Skip to main content

Advertisement

SpringerLink
Log in

Emerging roles of Golgi/endosome-localizing monomeric clathrin adaptors GGAs

  • Review Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

Abstract

GGAs (Golgi-localized, γ-adaptin ear-containing, ADP ribosylation factor [Arf]-binding proteins) are a family of ubiquitously expressed, Arf-dependent monomeric clathrin adaptor proteins, and are conserved from yeast to humans. Mammals have three GGAs (GGA1-3) that work not only at the trans-Golgi network, but also in endosomes to sort transmembrane cargo proteins such as mannose 6-phosphate receptors, sortilin, β-site amyloid precursor protein cleaving enzyme 1, and epidermal growth factor receptor. The cytoplasmic regions of these cargoes possess motifs of acidic amino acid cluster-dileucine and/or ubiquitination sites, which can be recognized by GGAs. Despite seminal investigations of the three molecules, their in vivo roles and functional redundancies, as well as relationships with a heterotetrameric adaptor protein, AP-1, which is functionally similar to GGAs were still poorly understood. Studies over the past two decades, however, discovered several new GGA cargoes, their interaction modes, and accessory proteins. These findings collectively suggest distinct and more fundamental roles of each GGA in regulating neuronal survival, lipid metabolism, and cell proliferation. This review aims to provide an update to the GGA research focusing on how GGAs became considered not only as players in the context of the TGN-endosome transport, but also as key regulators for physiologically and pathologically important phenomena.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Boman AL (2001) GGA proteins: new players in the sorting game. J Cell Sci 114:3413–3418

    CAS  PubMed  Google Scholar 

  • Boman AL, Zhang C, Zhu X, Kahn RA (2000) A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol Biol Cell 11:1241–1255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bonifacino JS (2004) The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 5:23–32

    CAS  PubMed  Google Scholar 

  • Boucher R, Larkin H, Brodeur J, Gagnon H, Theriault C, Lavoie C (2008) Intracellular trafficking of LRP9 is dependent on two acidic cluster/dileucine motifs. Histochem Cell Biol 130:315–327

    CAS  PubMed  Google Scholar 

  • Brodeur J, Theriault C, Lessard-Beaudoin M, Marcil A, Dahan S, Lavoie C (2012) LDLR-related protein 10 (LRP10) regulates amyloid precursor protein (APP) trafficking and processing: evidence for a role in Alzheimer's disease. Mol Neurodegener 7:31

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conlon DM (2019) Role of sortilin in lipid metabolism. Curr Opin Lipidol 30:198–204

    CAS  PubMed  Google Scholar 

  • Daboussi L, Costaguta G, Payne GS (2012) Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat Cell Biol 14:239–248

    CAS  PubMed  PubMed Central  Google Scholar 

  • del Castillo FJ, Cohen-Salmon M, Charollais A et al (2010) Consortin, a trans-Golgi network cargo receptor for the plasma membrane targeting and recycling of connexins. Hum Mol Genet 19:262–275

    PubMed  Google Scholar 

  • Dell'Angelica EC (2001) Clathrin-binding proteins: got a motif? Join the network! Trends Cell Biol 11:315–318

    CAS  PubMed  Google Scholar 

  • Dell'Angelica EC, Puertollano R, Mullins C et al (2000) GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol 149:81–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doray B, Bruns K, Ghosh P, Kornfeld SA (2002a) Autoinhibition of the ligand-binding site of GGA1/3 VHS domains by an internal acidic cluster-dileucine motif. Proc Natl Acad Sci USA 99:8072–8077

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doray B, Ghosh P, Griffith J, Geuze HJ, Kornfeld S (2002b) Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297:1700–1703

    CAS  PubMed  Google Scholar 

  • Doray B, Knisely JM, Wartman L, Bu G, Kornfeld S (2008) Identification of acidic dileucine signals in LRP9 that interact with both GGAs and AP-1/AP-2. Traffic 9:1551–1562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doray B, Govero J, Kornfeld S (2014) Impact of genetic background on neonatal lethality of Gga2 gene-trap mice. G3 (Bethesda) 4:885–890

    CAS  PubMed  PubMed Central  Google Scholar 

  • Escamilla M, Lee BD, Ontiveros A et al (2008) The epsin 4 gene is associated with psychotic disorders in families of Latin American origin. Schizophr Res 106:253–257

    PubMed  Google Scholar 

  • Goettsch C, Kjolby M, Aikawa E (2018) Sortilin and its multiple roles in cardiovascular and metabolic diseases. Arterioscler Thromb Vasc Biol 38:19–25

    CAS  PