RG, Wu JW, Yang H (2017) ORP5 and ORP8 bind phosphatidylinositol-4, 5-biphosphate (PtdIns(4,5)P 2) and regulate its level at the plasma membrane. Nat Commun 8(1):757. https://doi.org/10.1038/s41467-017-00861-5
Gil JE, Kim E, Kim IS, Ku B, Park WS, Oh BH, Ryu SH, Cho W, Heo WD (2012) Phosphoinositides differentially regulate protrudin localization through the FYVE domain. J Biol Chem 287(49):41268–41276. https://doi.org/10.1074/jbc.M112.419127
Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19(17):4577–4588. https://doi.org/10.1093/emboj/19.17.4577
Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153(7):1494–1509. https://doi.org/10.1016/j.cell.2013.05.026
Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA (1999) ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat Cell Biol 1(5):280–287. https://doi.org/10.1038/12993
Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 6(5):393–404. https://doi.org/10.1038/ncb1119
Grabon A, Khan D, Bankaitis VA (2015) Phosphatidylinositol transfer proteins and instructive regulation of lipid kinase biology. Biochim Biophys Acta 1851(6):724–735. https://doi.org/10.1016/j.bbalip.2014.12.011
Grabon A, Orlowski A, Tripathi A, Vuorio J, Javanainen M, Rog T, Lonnfors M, McDermott MI, Siebert G, Somerharju P, Vattulainen I, Bankaitis VA (2017) Dynamics and energetics of the mammalian phosphatidylinositol transfer protein phospholipid exchange cycle. J Biol Chem 292(35):14438–14455. https://doi.org/10.1074/jbc.M117.791467
Grobler JA, Essen LO, Williams RL, Hurley JH (1996) C2 domain conformational changes in phospholipase C-delta 1. Nat Struct Biol 3(9):788–795
Guerrero-Valero M, Ferrer-Orta C, Querol-Audi J, Marin-Vicente C, Fita I, Gomez-Fernandez JC, Verdaguer N, Corbalan-Garcia S (2009) Structural and mechanistic insights into the association of PKCalpha-C2 domain to PtdIns(4,5)P2. Proc Natl Acad Sci U S A 106(16):6603–6607. https://doi.org/10.1073/pnas.0813099106
Guillen J, Ferrer-Orta C, Buxaderas M, Perez-Sanchez D, Guerrero-Valero M, Luengo-Gil G, Pous J, Guerra P, Gomez-Fernandez JC, Verdaguer N, Corbalan-Garcia S (2013) Structural insights into the Ca2+ and PI(4,5)P2 binding modes of the C2 domains of rabphilin 3A and synaptotagmin 1. Proc Natl Acad Sci U S A 110(51):20503–20508. https://doi.org/10.1073/pnas.1316179110
Gulyas G, Radvanszki G, Matuska R, Balla A, Hunyady L, Balla T, Varnai P (2017) Plasma membrane phosphatidylinositol 4-phosphate and 4,5-bisphosphate determine the distribution and function of K-Ras4B but not H-Ras proteins. J Biol Chem 292(46):18862–18877. https://doi.org/10.1074/jbc.M117.806679
Ham H, Sreelatha A, Orth K (2011) Manipulation of host membranes by bacterial effectors. Nat Rev Microbiol 9(9):635–646. https://doi.org/10.1038/nrmicro2602
Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T (2000) Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J 19(17):4449–4462. https://doi.org/10.1093/emboj/19.17.4449
Hammond GR, Balla T (2015) Polyphosphoinositide binding domains: key to inositol lipid biology. Biochim Biophys Acta 1851(6):746–758. https://doi.org/10.1016/j.bbalip.2015.02.013
Hammond GR, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T, Irvine RF (2012) PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337(6095):727–730. https://doi.org/10.1126/science.1222483
Hammond GR, Machner MP, Balla T (2014) A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J Cell Biol 205(1):113–126. https://doi.org/10.1083/jcb.201312072
Hammond GR, Takasuga S, Sasaki T, Balla T (2015) The ML1Nx2 phosphatidylinositol 3,5-bisphosphate probe shows poor selectivity in cells. PLoS One 10(10):e0139957. https://doi.org/10.1371/journal.pone.0139957
Handa Y, Suzuki M, Ohya K, Iwai H, Ishijima N, Koleske AJ, Fukui Y, Sasakawa C (2007) Shigella IpgB1 promotes bacterial entry through the ELMO-Dock180 machinery. Nat Cell Biol 9(1):121–128. https://doi.org/10.1038/ncb1526
Harlan JE, Hajduk PJ, Yoon HS, Fesik SW (1994) Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371(6493):168–170. https://doi.org/10.1038/371168a0
Haslam RJ, Koide HB, Hemmings BA (1993) Pleckstrin domain homology. Nature 363(6427):309–310. https://doi.org/10.1038/363309b0
Hawkins PT, Stephens LR (2016) Emerging evidence of signalling roles for PI(3,4)P2 in Class I and II PI3K-regulated pathways. Biochem Soc Trans 44(1):307–314. https://doi.org/10.1042/BST20150248
Hawkins PT, Jackson TR, Stephens LR (1992) Platelet-derived growth factor stimulates synthesis of PtdIns(3,4,5)P3 by activating a PtdIns(4,5)P2 3-OH kinase. Nature 358(6382):157–159. https://doi.org/10.1038/358157a0
Hayakawa A, Hayes SJ, Lawe DC, Sudharshan E, Tuft R, Fogarty K, Lambright D, Corvera S (2004) Structural basis for endosomal targeting by FYVE domains. J Biol Chem 279(7):5958–5966. https://doi.org/10.1074/jbc.M310503200
He J, Haney RM, Vora M, Verkhusha VV, Stahelin RV, Kutateladze TG (2008) Molecular mechanism of membrane targeting by the GRP1 PH domain. J Lipid Res 49(8):1807–1815. https://doi.org/10.1194/jlr.M800150-JLR200
He J, Vora M, Haney RM, Filonov GS, Musselman CA, Burd CG, Kutateladze AG, Verkhusha VV, Stahelin RV, Kutateladze TG (2009) Membrane insertion of the FYVE domain is modulated by pH. Proteins 76(4):852–860. https://doi.org/10.1002/prot.22392
Hedger G, Sansom MSP (2016) Lipid interaction sites on channels, transporters and receptors: recent insights from molecular dynamics simulations. Biochim Biophys Acta 1858(10):2390–2400. https://doi.org/10.1016/j.bbamem.2016.02.037
Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314(5804):1458–1461. https://doi.org/10.1126/science.1134389
Hertig S, Latorraca NR, Dror RO (2016) Revealing atomic-level mechanisms of protein allostery with molecular dynamics simulations. PLoS Comput Biol 12(6):e1004746. https://doi.org/10.1371/journal.pcbi.1004746
Hilgemann DW, Ball R (1996) Regulation of cardiac Na+,Ca2+ exchange and KATP potassium channels by PIP2. Science 273(5277):956–959
Hilgemann DW, Feng S, Nasuhoglu C (2001) The complex and intriguing lives of PIP2 with ion channels and transporters. Sci STKE 2001(111):re19. https://doi.org/10.1126/stke.2001.111.re19
Hill K, Krugmann S, Andrews SR, Coadwell WJ, Finan P, Welch HC, Hawkins PT, Stephens LR (2005) Regulation of P-Rex1 by phosphatidylinositol (3,4,5)-trisphosphate and Gbetagamma subunits. J Biol Chem 280(6):4166–4173. https://doi.org/10.1074/jbc.M411262200
Hille B, Dickson EJ, Kruse M, Vivas O, Suh BC (2015) Phosphoinositides regulate ion channels. Biochim Biophys Acta 1851(6):844–856. https://doi.org/10.1016/j.bbalip.2014.09.010
Hirano S, Suzuki N, Slagsvold T, Kawasaki M, Trambaiolo D, Kato R, Stenmark H, Wakatsuki S (2006) Structural basis of ubiquitin recognition by mammalian Eap45 GLUE domain. Nat Struct Mol Biol 13(11):1031–1032. https://doi.org/10.1038/nsmb1163
Hiroaki H, Ago T, Ito T, Sumimoto H, Kohda D (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat Struct Biol 8(6):526–530. https://doi.org/10.1038/88591
Hnia K, Vaccari I, Bolino A, Laporte J (2012) Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology. Trends Mol Med 18(6):317–327. https://doi.org/10.1016/j.molmed.2012.04.004
Holthuis JC, Menon AK (2014) Lipid landscapes and pipelines in membrane homeostasis. Nature 510(7503):48–57. https://doi.org/10.1038/nature13474
Honigmann A, van den Bogaart G, Iraheta E, Risselada HJ, Milovanovic D, Mueller V, Mullar S, Diederichsen U, Fasshauer D, Grubmuller H, Hell SW, Eggeling C, Kuhnel K, Jahn R (2013) Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat Struct Mol Biol 20(6):679–686. https://doi.org/10.1038/nsmb.2570
Hospital A, Goni JR, Orozco M, Gelpi JL (2015) Molecular dynamics simulations: advances and applications. Adv Appl Bioinforma Chem 8:37–47. https://doi.org/10.2147/AABC.S70333
Hsu F, Mao Y (2015) The structure of phosphoinositide phosphatases: Insights into substrate specificity and catalysis. Biochim Biophys Acta 1851(6):698–710. https://doi.org/10.1016/j.bbalip.2014.09.015
Hsuan J, Cockcroft S (2001) The PITP family of phosphatidylinositol transfer proteins. Genome Biol 2(9):REVIEWS3011
Huang CL, Feng S, Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391(6669):803–806. https://doi.org/10.1038/35882
Huang Y, Shah V, Liu T, Keshvara L (2005) Signaling through disabled 1 requires phosphoinositide binding. Biochem Biophys Res Commun 331(4):1460–1468. https://doi.org/10.1016/j.bbrc.2005.04.064
Hurley JH (2008) ESCRT complexes and the biogenesis of multivesicular bodies. Curr Opin Cell Biol 20(1):4–11. https://doi.org/10.1016/j.ceb.2007.12.002
Hyman J, Chen H, Di Fiore PP, De Camilli P, Brunger AT (2000) Epsin 1 undergoes nucleocytosolic shuttling and its eps15 interactor NH(2)-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor promyelocytic leukemia Zn(2)+ finger protein (PLZF). J Cell Biol 149(3):537–546
Hyvonen M, Macias MJ, Nilges M, Oschkinat H, Saraste M, Wilmanns M (1995) Structure of the binding site for inositol phosphates in a PH domain. EMBO J 14(19):4676–4685
Iijima M, Huang YE, Luo HR, Vazquez F, Devreotes PN (2004) Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J Biol Chem 279(16):16606–16613. https://doi.org/10.1074/jbc.M312098200
Ile KE, Schaaf G, Bankaitis VA (2006) Phosphatidylinositol transfer proteins and cellular nanoreactors for lipid signaling. Nat Chem Biol 2(11):576–583. https://doi.org/10.1038/nchembio835
Im YJ, Hurley JH (2008) Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev Cell 14(6):902–913. https://doi.org/10.1016/j.devcel.2008.04.004
Im YJ, Raychaudhuri S, Prinz WA, Hurley JH (2005) Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437(7055):154–158. https://doi.org/10.1038/nature03923
Ingmundson A, Delprato A, Lambright DG, Roy CR (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450(7168):365–369. https://doi.org/10.1038/nature06336
Inoue H, Baba T, Sato S, Ohtsuki R, Takemori A, Watanabe T, Tagaya M, Tani K (2012) Roles of SAM and DDHD domains in mammalian intracellular phospholipase A1 KIAA0725p. Biochim Biophys Acta 1823(4):930–939. https://doi.org/10.1016/j.bbamcr.2012.02.002
Irvine RF (2003) Nuclear lipid signalling. Nat Rev Mol Cell Biol 4(5):349–360. https://doi.org/10.1038/nrm1100
Isakoff SJ, Cardozo T, Andreev J, Li Z, Ferguson KM, Abagyan R, Lemmon MA, Aronheim A, Skolnik EY (1998) Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J 17(18):5374–5387. https://doi.org/10.1093/emboj/17.18.5374
Itoh T, De Camilli P (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim Biophys Acta 1761(8):897–912. https://doi.org/10.1016/j.bbalip.2006.06.015
Itoh T, Koshiba S, Kigawa T, Kikuchi A, Yokoyama S, Takenawa T (2001) Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291(5506):1047–1051. https://doi.org/10.1126/science.291.5506.1047
Ivarsson Y (2012) Plasticity of PDZ domains in ligand recognition and signaling. FEBS Lett 586(17):2638–2647. https://doi.org/10.1016/j.febslet.2012.04.015
Ivarsson Y, Wawrzyniak AM, Wuytens G, Kosloff M, Vermeiren E, Raport M, Zimmermann P (2011) Cooperative phosphoinositide and peptide binding by PSD-95/discs large/ZO-1 (PDZ) domain of polychaetoid, Drosophila zonulin. J Biol Chem 286(52):44669–44678. https://doi.org/10.1074/jbc.M111.285734
Ivarsson Y, Wawrzyniak AM, Kashyap R, Polanowska J, Betzi S, Lembo F, Vermeiren E, Chiheb D, Lenfant N, Morelli X, Borg JP, Reboul J, Zimmermann P (2013) Prevalence, specificity and determinants of lipid-interacting PDZ domains from an in-cell screen and in vitro binding experiments. PLoS One 8(2):e54581. https://doi.org/10.1371/journal.pone.0054581
Jackson CL, Walch L, Verbavatz JM (2016) Lipids and their trafficking: an integral part of cellular organization. Dev Cell 39(2):139–153. https://doi.org/10.1016/j.devcel.2016.09.030
Jain A, Holthuis JCM (2017) Membrane contact sites, ancient and central hubs of cellular lipid logistics. Biochim Biophys Acta 1864(9):1450–1458. https://doi.org/10.1016/j.bbamcr.2017.05.017
Jank T, Bohmer KE, Tzivelekidis T, Schwan C, Belyi Y, Aktories K (2012) Domain organization of Legionella effector SetA. Cell Microbiol 14(6):852–868. https://doi.org/10.1111/j.1462-5822.2012.01761.x
Jarsch IK, Daste F, Gallop JL (2016) Membrane curvature in cell biology: an integration of molecular mechanisms. J Cell Biol 214(4):375–387. https://doi.org/10.1083/jcb.201604003
Jaworski CJ, Moreira E, Li A, Lee R, Rodriguez IR (2001) A family of 12 human genes containing oxysterol-binding domains. Genomics 78(3):185–196. https://doi.org/10.1006/geno.2001.6663
Jayasundar JJ, Ju JH, He L, Liu D, Meilleur F, Zhao J, Callaway DJ, Bu Z (2012) Open conformation of ezrin bound to phosphatidylinositol 4,5-bisphosphate and to F-actin revealed by neutron scattering. J Biol Chem 287(44):37119–37133. https://doi.org/10.1074/jbc.M112.380972
Jian X, Tang WK, Zhai P, Roy NS, Luo R, Gruschus JM, Yohe ME, Chen PW, Li Y, Byrd RA, Xia D, Randazzo PA (2015) Molecular basis for cooperative binding of anionic phospholipids to the PH domain of the Arf GAP ASAP1. Structure 23(11):1977–1988. https://doi.org/10.1016/j.str.2015.08.008
Johansson M, Bocher V, Lehto M, Chinetti G, Kuismanen E, Ehnholm C, Staels B, Olkkonen VM (2003) The two variants of oxysterol binding protein-related protein-1 display different tissue expression patterns, have different intracellular localization, and are functionally distinct. Mol Biol Cell 14(3):903–915. https://doi.org/10.1091/mbc.E02-08-0459
Joseph RE, Wales TE, Fulton DB, Engen JR, Andreotti AH (2017) Achieving a graded immune response: BTK adopts a range of active/inactive conformations dictated by multiple interdomain contacts. Structure 25(10):1481–1494 e1484. https://doi.org/10.1016/j.str.2017.07.014
Jungmichel S, Sylvestersen KB, Choudhary C, Nguyen S, Mann M, Nielsen ML (2014) Specificity and commonality of the phosphoinositide-binding proteome analyzed by quantitative mass spectrometry. Cell Rep 6(3):578–591. https://doi.org/10.1016/j.celrep.2013.12.038
Kam JL, Miura K, Jackson TR, Gruschus J, Roller P, Stauffer S, Clark J, Aneja R, Randazzo PA (2000) Phosphoinositide-dependent activation of the ADP-ribosylation factor GTPase-activating protein ASAP1. Evidence for the pleckstrin homology domain functioning as an allosteric site. J Biol Chem 275(13):9653–9663
Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE, Cantley LC, Yaffe MB (2001) The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol 3(7):675–678. https://doi.org/10.1038/35083070
Kaneko T, Joshi R, Feller SM, Li SS (2012) Phosphotyrosine recognition domains: the typical, the atypical and the versatile. Cell Commun Signal 10(1):32. https://doi.org/10.1186/1478-811X-10-32
Karathanassis D, Stahelin RV, Bravo J, Perisic O, Pacold CM, Cho W, Williams RL (2002) Binding of the PX domain of p47(phox) to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J 21(19):5057–5068
Kavran JM, Klein DE, Lee A, Falasca M, Isakoff SJ, Skolnik EY, Lemmon MA (1998) Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J Biol Chem 273(46):30497–30508
Kay BK, Yamabhai M, Wendland B, Emr SD (1999) Identification of a novel domain shared by putative components of the endocytic and cytoskeletal machinery. Protein Sci 8(2):435–438. https://doi.org/10.1110/ps.8.2.435
Kentala H, Weber-Boyvat M, Olkkonen VM (2016) OSBP-related protein family: mediators of lipid transport and signaling at membrane contact sites. Int Rev Cell Mol Biol 321:299–340. https://doi.org/10.1016/bs.ircmb.2015.09.006
Ketel K, Krauss M, Nicot AS, Puchkov D, Wieffer M, Muller R, Subramanian D, Schultz C, Laporte J, Haucke V (2016) A phosphoinositide conversion mechanism for exit from endosomes. Nature 529(7586):408–412. https://doi.org/10.1038/nature16516
Killian JA, von Heijne G (2000) How proteins adapt to a membrane-water interface. Trends Biochem Sci 25(9):429–434
Kim YJ, Guzman-Hernandez ML, Balla T (2011) A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev Cell 21(5):813–824. https://doi.org/10.1016/j.devcel.2011.09.005
Kim S, Kedan A, Marom M, Gavert N, Keinan O, Selitrennik M, Laufman O, Lev S (2013a) The phosphatidylinositol-transfer protein Nir2 binds phosphatidic acid and positively regulates phosphoinositide signalling. EMBO Rep 14(10):891–899. https://doi.org/10.1038/embor.2013.113
Kim YJ, Hernandez ML, Balla T (2013b) Inositol lipid regulation of lipid transfer in specialized membrane domains. Trends Cell Biol 23(6):270–278. https://doi.org/10.1016/j.tcb.2013.01.009
Kim YJ, Guzman-Hernandez ML, Wisniewski E, Balla T (2015) Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev Cell 33(5):549–561. https://doi.org/10.1016/j.devcel.2015.04.028
Kim YJ, Guzman-Hernandez ML, Wisniewski E, Echeverria N, Balla T (2016) Phosphatidylinositol and phosphatidic acid transport between the ER and plasma membrane during PLC activation requires the Nir2 protein. Biochem Soc Trans 44(1):197–201. https://doi.org/10.1042/BST20150187
Kleyn PW, Fan W, Kovats SG, Lee JJ, Pulido JC, Wu Y, Berkemeier LR, Misumi DJ, Holmgren L, Charlat O, Woolf EA, Tayber O, Brody T, Shu P, Hawkins F, Kennedy B, Baldini L, Ebeling C, Alperin GD, Deeds J, Lakey ND, Culpepper J, Chen H, Glucksmann-Kuis MA, Carlson GA, Duyk GM, Moore KJ (1996) Identification and characterization of the mouse obesity gene tubby: a member of a novel gene family. Cell 85(2):281–290
Knight JD, Falke JJ (2009) Single-molecule fluorescence studies of a PH domain: new insights into the membrane docking reaction. Biophys J 96(2):566–582. https://doi.org/10.1016/j.bpj.2008.10.020
Kohout SC, Corbalan-Garcia S, Gomez-Fernandez JC, Falke JJ (2003) C2 domain of protein kinase C alpha: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling. Biochemistry 42(5):1254–1265. https://doi.org/10.1021/bi026596f
Konermann L, Vahidi S, Sowole MA (2014) Mass spectrometry methods for studying structure and dynamics of biological macromolecules. Anal Chem 86(1):213–232. https://doi.org/10.1021/ac4039306
Kontos CD, Stauffer TP, Yang WP, York JD, Huang L, Blanar MA, Meyer T, Peters KG (1998) Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt. Mol Cell Biol 18(7):4131–4140
Krick R, Tolstrup J, Appelles A, Henke S, Thumm M (2006) The relevance of the phosphatidylinositolphosphat-binding motif FRRGT of Atg18 and Atg21 for the Cvt pathway and autophagy. FEBS Lett 580(19):4632–4638. https://doi.org/10.1016/j.febslet.2006.07.041
Krick R, Busse RA, Scacioc A, Stephan M, Janshoff A, Thumm M, Kuhnel K (2012) Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a beta-propeller protein family. Proc Natl Acad Sci U S A 109(30):E2042–E2049. https://doi.org/10.1073/pnas.1205128109
Kular GS, Chaudhary A, Prestwich G, Swigart P, Wetzker R, Cockcroft S (2002) Co-operation of phosphatidylinositol transfer protein with phosphoinositide 3-kinase gamma in vitro. Adv Enzym Regul 42:53–61
Kulkarni S, Das S, Funk CD, Murray D, Cho W (2002) Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J Biol Chem 277(15):13167–13174. https://doi.org/10.1074/jbc.M112393200
Kutateladze TG (2006) Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim Biophys Acta 1761(8):868–877. https://doi.org/10.1016/j.bbalip.2006.03.011
Kutateladze TG (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6(7):507–513. https://doi.org/10.1038/nchembio.390
Kutateladze T, Overduin M (2001) Structural mechanism of endosome docking by the FYVE domain. Science 291(5509):1793–1796. https://doi.org/10.1126/science.291.5509.1793
Kutateladze TG, Ogburn KD, Watson WT, de Beer T, Emr SD, Burd CG, Overduin M (1999) Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol Cell 3(6):805–811
Kutateladze TG, Capelluto DG, Ferguson CG, Cheever ML, Kutateladze AG, Prestwich GD, Overduin M (2004) Multivalent mechanism of membrane insertion by the FYVE domain. J Biol Chem 279(4):3050–3057. https://doi.org/10.1074/jbc.M309007200
Kweon DH, Shin YK, Shin JY, Lee JH, Lee JB, Seo JH, Kim YS (2006) Membrane topology of helix 0 of the Epsin N-terminal homology domain. Mol Cells 21(3):428–435
Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT, Baldwin AJ, Robinson CV (2014) Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510(7503):172–175. https://doi.org/10.1038/nature13419
Lai CL, Landgraf KE, Voth GA, Falke JJ (2010) Membrane docking geometry and target lipid stoichiometry of membrane-bound PKCalpha C2 domain: a combined molecular dynamics and experimental study. J Mol Biol 402(2):301–310. https://doi.org/10.1016/j.jmb.2010.07.037
Lai CL, Jao CC, Lyman E, Gallop JL, Peter BJ, McMahon HT, Langen R, Voth GA (2012) Membrane binding and self-association of the epsin N-terminal homology domain. J Mol Biol 423(5):800–817. https://doi.org/10.1016/j.jmb.2012.08.010
Larijani B, Allen-Baume V, Morgan CP, Li M, Cockcroft S (2003) EGF regulation of PITP dynamics is blocked by inhibitors of phospholipase C and of the Ras-MAP kinase pathway. Curr Biol 13(1):78–84
Lawe DC, Patki V, Heller-Harrison R, Lambright D, Corvera S (2000) The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J Biol Chem 275(5):3699–3705
Lee AG (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612(1):1–40
Lee SA, Eyeson R, Cheever ML, Geng J, Verkhusha VV, Burd C, Overduin M, Kutateladze TG (2005) Targeting of the FYVE domain to endosomal membranes is regulated by a histidine switch. Proc Natl Acad Sci U S A 102(37):13052–13057. https://doi.org/10.1073/pnas.0503900102
Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 117(Pt 1):9–18. https://doi.org/10.1242/jcs.00928
Lehto M, Laitinen S, Chinetti G, Johansson M, Ehnholm C, Staels B, Ikonen E, Olkkonen VM (2001) The OSBP-related protein family in humans. J Lipid Res 42(8):1203–1213
Lemmon MA (2003) Phosphoinositide recognition domains. Traffic 4(4):201–213
Lemmon MA (2004) Pleckstrin homology domains: not just for phosphoinositides. Biochem Soc Trans 32. (Pt 5:707–711. https://doi.org/10.1042/BST0320707
Lemmon MA (2007) Pleckstrin homology (PH) domains and phosphoinositides. Biochem Soc Symp 74:81–93. https://doi.org/10.1042/BSS0740081
Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9(2):99–111. https://doi.org/10.1038/nrm2328
Lemmon MA, Ferguson KM (2001) Molecular determinants in pleckstrin homology domains that allow specific recognition of phosphoinositides. Biochem Soc Trans 29(Pt 4):377–384
Lemmon MA, Ferguson KM, O’Brien R, Sigler PB, Schlessinger J (1995) Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc Natl Acad Sci U S A 92(23):10472–10476
Lemmon MA, Ferguson KM, Abrams CS (2002) Pleckstrin homology domains and the cytoskeleton. FEBS Lett 513(1):71–76
Lenoir M, Kufareva I, Abagyan R, Overduin M (2015) Membrane and protein interactions of the pleckstrin homology domain superfamily. Membranes (Basel) 5(4):646–663. https://doi.org/10.3390/membranes5040646
Lev S (2010) Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol 11(10):739–750. https://doi.org/10.1038/nrm2971
Levine TP, Munro S (1998) The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr Biol 8(13):729–739
Li H, Marshall AJ (2015) Phosphatidylinositol (3,4) bisphosphate-specific phosphatases and effector proteins: a distinct branch of PI3K signaling. Cell Signal 27(9):1789–1798. https://doi.org/10.1016/j.cellsig.2015.05.013
Li X, Routt SM, Xie Z, Cui X, Fang M, Kearns MA, Bard M, Kirsch DR, Bankaitis VA (2000) Identification of a novel family of nonclassic yeast phosphatidylinositol transfer proteins whose function modulates phospholipase D activity and Sec14p-independent cell growth. Mol Biol Cell 11(6):1989–2005
Li H, Tremblay JM, Yarbrough LR, Helmkamp GM Jr (2002) Both isoforms of mammalian phosphatidylinositol transfer protein are capable of binding and transporting sphingomyelin. Biochim Biophys Acta 1580(1):67–76
Li J, Mao X, Dong LQ, Liu F, Tong L (2007) Crystal structures of the BAR-PH and PTB domains of human APPL1. Structure 15(5):525–533. https://doi.org/10.1016/j.str.2007.03.011
Liang B, Tamm LK (2016) NMR as a tool to investigate the structure, dynamics and function of membrane proteins. Nat Struct Mol Biol 23(6):468–474. https://doi.org/10.1038/nsmb.3226
Lietzke SE, Bose S, Cronin T, Klarlund J, Chawla A, Czech MP, Lambright DG (2000) Structural basis of 3-phosphoinositide recognition by pleckstrin homology domains. Mol Cell 6(2):385–394
Lindahl E, Sansom MS (2008) Membrane proteins: molecular dynamics simulations. Curr Opin Struct Biol 18(4):425–431. https://doi.org/10.1016/j.sbi.2008.02.003
Liu X, Ridgway ND (2014) Characterization of the sterol and phosphatidylinositol 4-phosphate binding properties of Golgi-associated OSBP-related protein 9 (ORP9). PLoS One 9(9):e108368. https://doi.org/10.1371/journal.pone.0108368
Liu Y, Kahn RA, Prestegard JH (2014) Interaction of Fapp1 with Arf1 and PI4P at a membrane surface: an example of coincidence detection. Structure 22(3):421–430. https://doi.org/10.1016/j.str.2013.12.011
Lo WT, Vujicic Zagar A, Gerth F, Lehmann M, Puchkov D, Krylova O, Freund C, Scapozza L, Vadas O, Haucke V (2017) A coincidence detection mechanism controls PX-BAR domain-mediated endocytic membrane remodeling via an allosteric structural switch. Dev Cell 43(4):522–529.e524. https://doi.org/10.1016/j.devcel.2017.10.019
Loewen CJ, Levine TP (2005) A highly conserved binding site in vesicle-associated membrane protein-associated protein (VAP) for the FFAT motif of lipid-binding proteins. J Biol Chem 280(14):14097–14104. https://doi.org/10.1074/jbc.M500147200
Lomize AL, Pogozheva ID, Lomize MA, Mosberg HI (2007) The role of hydrophobic interactions in positioning of peripheral proteins in membranes. BMC Struct Biol 7:44. https://doi.org/10.1186/1472-6807-7-44
Lorenzo O, Urbe S, Clague MJ (2005) Analysis of phosphoinositide binding domain properties within the myotubularin-related protein MTMR3. J Cell Sci 118(Pt 9):2005–2012. https://doi.org/10.1242/jcs.02325
Lumb CN, Sansom MS (2012) Finding a needle in a haystack: the role of electrostatics in target lipid recognition by PH domains. PLoS Comput Biol 8(7):e1002617. https://doi.org/10.1371/journal.pcbi.1002617
Lumb CN, He J, Xue Y, Stansfeld PJ, Stahelin RV, Kutateladze TG, Sansom MS (2011) Biophysical and computational studies of membrane penetration by the GRP1 pleckstrin homology domain. Structure 19(9):1338–1346. https://doi.org/10.1016/j.str.2011.04.010
Luo X, Wasilko DJ, Liu Y, Sun J, Wu X, Luo ZQ, Mao Y (2015) Structure of the legionella virulence factor, SidC reveals a unique PI(4)P-specific binding domain essential for its targeting to the bacterial phagosome. PLoS Pathog 11(6):e1004965. https://doi.org/10.1371/journal.ppat.1004965
Machner MP, Isberg RR (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen legionella pneumophila. Dev Cell 11(1):47–56. https://doi.org/10.1016/j.devcel.2006.05.013
Macias MJ, Musacchio A, Ponstingl H, Nilges M, Saraste M, Oschkinat H (1994) Structure of the pleckstrin homology domain from beta-spectrin. Nature 369(6482):675–677. https://doi.org/10.1038/369675a0
Maffucci T, Falasca M (2001) Specificity in pleckstrin homology (PH) domain membrane targeting: a role for a phosphoinositide-protein co-operative mechanism. FEBS Lett 506(3):173–179
Malaby AW, van den Berg B, Lambright DG (2013) Structural basis for membrane recruitment and allosteric activation of cytohesin family Arf GTPase exchange factors. Proc Natl Acad Sci U S A 110(35):14213–14218. https://doi.org/10.1073/pnas.1301883110
Malek M, Kielkowska A, Chessa T, Anderson KE, Barneda D, Pir P, Nakanishi H, Eguchi S, Koizumi A, Sasaki J, Juvin V, Kiselev VY, Niewczas I, Gray A, Valayer A, Spensberger D, Imbert M, Felisbino S, Habuchi T, Beinke S, Cosulich S, Le Novere N, Sasaki T, Clark J, Hawkins PT, Stephens LR (2017) PTEN regulates PI(3,4)P2 signaling downstream of class I PI3K. Mol Cell 68(3):566–580.e510. https://doi.org/10.1016/j.molcel.2017.09.024
Malkova S, Stahelin RV, Pingali SV, Cho W, Schlossman ML (2006) Orientation and penetration depth of monolayer-bound p40phox-PX. Biochemistry 45(45):13566–13575. https://doi.org/10.1021/bi061133l
Manna D, Albanese A, Park WS, Cho W (2007) Mechanistic basis of differential cellular responses of phosphatidylinositol 3,4-bisphosphate- and phosphatidylinositol 3,4,5-trisphosphate-binding pleckstrin homology domains. J Biol Chem 282(44):32093–32105. https://doi.org/10.1074/jbc.M703517200
Manna D, Bhardwaj N, Vora MS, Stahelin RV, Lu H, Cho W (2008) Differential roles of phosphatidylserine, PtdIns(4,5)P2, and PtdIns(3,4,5)P3 in plasma membrane targeting of C2 domains. Molecular dynamics simulation, membrane binding, and cell translocation studies of the PKCalpha C2 domain. J Biol Chem 283(38):26047–26058. https://doi.org/10.1074/jbc.M802617200
Mao Y, Nickitenko A, Duan X, Lloyd TE, Wu MN, Bellen H, Quiocho FA (2000) Crystal structure of the VHS and FYVE tandem domains of Hrs, a protein involved in membrane trafficking and signal transduction. Cell 100(4):447–456
Mao Y, Chen J, Maynard JA, Zhang B, Quiocho FA (2001) A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in synaptic vesicle endocytosis. Cell 104(3):433–440
Marat AL, Haucke V (2016) Phosphatidylinositol 3-phosphates-at the interface between cell signalling and membrane traffic. EMBO J 35(6):561–579. https://doi.org/10.15252/embj.201593564
Marat AL, Wallroth A, Lo WT, Muller R, Norata GD, Falasca M, Schultz C, Haucke V (2017) mTORC1 activity repression by late endosomal phosphatidylinositol 3,4-bisphosphate. Science 356(6341):968–972. https://doi.org/10.1126/science.aaf8310
Marsh D (2008) Protein modulation of lipids, and vice-versa, in membranes. Biochim Biophys Acta 1778(7–8):1545–1575. https://doi.org/10.1016/j.bbamem.2008.01.015
Martelli AM, Ognibene A, Buontempo F, Fini M, Bressanin D, Goto K, McCubrey JA, Cocco L, Evangelisti C (2011) Nuclear phosphoinositides and their roles in cell biology and disease. Crit Rev Biochem Mol Biol 46(5):436–457. https://doi.org/10.3109/10409238.2011.609530
Masuda M, Takeda S, Sone M, Ohki T, Mori H, Kamioka Y, Mochizuki N (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J 25(12):2889–2897. https://doi.org/10.1038/sj.emboj.7601176
Mattila PK, Pykäläinen A, Saarikangas J, Paavilainen VO, Vihinen H, Jokitalo E, Lappalainen P (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain–like mechanism. J Cell Biol 176(7):953–964. https://doi.org/10.1083/jcb.200609176
Mayer BJ, Ren R, Clark KL, Baltimore D (1993) A putative modular domain present in diverse signaling proteins. Cell 73(4):629–630
McCrea HJ, De Camilli P (2009) Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24:8–16. https://doi.org/10.1152/physiol.00035.2008
McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438(7068):605–611. https://doi.org/10.1038/nature04398
McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590–596. https://doi.org/10.1038/nature04396
Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B (2013) A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155(4):830–843. https://doi.org/10.1016/j.cell.2013.09.056
Michell RH, Heath VL, Lemmon MA, Dove SK (2006) Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions. Trends Biochem Sci 31(1):52–63. https://doi.org/10.1016/j.tibs.2005.11.013
Millard TH, Bompard G, Heung MY, Dafforn TR, Scott DJ, Machesky LM, Futterer K (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J 24(2):240–250. https://doi.org/10.1038/sj.emboj.7600535
Miller SE, Sahlender DA, Graham SC, Honing S, Robinson MS, Peden AA, Owen DJ (2011) The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147(5):1118–1131. https://doi.org/10.1016/j.cell.2011.10.038
Miller SE, Mathiasen S, Bright NA, Pierre F, Kelly BT, Kladt N, Schauss A, Merrifield CJ, Stamou D, Honing S, Owen DJ (2015) CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev Cell 33(2):163–175. https://doi.org/10.1016/j.devcel.2015.03.002
Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37(12):526–533. https://doi.org/10.1016/j.tibs.2012.09.001
Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E, Voth GA, Unger VM (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149(1):137–145. https://doi.org/10.1016/j.cell.2012.01.048
Misawa H, Ohtsubo M, Copeland NG, Gilbert DJ, Jenkins NA, Yoshimura A (1998) Cloning and characterization of a novel class II phosphoinositide 3-kinase containing C2 domain. Biochem Biophys Res Commun 244(2):531–539. https://doi.org/10.1006/bbrc.1998.8294
Misra S, Hurley JH (1999) Crystal structure of a phosphatidylinositol 3-phosphate-specific membrane-targeting motif, the FYVE domain of Vps27p. Cell 97(5):657–666
Moleirinho S, Tilston-Lunel A, Angus L, Gunn-Moore F, Reynolds PA (2013) The expanding family of FERM proteins. Biochem J 452(2):183–193. https://doi.org/10.1042/BJ20121642
Monje-Galvan V, Klauda JB (2016) Peripheral membrane proteins: tying the knot between experiment and computation. Biochim Biophys Acta 1858(7 Pt B):1584–1593. https://doi.org/10.1016/j.bbamem.2016.02.018
Montaville P, Coudevylle N, Radhakrishnan A, Leonov A, Zweckstetter M, Becker S (2008) The PIP2 binding mode of the C2 domains of rabphilin-3A. Protein Sci 17(6):1025–1034. https://doi.org/10.1110/ps.073326608
Morales KA, Yang Y, Cole TR, Igumenova TI (2016) Dynamic response of the C2 domain of protein kinase calpha to Ca(2+) binding. Biophys J 111(8):1655–1667. https://doi.org/10.1016/j.bpj.2016.09.008
Moravcevic K, Mendrola JM, Schmitz KR, Wang YH, Slochower D, Janmey PA, Lemmon MA (2010) Kinase associated-1 domains drive MARK/PAR1 kinases to membrane targets by binding acidic phospholipids. Cell 143(6):966–977. https://doi.org/10.1016/j.cell.2010.11.028
Moravcevic K, Oxley CL, Lemmon MA (2012) Conditional peripheral membrane proteins: facing up to limited specificity. Structure 20(1):15–27. https://doi.org/10.1016/j.str.2011.11.012
Moravcevic K, Alvarado D, Schmitz KR, Kenniston JA, Mendrola JM, Ferguson KM, Lemmon MA (2015) Comparison of Saccharomyces cerevisiae F-BAR domain structures reveals a conserved inositol phosphate binding site. Structure 23(2):352–363. https://doi.org/10.1016/j.str.2014.12.009
Mortier E, Wuytens G, Leenaerts I, Hannes F, Heung MY, Degeest G, David G, Zimmermann P (2005) Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. EMBO J 24(14):2556–2565. https://doi.org/10.1038/sj.emboj.7600722
Moser von Filseck J, Copic A, Delfosse V, Vanni S, Jackson CL, Bourguet W, Drin G (2015a) Intracellular transport. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349(6246):432–436. https://doi.org/10.1126/science.aab1346
Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G (2015b) A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat Commun 6:6671. https://doi.org/10.1038/ncomms7671
Mu Y, Cai P, Hu S, Ma S, Gao Y (2014) Characterization of diverse internal binding specificities of PDZ domains by yeast two-hybrid screening of a special peptide library. PLoS One 9(2):e88286. https://doi.org/10.1371/journal.pone.0088286
Muallem S, Chung WY, Jha A, Ahuja M (2017) Lipids at membrane contact sites: cell signaling and ion transport. EMBO Rep 18(11):1893–1904. https://doi.org/10.15252/embr.201744331
Mukhopadhyay S, Jackson PK (2011) The tubby family proteins. Genome Biol 12(6):225. https://doi.org/10.1186/gb-2011-12-6-225
Mulgrew-Nesbitt A, Diraviyam K, Wang J, Singh S, Murray P, Li Z, Rogers L, Mirkovic N, Murray D (2006) The role of electrostatics in protein-membrane interactions. Biochim Biophys Acta 1761(8):812–826. https://doi.org/10.1016/j.bbalip.2006.07.002
Murphy SE, Levine TP (2016) VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome. Biochim Biophys Acta 1861(8 Pt B):952–961. https://doi.org/10.1016/j.bbalip.2016.02.009
Murray D, Honig B (2002) Electrostatic control of the membrane targeting of C2 domains. Mol Cell 9(1):145–154
Musacchio A, Gibson T, Rice P, Thompson J, Saraste M (1993) The PH domain: a common piece in the structural patchwork of signalling proteins. Trends Biochem Sci 18(9):343–348
Nakatsu F, Baskin JM, Chung J, Tanner LB, Shui G, Lee SY, Pirruccello M, Hao M, Ingolia NT, Wenk MR, De Camilli P (2012) PtdIns4P synthesis by PI4KIIIalpha at the plasma membrane and its impact on plasma membrane identity. J Cell Biol 199(6):1003–1016. https://doi.org/10.1083/jcb.201206095
Nalefski EA, McDonagh T, Somers W, Seehra J, Falke JJ, Clark JD (1998) Independent folding and ligand specificity of the C2 calcium-dependent lipid binding domain of cytosolic phospholipase A2. J Biol Chem 273(3):1365–1372
Naughton FB, Kalli AC, Sansom MS (2016) Association of peripheral membrane proteins with membranes: free energy of binding of GRP1 PH domain with phosphatidylinositol phosphate-containing model bilayers. J Phys Chem Lett 7(7):1219–1224. https://doi.org/10.1021/acs.jpclett.6b00153
Nawrotek A, Zeghouf M, Cherfils J (2016) Allosteric regulation of Arf GTPases and their GEFs at the membrane interface. Small GTPases 7(4):283–296. https://doi.org/10.1080/21541248.2016.1215778
Noben-Trauth K, Naggert JK, North MA, Nishina PM (1996) A candidate gene for the mouse mutation tubby. Nature 380(6574):534–538. https://doi.org/10.1038/380534a0
Nourry C, Grant SG, Borg JP (2003) PDZ domain proteins: plug and play! Sci STKE 2003(179):RE7. https://doi.org/10.1126/stke.2003.179.re7
Obara K, Sekito T, Niimi K, Ohsumi Y (2008) The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem 283(35):23972–23980. https://doi.org/10.1074/jbc.M803180200
Ocaka L, Spalluto C, Wilson DI, Hunt DM, Halford S (2005) Chromosomal localization, genomic organization and evolution of the genes encoding human phosphatidylinositol transfer protein membrane-associated (PITPNM) 1, 2 and 3. Cytogenet Genome Res 108(4):293–302. https://doi.org/10.1159/000081519
Ono Y, Fujii T, Igarashi K, Kuno T, Tanaka C, Kikkawa U, Nishizuka Y (1989) Phorbol ester binding to protein kinase C requires a cysteine-rich zinc-finger-like sequence. Proc Natl Acad Sci U S A 86(13):4868–4871
Ooms LM, Binge LC, Davies EM, Rahman P, Conway JR, Gurung R, Ferguson DT, Papa A, Fedele CG, Vieusseux JL, Chai RC, Koentgen F, Price JT, Tiganis T, Timpson P, McLean CA, Mitchell CA (2015) The inositol polyphosphate 5-phosphatase PIPP regulates AKT1-dependent breast cancer growth and metastasis. Cancer Cell 28(2):155–169. https://doi.org/10.1016/j.ccell.2015.07.003
Osada S, Mizuno K, Saido TC, Akita Y, Suzuki K, Kuroki T, Ohno S (1990) A phorbol ester receptor/protein kinase, nPKC eta, a new member of the protein kinase C family predominantly expressed in lung and skin. J Biol Chem 265(36):22434–22440
Pang X, Fan J, Zhang Y, Zhang K, Gao B, Ma J, Li J, Deng Y, Zhou Q, Egelman EH, Hsu VW, Sun F (2014) A PH domain in ACAP1 possesses key features of the BAR domain in promoting membrane curvature. Dev Cell 31(1):73–86. https://doi.org/10.1016/j.devcel.2014.08.020
Park WS, Heo WD, Whalen JH, O’Rourke NA, Bryan HM, Meyer T, Teruel MN (2008) Comprehensive identification of PIP3-regulated PH domains from C. elegans to H. sapiens by model prediction and live imaging. Mol Cell 30(3):381–392. https://doi.org/10.1016/j.molcel.2008.04.008
Parkinson GN, Vines D, Driscoll PC, Djordjevic S (2008) Crystal structures of PI3K-C2alpha PX domain indicate conformational change associated with ligand binding. BMC Struct Biol 8:13. https://doi.org/10.1186/1472-6807-8-13
Pasenkiewicz-Gierula M, Baczynski K, Markiewicz M, Murzyn K (2016) Computer modelling studies of the bilayer/water interface. Biochim Biophys Acta 1858(10):2305–2321. https://doi.org/10.1016/j.bbamem.2016.01.024
Payrastre B, Gaits-Iacovoni F, Sansonetti P, Tronchere H (2012) Phosphoinositides and cellular pathogens. Subcell Biochem 59:363–388. https://doi.org/10.1007/978-94-007-3015-1_12
Pearson MA, Reczek D, Bretscher A, Karplus PA (2000) Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101(3):259–270
Pendaries C, Tronchere H, Plantavid M, Payrastre B (2003) Phosphoinositide signaling disorders in human diseases. FEBS Lett 546(1):25–31
Perisic O, Fong S, Lynch DE, Bycroft M, Williams RL (1998) Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J Biol Chem 273(3):1596–1604
Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303(5657):495–499. https://doi.org/10.1126/science.1092586
Phillips SE, Ile KE, Boukhelifa M, Huijbregts RP, Bankaitis VA (2006) Specific and nonspecific membrane-binding determinants cooperate in targeting phosphatidylinositol transfer protein beta-isoform to the mammalian trans-Golgi network. Mol Biol Cell 17(6):2498–2512. https://doi.org/10.1091/mbc.E06-01-0089
Pizarro-Cerda J, Kuhbacher A, Cossart P (2015) Phosphoinositides and host-pathogen interactions. Biochim Biophys Acta 1851(6):911–918. https://doi.org/10.1016/j.bbalip.2014.09.011
Pogozheva ID, Tristram-Nagle S, Mosberg HI, Lomize AL (2013) Structural adaptations of proteins to different biological membranes. Biochim Biophys Acta 1828(11):2592–2608. https://doi.org/10.1016/j.bbamem.2013.06.023
Ponting CP (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci 5(11):2353–2357. https://doi.org/10.1002/pro.5560051122
Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, Lampe A, Muller R, Zarbakhsh S, Gulluni F, Hirsch E, Krauss M, Schultz C, Schmoranzer J, Noe F, Haucke V (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499(7457):233–237. https://doi.org/10.1038/nature12360
Prehoda KE, Lee DJ, Lim WA (1999) Structure of the enabled/VASP homology 1 domain-peptide complex: a key component in the spatial control of actin assembly. Cell 97(4):471–480
Premkumar L, Bobkov AA, Patel M, Jaroszewski L, Bankston LA, Stec B, Vuori K, Cote JF, Liddington RC (2010) Structural basis of membrane targeting by the Dock180 family of Rho family guanine exchange factors (Rho-GEFs). J Biol Chem 285(17):13211–13222. https://doi.org/10.1074/jbc.M110.102517
Prinz WA (2010) Lipid trafficking sans vesicles: where, why, how? Cell 143(6):870–874. https://doi.org/10.1016/j.cell.2010.11.031
Psachoulia E, Sansom MS (2008) Interactions of the pleckstrin homology domain with phosphatidylinositol phosphate and membranes: characterization via molecular dynamics simulations. Biochemistry 47(14):4211–4220. https://doi.org/10.1021/bi702319k
Pykalainen A, Boczkowska M, Zhao H, Saarikangas J, Rebowski G, Jansen M, Hakanen J, Koskela EV, Peranen J, Vihinen H, Jokitalo E, Salminen M, Ikonen E, Dominguez R, Lappalainen P (2011) Pinkbar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat Struct Mol Biol 18(8):902–907. https://doi.org/10.1038/nsmb.2079
Pylypenko O, Lundmark R, Rasmuson E, Carlsson SR, Rak A (2007) The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J 26(22):4788–4800. https://doi.org/10.1038/sj.emboj.7601889
Qualmann B, Koch D, Kessels MM (2011) Let’s go bananas: revisiting the endocytic BAR code. EMBO J 30(17):3501–3515. https://doi.org/10.1038/emboj.2011.266
Ragaz C, Pietsch H, Urwyler S, Tiaden A, Weber SS, Hilbi H (2008) The Legionella pneumophila phosphatidylinositol-4 phosphate-binding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell Microbiol 10(12):2416–2433. https://doi.org/10.1111/j.1462-5822.2008.01219.x
Rameh LE, Arvidsson A, Carraway KL 3rd, Couvillon AD, Rathbun G, Crompton A, VanRenterghem B, Czech MP, Ravichandran KS, Burakoff SJ, Wang DS, Chen CS, Cantley LC (1997) A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J Biol Chem 272(35):22059–22066
Ramel D, Lagarrigue F, Pons V, Mounier J, Dupuis-Coronas S, Chicanne G, Sansonetti PJ, Gaits-Iacovoni F, Tronchere H, Payrastre B (2011) Shigella flexneri infection generates the lipid PI5P to alter endocytosis and prevent termination of EGFR signaling. Sci Signal 4(191):ra61. https://doi.org/10.1126/scisignal.2001619
Ravichandran KS, Zhou MM, Pratt JC, Harlan JE, Walk SF, Fesik SW, Burakoff SJ (1997) Evidence for a requirement for both phospholipid and phosphotyrosine binding via the Shc phosphotyrosine-binding domain in vivo. Mol Cell Biol 17(9):5540–5549
Raychaudhuri S, Im YJ, Hurley JH, Prinz WA (2006) Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J Cell Biol 173(1):107–119. https://doi.org/10.1083/jcb.200510084
Redfern RE, Redfern D, Furgason ML, Munson M, Ross AH, Gericke A (2008) PTEN phosphatase selectively binds phosphoinositides and undergoes structural changes. Biochemistry 47(7):2162–2171. https://doi.org/10.1021/bi702114w
Renard HF, Simunovic M, Lemiere J, Boucrot E, Garcia-Castillo MD, Arumugam S, Chambon V, Lamaze C, Wunder C, Kenworthy AK, Schmidt AA, McMahon HT, Sykes C, Bassereau P, Johannes L (2015) Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature 517(7535):493–496. https://doi.org/10.1038/nature14064
Reue K (2009) The lipin family: mutations and metabolism. Curr Opin Lipidol 20(3):165–170. https://doi.org/10.1097/MOL.0b013e32832adee5
Rizo J, Sudhof TC (1998) C2-domains, structure and function of a universal Ca2+−binding domain. J Biol Chem 273(26):15879–15882
Roderick SL, Chan WW, Agate DS, Olsen LR, Vetting MW, Rajashankar KR, Cohen DE (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat Struct Biol 9(7):507–511. https://doi.org/10.1038/nsb812
Rogaski B, Klauda JB (2012) Membrane-binding mechanism of a peripheral membrane protein through microsecond molecular dynamics simulations. J Mol Biol 423(5):847–861. https://doi.org/10.1016/j.jmb.2012.08.015
Rohacs T, Lopes CM, Jin T, Ramdya PP, Molnar Z, Logothetis DE (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc Natl Acad Sci U S A 100(2):745–750. https://doi.org/10.1073/pnas.0236364100
Romanowski MJ, Soccio RE, Breslow JL, Burley SK (2002) Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain. Proc Natl Acad Sci U S A 99(10):6949–6954. https://doi.org/10.1073/pnas.052140699
Roy NS, Yohe ME, Randazzo PA, Gruschus JM (2016) Allosteric properties of PH domains in Arf regulatory proteins. Cell Logist 6(2):e1181700. https://doi.org/10.1080/21592799.2016.1181700
Ryan MM, Temple BR, Phillips SE, Bankaitis VA (2007) Conformational dynamics of the major yeast phosphatidylinositol transfer protein sec14p: insight into the mechanisms of phospholipid exchange and diseases of sec14p-like protein deficiencies. Mol Biol Cell 18(5):1928–1942. https://doi.org/10.1091/mbc.E06-11-1024
Saarikangas J, Zhao H, Pykalainen A, Laurinmaki P, Mattila PK, Kinnunen PK, Butcher SJ, Lappalainen P (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19(2):95–107. https://doi.org/10.1016/j.cub.2008.12.029
Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90(1):259–289. https://doi.org/10.1152/physrev.00036.2009
Saksena S, Sun J, Chu T, Emr SD (2007) ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 32(12):561–573. https://doi.org/10.1016/j.tibs.2007.09.010
Salama SR, Cleves AE, Malehorn DE, Whitters EA, Bankaitis VA (1990) Cloning and characterization of Kluyveromyces lactis SEC14, a gene whose product stimulates Golgi secretory function in Saccharomyces cerevisiae. J Bacteriol 172(8):4510–4521
Salomon D, Guo Y, Kinch LN, Grishin NV, Gardner KH, Orth K (2013) Effectors of animal and plant pathogens use a common domain to bind host phosphoinositides. Nat Commun 4:2973. https://doi.org/10.1038/ncomms3973
Salzer U, Kostan J, Djinovic-Carugo K (2017) Deciphering the BAR code of membrane modulators. Cell Mol Life Sci 74(13):2413–2438. https://doi.org/10.1007/s00018-017-2478-0
Sanchez-Bautista S, Marin-Vicente C, Gomez-Fernandez JC, Corbalan-Garcia S (2006) The C2 domain of PKCalpha is a Ca2+ −dependent PtdIns(4,5)P2 sensing domain: a new insight into an old pathway. J Mol Biol 362(5):901–914. https://doi.org/10.1016/j.jmb.2006.07.093
Santagata S, Boggon TJ, Baird CL, Gomez CA, Zhao J, Shan WS, Myszka DG, Shapiro L (2001) G-protein signaling through tubby proteins. Science 292(5524):2041–2050. https://doi.org/10.1126/science.1061233
Saras J, Heldin CH (1996) PDZ domains bind carboxy-terminal sequences of target proteins. Trends Biochem Sci 21(12):455–458
Sarkes D, Rameh LE (2010) A novel HPLC-based approach makes possible the spatial characterization of cellular PtdIns5P and other phosphoinositides. Biochem J 428(3):375–384. https://doi.org/10.1042/BJ20100129
Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki M, Suzuki A (2009) Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res 48(6):307–343. https://doi.org/10.1016/j.plipres.2009.06.001
Sato TK, Overduin M, Emr SD (2001) Location, location, location: membrane targeting directed by PX domains. Science 294(5548):1881–1885. https://doi.org/10.1126/science.1065763
Sbrissa D, Ikonomov OC, Filios C, Delvecchio K, Shisheva A (2012) Functional dissociation between PIKfyve-synthesized PtdIns5P and PtdIns(3,5)P2 by means of the PIKfyve inhibitor YM201636. Am J Physiol Cell Physiol 303(4):C436–C446. https://doi.org/10.1152/ajpcell.00105.2012
Scacioc A, Schmidt C, Hofmann T, Urlaub H, Kuhnel K, Perez-Lara A (2017) Structure based biophysical characterization of the PROPPIN Atg18 shows Atg18 oligomerization upon membrane binding. Sci Rep 7(1):14008. https://doi.org/10.1038/s41598-017-14337-5
Schaaf G, Ortlund EA, Tyeryar KR, Mousley CJ, Ile KE, Garrett TA, Ren J, Woolls MJ, Raetz CR, Redinbo MR, Bankaitis VA (2008) Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol Cell 29(2):191–206. https://doi.org/10.1016/j.molcel.2007.11.026
Schaaf G, Dynowski M, Mousley CJ, Shah SD, Yuan P, Winklbauer EM, de Campos MK, Trettin K, Quinones MC, Smirnova TI, Yanagisawa LL, Ortlund EA, Bankaitis VA (2011) Resurrection of a functional phosphatidylinositol transfer protein from a pseudo-Sec14 scaffold by directed evolution. Mol Biol Cell 22(6):892–905. https://doi.org/10.1091/mbc.E10-11-0903
Scheffzek K, Welti S (2012) Pleckstrin homology (PH) like domains – versatile modules in protein-protein interaction platforms. FEBS Lett 586(17):2662–2673. https://doi.org/10.1016/j.febslet.2012.06.006
Schink KO, Tan KW, Stenmark H (2016) Phosphoinositides in control of membrane dynamics. Annu Rev Cell Dev Biol 32:143–171. https://doi.org/10.1146/annurev-cellbio-111315-125349
Schoebel S, Blankenfeldt W, Goody RS, Itzen A (2010) High-affinity binding of phosphatidylinositol 4-phosphate by Legionella pneumophila DrrA. EMBO Rep 11(8):598–604. https://doi.org/10.1038/embor.2010.97
Schoneberg J, Lehmann M, Ullrich A, Posor Y, Lo WT, Lichtner G, Schmoranzer J, Haucke V, Noe F (2017) Lipid-mediated PX-BAR domain recruitment couples local membrane constriction to endocytic vesicle fission. Nat Commun 8:15873. https://doi.org/10.1038/ncomms15873
Schouten A, Agianian B, Westerman J, Kroon J, Wirtz KW, Gros P (2002) Structure of apo-phosphatidylinositol transfer protein alpha provides insight into membrane association. EMBO J 21(9):2117–2121. https://doi.org/10.1093/emboj/21.9.2117
Schulz TA, Choi MG, Raychaudhuri S, Mears JA, Ghirlando R, Hinshaw JE, Prinz WA (2009) Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J Cell Biol 187(6):889–903. https://doi.org/10.1083/jcb.200905007
Seet LF, Hong W (2006) The Phox (PX) domain proteins and membrane traffic. Biochim Biophys Acta 1761(8):878–896. https://doi.org/10.1016/j.bbalip.2006.04.011
Segui B, Allen-Baume V, Cockcroft S (2002) Phosphatidylinositol transfer protein beta displays minimal sphingomyelin transfer activity and is not required for biosynthesis and trafficking of sphingomyelin. Biochem J 366(Pt 1):23–34. https://doi.org/10.1042/BJ20020317
Senju Y, Kalimeri M, Koskela EV, Somerharju P, Zhao H, Vattulainen I, Lappalainen P (2017) Mechanistic principles underlying regulation of the actin cytoskeleton by phosphoinositides. Proc Natl Acad Sci U S A 114(43):E8977–E8986. https://doi.org/10.1073/pnas.1705032114
Servant G, Weiner OD, Herzmark P, Balla T, Sedat JW, Bourne HR (2000) Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287(5455):1037–1040
Sha B, Phillips SE, Bankaitis VA, Luo M (1998) Crystal structure of the Saccharomyces cerevisiae phosphatidylinositol-transfer protein. Nature 391(6666):506–510. https://doi.org/10.1038/35179
Shadan S, Holic R, Carvou N, Ee P, Li M, Murray-Rust J, Cockcroft S (2008) Dynamics of lipid transfer by phosphatidylinositol transfer proteins in cells. Traffic 9(10):1743–1756. https://doi.org/10.1111/j.1600-0854.2008.00794.x
Shah ZH, Jones DR, Sommer L, Foulger R, Bultsma Y, D’Santos C, Divecha N (2013) Nuclear phosphoinositides and their impact on nuclear functions. FEBS J 280(24):6295–6310. https://doi.org/10.1111/febs.12543
Shao X, Davletov BA, Sutton RB, Sudhof TC, Rizo J (1996) Bipartite Ca2+−binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273(5272):248–251
Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K, Akasaka R, Nishino Y, Toyama M, Chen L, Liu ZJ, Wang BC, Yamamoto M, Terada T, Miyazawa A, Tanaka A, Sugano S, Shirouzu M, Nagayama K, Takenawa T, Yokoyama S (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129(4):761–772. https://doi.org/10.1016/j.cell.2007.03.040
Sidhu G, Li W, Laryngakis N, Bishai E, Balla T, Southwick F (2005) Phosphoinositide 3-kinase is required for intracellular Listeria monocytogenes actin-based motility and filopod formation. J Biol Chem 280(12):11379–11386. https://doi.org/10.1074/jbc.M414533200
Silkov A, Yoon Y, Lee H, Gokhale N, Adu-Gyamfi E, Stahelin RV, Cho W, Murray D (2011) Genome-wide structural analysis reveals novel membrane binding properties of AP180 N-terminal homology (ANTH) domains. J Biol Chem 286(39):34155–34163. https://doi.org/10.1074/jbc.M111.265611
Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394(6692):494–498. https://doi.org/10.1038/28879
Simunovic M, Voth GA, Callan-Jones A, Bassereau P (2015) When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25(12):780–792. https://doi.org/10.1016/j.tcb.2015.09.005
Skoble J, Portnoy DA, Welch MD (2000) Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J Cell Biol 150(3):527–538
Skruzny M, Desfosses A, Prinz S, Dodonova SO, Gieras A, Uetrecht C, Jakobi AJ, Abella M, Hagen WJ, Schulz J, Meijers R, Rybin V, Briggs JA, Sachse C, Kaksonen M (2015) An organized co-assembly of clathrin adaptors is essential for endocytosis. Dev Cell 33(2):150–162. https://doi.org/10.1016/j.devcel.2015.02.023
Slagsvold T, Aasland R, Hirano S, Bache KG, Raiborg C, Trambaiolo D, Wakatsuki S, Stenmark H (2005) Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J Biol Chem 280(20):19600–19606. https://doi.org/10.1074/jbc.M501510200
Smirnova TI, Chadwick TG, MacArthur R, Poluektov O, Song L, Ryan MM, Schaaf G, Bankaitis VA (2006) The chemistry of phospholipid binding by the Saccharomyces cerevisiae phosphatidylinositol transfer protein Sec14p as determined by EPR spectroscopy. J Biol Chem 281(46):34897–34908. https://doi.org/10.1074/jbc.M603054200
Smirnova TI, Chadwick TG, Voinov MA, Poluektov O, van Tol J, Ozarowski A, Schaaf G, Ryan MM, Bankaitis VA (2007) Local polarity and hydrogen bonding inside the Sec14p phospholipid-binding cavity: high-field multi-frequency electron paramagnetic resonance studies. Biophys J 92(10):3686–3695. https://doi.org/10.1529/biophysj.106.097899
Smith WJ, Nassar N, Bretscher A, Cerione RA, Karplus PA (2003) Structure of the active N-terminal domain of Ezrin. Conformational and mobility changes identify keystone interactions. J Biol Chem 278(7):4949–4956. https://doi.org/10.1074/jbc.M210601200
Snoek GT, Berrie CP, Geijtenbeek TB, van der Helm HA, Cadee JA, Iurisci C, Corda D, Wirtz KW (1999) Overexpression of phosphatidylinositol transfer protein alpha in NIH3T3 cells activates a phospholipase A. J Biol Chem 274(50):35393–35399
Sohn M, Ivanova P, Brown HA, Toth DJ, Varnai P, Kim YJ, Balla T (2016) Lenz-Majewski mutations in PTDSS1 affect phosphatidylinositol 4-phosphate metabolism at ER-PM and ER-Golgi junctions. Proc Natl Acad Sci U S A 113(16):4314–4319. https://doi.org/10.1073/pnas.1525719113
Song X, Xu W, Zhang A, Huang G, Liang X, Virbasius JV, Czech MP, Zhou GW (2001) Phox homology domains specifically bind phosphatidylinositol phosphates. Biochemistry 40(30):8940–8944
Sot B, Behrmann E, Raunser S, Wittinghofer A (2013) Ras GTPase activating (RasGAP) activity of the dual specificity GAP protein Rasal requires colocalization and C2 domain binding to lipid membranes. Proc Natl Acad Sci U S A 110(1):111–116. https://doi.org/10.1073/pnas.1201658110
Stahelin RV, Long F, Diraviyam K, Bruzik KS, Murray D, Cho W (2002) Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J Biol Chem 277(29):26379–26388. https://doi.org/10.1074/jbc.M201106200
Stahelin RV, Burian A, Bruzik KS, Murray D, Cho W (2003a) Membrane binding mechanisms of the PX domains of NADPH oxidase p40phox and p47phox. J Biol Chem 278(16):14469–14479. https://doi.org/10.1074/jbc.M212579200
Stahelin RV, Long F, Peter BJ, Murray D, De Camilli P, McMahon HT, Cho W (2003b) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J Biol Chem 278(31):28993–28999. https://doi.org/10.1074/jbc.M302865200
Stahelin RV, Rafter JD, Das S, Cho W (2003c) The molecular basis of differential subcellular localization of C2 domains of protein kinase C-alpha and group IVa cytosolic phospholipase A2. J Biol Chem 278(14):12452–12460. https://doi.org/10.1074/jbc.M212864200
Stahelin RV, Ananthanarayanan B, Blatner NR, Singh S, Bruzik KS, Murray D, Cho W (2004) Mechanism of membrane binding of the phospholipase D1 PX domain. J Biol Chem 279(52):54918–54926. https://doi.org/10.1074/jbc.M407798200
Stahelin RV, Karathanassis D, Bruzik KS, Waterfield MD, Bravo J, Williams RL, Cho W (2006) Structural and membrane binding analysis of the Phox homology domain of phosphoinositide 3-kinase-C2alpha. J Biol Chem 281(51):39396–39406. https://doi.org/10.1074/jbc.M607079200
Stahelin RV, Karathanassis D, Murray D, Williams RL, Cho W (2007) Structural and membrane binding analysis of the Phox homology domain of Bem1p: basis of phosphatidylinositol 4-phosphate specificity. J Biol Chem 282(35):25737–25747. https://doi.org/10.1074/jbc.M702861200
Stahelin RV, Scott JL, Frick CT (2014) Cellular and molecular interactions of phosphoinositides and peripheral proteins. Chem Phys Lipids 182:3–18. https://doi.org/10.1016/j.chemphyslip.2014.02.002
Stauffer TP, Ahn S, Meyer T (1998) Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol 8(6):343–346
Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144(3):389–401. https://doi.org/10.1016/j.cell.2010.12.034
Steffen P, Schafer DA, David V, Gouin E, Cooper JA, Cossart P (2000) Listeria monocytogenes ActA protein interacts with phosphatidylinositol 4,5-bisphosphate in vitro. Cell Motil Cytoskeleton 45(1):58–66. https://doi.org/10.1002/(SICI)1097-0169(200001)45:1<58::AID-CM6>3.0.CO;2-Y
Stenmark H, Aasland R, Toh BH, D’Arrigo A (1996) Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem 271(39):24048–24054
Stolt PC, Jeon H, Song HK, Herz J, Eck MJ, Blacklow SC (2003) Origins of peptide selectivity and phosphoinositide binding revealed by structures of disabled-1 PTB domain complexes. Structure 11(5):569–579
Stolt PC, Vardar D, Blacklow SC (2004) The dual-function disabled-1 PTB domain exhibits site independence in binding phosphoinositide and peptide ligands. Biochemistry 43(34):10979–10987. https://doi.org/10.1021/bi049092l
Stolt PC, Chen Y, Liu P, Bock HH, Blacklow SC, Herz J (2005) Phosphoinositide binding by the disabled-1 PTB domain is necessary for membrane localization and Reelin signal transduction. J Biol Chem 280(10):9671–9677. https://doi.org/10.1074/jbc.M413356200
Stromhaug PE, Reggiori F, Guan J, Wang CW, Klionsky DJ (2004) Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell 15(8):3553–3566. https://doi.org/10.1091/mbc.E04-02-0147
Sutton RB, Davletov BA, Berghuis AM, Sudhof TC, Sprang SR (1995) Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 80(6):929–938
Szentpetery Z, Balla A, Kim YJ, Lemmon MA, Balla T (2009) Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biol 10:67. https://doi.org/10.1186/1471-2121-10-67
Takeuchi H, Kanematsu T, Misumi Y, Sakane F, Konishi H, Kikkawa U, Watanabe Y, Katan M, Hirata M (1997) Distinct specificity in the binding of inositol phosphates by pleckstrin homology domains of pleckstrin, RAC-protein kinase, diacylglycerol kinase and a new 130 kDa protein. Biochim Biophys Acta 1359(3):275–285
Takeuchi H, Matsuda M, Yamamoto T, Kanematsu T, Kikkawa U, Yagisawa H, Watanabe Y, Hirata M (1998) PTB domain of insulin receptor substrate-1 binds inositol compounds. Biochem J 334(Pt 1):211–218
Tan X, Thapa N, Choi S, Anderson RA (2015) Emerging roles of PtdIns(4,5)P2--beyond the plasma membrane. J Cell Sci 128(22):4047–4056. https://doi.org/10.1242/jcs.175208
Tani K, Kogure T, Inoue H (2012) The intracellular phospholipase A1 protein family. Biomol Concepts 3(5):471–478. https://doi.org/10.1515/bmc-2012-0014
Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL (2006) ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125(1):99–111. https://doi.org/10.1016/j.cell.2006.01.047
Thapa N, Tan X, Choi S, Lambert PF, Rapraeger AC, Anderson RA (2016) The hidden conundrum of phosphoinositide signaling in cancer. Trends Cancer 2(7):378–390. https://doi.org/10.1016/j.trecan.2016.05.009
Tilley SJ, Skippen A, Murray-Rust J, Swigart PM, Stewart A, Morgan CP, Cockcroft S, McDonald NQ (2004) Structure-function analysis of human [corrected] phosphatidylinositol transfer protein alpha bound to phosphatidylinositol. Structure 12(2):317–326. https://doi.org/10.1016/j.str.2004.01.013
Toker A, Cantley LC (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387(6634):673–676. https://doi.org/10.1038/42648
Tong J, Yang H, Yang H, Eom SH, Im YJ (2013) Structure of Osh3 reveals a conserved mode of phosphoinositide binding in oxysterol-binding proteins. Structure 21(7):1203–1213. https://doi.org/10.1016/j.str.2013.05.007
Tong J, Manik MK, Yang H, Im YJ (2016) Structural insights into nonvesicular lipid transport by the oxysterol binding protein homologue family. Biochim Biophys Acta 1861(8 Pt B):928–939. https://doi.org/10.1016/j.bbalip.2016.01.008
Tsujishita Y, Hurley JH (2000) Structure and lipid transport mechanism of a StAR-related domain. Nat Struct Biol 7(5):408–414. https://doi.org/10.1038/75192
Tsujita K, Itoh T, Ijuin T, Yamamoto A, Shisheva A, Laporte J, Takenawa T (2004) Myotubularin regulates the function of the late endosome through the gram domain-phosphatidylinositol 3,5-bisphosphate interaction. J Biol Chem 279(14):13817–13824. https://doi.org/10.1074/jbc.M312294200
Tuzi S, Uekama N, Okada M, Yamaguchi S, Saito H, Yagisawa H (2003) Structure and dynamics of the phospholipase C-delta1 pleckstrin homology domain located at the lipid bilayer surface. J Biol Chem 278(30):28019–28025. https://doi.org/10.1074/jbc.M300101200
Tyson GH, Halavaty AS, Kim H, Geissler B, Agard M, Satchell KJ, Cho W, Anderson WF, Hauser AR (2015) A novel phosphatidylinositol 4,5-bisphosphate binding domain mediates plasma membrane localization of ExoU and other patatin-like phospholipases. J Biol Chem 290(5):2919–2937. https://doi.org/10.1074/jbc.M114.611251
Uchida Y, Hasegawa J, Chinnapen D, Inoue T, Okazaki S, Kato R, Wakatsuki S, Misaki R, Koike M, Uchiyama Y, Iemura S, Natsume T, Kuwahara R, Nakagawa T, Nishikawa K, Mukai K, Miyoshi E, Taniguchi N, Sheff D, Lencer WI, Taguchi T, Arai H (2011) Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc Natl Acad Sci U S A 108(38):15846–15851. https://doi.org/10.1073/pnas.1109101108
Vadas O, Burke JE (2015) Probing the dynamic regulation of peripheral membrane proteins using hydrogen deuterium exchange-MS (HDX-MS). Biochem Soc Trans 43(5):773–786. https://doi.org/10.1042/BST20150065
van den Bogaart G, Meyenberg K, Diederichsen U, Jahn R (2012) Phosphatidylinositol 4,5-bisphosphate increases Ca2+ affinity of synaptotagmin-1 by 40-fold. J Biol Chem 287(20):16447–16453. https://doi.org/10.1074/jbc.M112.343418
van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112–124. https://doi.org/10.1038/nrm2330
Van Paridon PA, Somerharju P, Wirtz KW (1987) Phosphatidylinositol-transfer protein and cellular phosphatidylinositol metabolism. Biochem Soc Trans 15(3):321–323
Vance JE (2015) Phospholipid synthesis and transport in mammalian cells. Traffic 16(1):1–18. https://doi.org/10.1111/tra.12230
Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11(5):329–341. https://doi.org/10.1038/nrm2882
Varnai P, Balla T (1998) Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143(2):501–510
Varnai P, Rother KI, Balla T (1999) Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton’s tyrosine kinase pleckstrin homology domain visualized in single living cells. J Biol Chem 274(16):10983–10989
Varnai P, Gulyas G, Toth DJ, Sohn M, Sengupta N, Balla T (2017) Quantifying lipid changes in various membrane compartments using lipid binding protein domains. Cell Calcium 64:72–82. https://doi.org/10.1016/j.ceca.2016.12.008
Verdaguer N, Corbalan-Garcia S, Ochoa WF, Fita I, Gomez-Fernandez JC (1999) Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine. EMBO J 18(22):6329–6338. https://doi.org/10.1093/emboj/18.22.6329
Vetter IR, Nowak C, Nishimoto T, Kuhlmann J, Wittinghofer A (1999) Structure of a Ran-binding domain complexed with Ran bound to a GTP analogue: implications for nuclear transport. Nature 398(6722):39–46. https://doi.org/10.1038/17969
Vihtelic TS, Hyde DR, O’Tousa JE (1991) Isolation and characterization of the Drosophila retinal degeneration B (rdgB) gene. Genetics 127(4):761–768
Vihtelic TS, Goebl M, Milligan S, O’Tousa JE, Hyde DR (1993) Localization of Drosophila retinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J Cell Biol 122(5):1013–1022
Vollert CS, Uetz P (2004) The phox homology (PX) domain protein interaction network in yeast. Mol Cell Proteomics 3(11):1053–1064. https://doi.org/10.1074/mcp.M400081-MCP200
Vonkova I, Saliba AE, Deghou S, Anand K, Ceschia S, Doerks T, Galih A, Kugler KG, Maeda K, Rybin V, van Noort V, Ellenberg J, Bork P, Gavin AC (2015) Lipid cooperativity as a general membrane-recruitment principle for PH domains. Cell Rep 12(9):1519–1530. https://doi.org/10.1016/j.celrep.2015.07.054
Vordtriede PB, Doan CN, Tremblay JM, Helmkamp GM Jr, Yoder MD (2005) Structure of PITPbeta in complex with phosphatidylcholine: comparison of structure and lipid transfer to other PITP isoforms. Biochemistry 44(45):14760–14771. https://doi.org/10.1021/bi051191r
Walker SM, Leslie NR, Perera NM, Batty IH, Downes CP (2004) The tumour-suppressor function of PTEN requires an N-terminal lipid-binding motif. Biochem J 379(Pt 2):301–307. https://doi.org/10.1042/BJ20031839
Wang J, Gambhir A, Hangyas-Mihalyne G, Murray D, Golebiewska U, McLaughlin S (2002) Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J Biol Chem 277(37):34401–34412. https://doi.org/10.1074/jbc.M203954200
Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114(3):299–310
Wang J, Gambhir A, McLaughlin S, Murray D (2004) A computational model for the electrostatic sequestration of PI(4,5)P2 by membrane-adsorbed basic peptides. Biophys J 86(4):1969–1986. https://doi.org/10.1016/S0006-3495(04)74260-5
Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363(Pt 3):657–666
Watton SJ, Downward J (1999) Akt/PKB localisation and 3′ phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr Biol 9(8):433–436
Wawrzyniak AM, Kashyap R, Zimmermann P (2013) Phosphoinositides and PDZ domain scaffolds. Adv Exp Med Biol 991:41–57. https://doi.org/10.1007/978-94-007-6331-9_4
Weber SS, Ragaz C, Hilbi H (2009) The inositol polyphosphate 5-phosphatase OCRL1 restricts intracellular growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE. Cell Microbiol 11(3):442–460. https://doi.org/10.1111/j.1462-5822.2008.01266.x
Weber-Boyvat M, Kentala H, Peranen J, Olkkonen VM (2015) Ligand-dependent localization and function of ORP-VAP complexes at membrane contact sites. Cell Mol Life Sci 72(10):1967–1987. https://doi.org/10.1007/s00018-014-1786-x
Wei Y, Stec B, Redfield AG, Weerapana E, Roberts MF (2015) Phospholipid-binding sites of phosphatase and tensin homolog (PTEN): exploring the mechanism of phosphatidylinositol 4,5-bisphosphate activation. J Biol Chem 290(3):1592–1606. https://doi.org/10.1074/jbc.M114.588590
Weigele BA, Orchard RC, Jimenez A, Cox GW, Alto NM (2017) A systematic exploration of the interactions between bacterial effector proteins and host cell membranes. Nat Commun 8(1):532. https://doi.org/10.1038/s41467-017-00700-7
Weixel KM, Blumental-Perry A, Watkins SC, Aridor M, Weisz OA (2005) Distinct Golgi populations of phosphatidylinositol 4-phosphate regulated by phosphatidylinositol 4-kinases. J Biol Chem 280(11):10501–10508. https://doi.org/10.1074/jbc.M414304200
Welch MD, Rosenblatt J, Skoble J, Portnoy DA, Mitchison TJ (1998) Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281(5373):105–108
Welch HC, Coadwell WJ, Ellson CD, Ferguson GJ, Andrews SR, Erdjument-Bromage H, Tempst P, Hawkins PT, Stephens LR (2002) P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108(6):809–821
Whited AM, Johs A (2015) The interactions of peripheral membrane proteins with biological membranes. Chem Phys Lipids 192:51–59. https://doi.org/10.1016/j.chemphyslip.2015.07.015
Whorton MR, MacKinnon R (2011) Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147(1):199–208. https://doi.org/10.1016/j.cell.2011.07.046
Wientjes FB, Reeves EP, Soskic V, Furthmayr H, Segal AW (2001) The NADPH oxidase components p47(phox) and p40(phox) bind to moesin through their PX domain. Biochem Biophys Res Commun 289(2):382–388. https://doi.org/10.1006/bbrc.2001.5982
Williams RL, Urbe S (2007) The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 8(5):355–368. https://doi.org/10.1038/nrm2162
Wirtz KW (1991) Phospholipid transfer proteins. Annu Rev Biochem 60:73–99. https://doi.org/10.1146/annurev.bi.60.070191.000445
Wirtz KW (1997) Phospholipid transfer proteins revisited. Biochem J 324(Pt 2):353–360
Wishart MJ, Taylor GS, Dixon JE (2001) Phoxy lipids: revealing PX domains as phosphoinositide binding modules. Cell 105(7):817–820
Wong LH, Levine TP (2016) Lipid transfer proteins do their thing anchored at membrane contact sites… but what is their thing? Biochem Soc Trans 44(2):517–527. https://doi.org/10.1042/BST20150275
Wong LH, Copic A, Levine TP (2017) Advances on the transfer of lipids by lipid transfer proteins. Trends Biochem Sci 42(7):516–530. https://doi.org/10.1016/j.tibs.2017.05.001
Wu H, Feng W, Chen J, Chan LN, Huang S, Zhang M (2007) PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol Cell 28(5):886–898. https://doi.org/10.1016/j.molcel.2007.10.028
Wyckoff GJ, Solidar A, Yoden MD (2010) Phosphatidylinositol transfer proteins: sequence motifs in structural and evolutionary analyses. J Biomed Sci Eng 3(1):65–77. https://doi.org/10.4236/jbise.2010.31010
Wymann MP, Schneiter R (2008) Lipid signalling in disease. Nat Rev Mol Cell Biol 9(2):162–176. https://doi.org/10.1038/nrm2335
Xing Y, Liu D, Zhang R, Joachimiak A, Songyang Z, Xu W (2004) Structural basis of membrane targeting by the Phox homology domain of cytokine-independent survival kinase (CISK-PX). J Biol Chem 279(29):30662–30669. https://doi.org/10.1074/jbc.M404107200
Xu J, Liu D, Gill G, Songyang Z (2001) Regulation of cytokine-independent survival kinase (CISK) by the Phox homology domain and phosphoinositides. J Cell Biol 154(4):699–705. https://doi.org/10.1083/jcb.200105089
Xu C, Watras J, Loew LM (2003) Kinetic analysis of receptor-activated phosphoinositide turnover. J Cell Biol 161(4):779–791. https://doi.org/10.1083/jcb.200301070
Xu M, Arnaud L, Cooper JA (2005) Both the phosphoinositide and receptor binding activities of Dab1 are required for Reelin-stimulated Dab1 tyrosine phosphorylation. Brain Res Mol Brain Res 139(2):300–305. https://doi.org/10.1016/j.molbrainres.2005.06.001
Xu Q, Bateman A, Finn RD, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, Carlton D, Chen C, Chiu HJ, Chiu M, Clayton T, Das D, Deller MC, Duan L, Ellrott K, Ernst D, Farr CL, Feuerhelm J, Grant JC, Grzechnik A, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Marciano D, McMullan D, Miller MD, Morse AT, Nigoghossian E, Nopakun A, Okach L, Puckett C, Reyes R, Rife CL, Sefcovic N, Tien HJ, Trame CB, van den Bedem H, Weekes D, Wooten T, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA (2010) Bacterial pleckstrin homology domains: a prokaryotic origin for the PH domain. J Mol Biol 396(1):31–46. https://doi.org/10.1016/j.jmb.2009.11.006
Yadav S, Garner K, Georgiev P, Li M, Gomez-Espinosa E, Panda A, Mathre S, Okkenhaug H, Cockcroft S, Raghu P (2015) RDGBalpha, a PtdIns-PtdOH transfer protein, regulates G-protein-coupled PtdIns(4,5)P2 signalling during Drosophila phototransduction. J Cell Sci 128(17):3330–3344. https://doi.org/10.1242/jcs.173476
Yamamoto E, Kalli AC, Yasuoka K, Sansom MSP (2016) Interactions of pleckstrin homology domains with membranes: adding back the bilayer via high-throughput molecular dynamics. Structure 24(8):1421–1431. https://doi.org/10.1016/j.str.2016.06.002
Yamamoto E, Akimoto T, Kalli AC, Yasuoka K, Sansom MS (2017) Dynamic interactions between a membrane binding protein and lipids induce fluctuating diffusivity. Sci Adv 3(1):e1601871. https://doi.org/10.1126/sciadv.1601871
Yan D, Olkkonen VM (2008) Characteristics of oxysterol binding proteins. Int Rev Cytol 265:253–285. https://doi.org/10.1016/S0074-7696(07)65007-4
Yau WM, Wimley WC, Gawrisch K, White SH (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37(42):14713–14718. https://doi.org/10.1021/bi980809c
Yeung T, Terebiznik M, Yu L, Silvius J, Abidi WM, Philips M, Levine T, Kapus A, Grinstein S (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313(5785):347–351. https://doi.org/10.1126/science.1129551
Yoder MD, Thomas LM, Tremblay JM, Oliver RL, Yarbrough LR, Helmkamp GM Jr (2001) Structure of a multifunctional protein. Mammalian phosphatidylinositol transfer protein complexed with phosphatidylcholine. J Biol Chem 276(12):9246–9252. https://doi.org/10.1074/jbc.M010131200
Yoon Y, Tong J, Lee PJ, Albanese A, Bhardwaj N, Kallberg M, Digman MA, Lu H, Gratton E, Shin YK, Cho W (2010) Molecular basis of the potent membrane-remodeling activity of the epsin 1 N-terminal homology domain. J Biol Chem 285(1):531–540. https://doi.org/10.1074/jbc.M109.068015
Yoon Y, Zhang X, Cho W (2012) Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) specifically induces membrane penetration and deformation by Bin/amphiphysin/Rvs (BAR) domains. J Biol Chem 287(41):34078–34090. https://doi.org/10.1074/jbc.M112.372789
Yu JW, Lemmon MA (2001) All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate. J Biol Chem 276(47):44179–44184. https://doi.org/10.1074/jbc.M108811200
Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, DeWald DB, Murray D, Emr SD, Lemmon MA (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13(5):677–688
Yun M, Keshvara L, Park CG, Zhang YM, Dickerson JB, Zheng J, Rock CO, Curran T, Park HW (2003) Crystal structures of the Dab homology domains of mouse disabled 1 and 2. J Biol Chem 278(38):36572–36581. https://doi.org/10.1074/jbc.M304384200
Zalevsky J, Grigorova I, Mullins RD (2001) Activation of the Arp2/3 complex by the Listeria acta protein. Acta binds two actin monomers and three subunits of the Arp2/3 complex. J Biol Chem 276(5):3468–3475. https://doi.org/10.1074/jbc.M006407200
Zhao L, Ma Y, Seemann J, Huang LJ (2010) A regulating role of the JAK2 FERM domain in hyperactivation of JAK2(V617F). Biochem J 426(1):91–98. https://doi.org/10.1042/BJ20090615
Zhao H, Michelot A, Koskela EV, Tkach V, Stamou D, Drubin DG, Lappalainen P (2013) Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep 4(6):1213–1223. https://doi.org/10.1016/j.celrep.2013.08.024
Zhou MM, Fesik SW (1995) Structure and function of the phosphotyrosine binding (PTB) domain. Prog Biophys Mol Biol 64(2–3):221–235
Zhou MM, Ravichandran KS, Olejniczak EF, Petros AM, Meadows RP, Sattler M, Harlan JE, Wade WS, Burakoff SJ, Fesik SW (1995) Structure and ligand recognition of the phosphotyrosine binding domain of Shc. Nature 378(6557):584–592. https://doi.org/10.1038/378584a0
Zhou CZ, Li de La Sierra-Gallay I, Quevillon-Cheruel S, Collinet B, Minard P, Blondeau K, Henckes G, Aufrere R, Leulliot N, Graille M, Sorel I, Savarin P, de la Torre F, Poupon A, Janin J, van Tilbeurgh H (2003) Crystal structure of the yeast Phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate. J Biol Chem 278(50):50371–50376. https://doi.org/10.1074/jbc.M304392200
Zhu G, Chen J, Liu J, Brunzelle JS, Huang B, Wakeham N, Terzyan S, Li X, Rao Z, Li G, Zhang XC (2007) Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J 26(14):3484–3493. https://doi.org/10.1038/sj.emboj.7601771
Zhu Y, Hu L, Zhou Y, Yao Q, Liu L, Shao F (2010) Structural mechanism of host Rab1 activation by the bifunctional Legionella type IV effector SidM/DrrA. Proc Natl Acad Sci U S A 107(10):4699–4704. https://doi.org/10.1073/pnas.0914231107
Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7(1):9–19. https://doi.org/10.1038/nrm1784
Zimmermann P (2006) The prevalence and significance of PDZ domain-phosphoinositide interactions. Biochim Biophys Acta 1761(8):947–956. https://doi.org/10.1016/j.bbalip.2006.04.003
Zimmermann P, Meerschaert K, Reekmans G, Leenaerts I, Small JV, Vandekerckhove J, David G, Gettemans J (2002) PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol Cell 9(6):1215–1225
Zolov SN, Bridges D, Zhang Y, Lee WW, Riehle E, Verma R, Lenk GM, Converso-Baran K, Weide T, Albin RL, Saltiel AR, Meisler MH, Russell MW, Weisman LS (2012) In vivo, Pikfyve generates PI(3,5)P2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci U S A 109(43):17472–17477. https://doi.org/10.1073/pnas.1203106109
Disclosures Statement
The authors have nothing to disclose.
Sources of Research Support
TB is supported by the National Institutes of Health (NIH) Intramural Research Program (IRP). JGP is supported by an NICHD Visiting Fellowship and a Natural Sciences and Engineering Research Council of Canada (NSERC) Banting Postdoctoral Fellowship.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply
About this chapter
Cite this chapter
Pemberton, J.G., Balla, T. (2019). Polyphosphoinositide-Binding Domains: Insights from Peripheral Membrane and Lipid-Transfer Proteins. In: Atassi, M. (eds) Protein Reviews – Purinergic Receptors. Advances in Experimental Medicine and Biology(), vol 1111. Springer, Cham. https://doi.org/10.1007/5584_2018_288
Download citation
DOI: https://doi.org/10.1007/5584_2018_288
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-14338-1
Online ISBN: 978-3-030-14339-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)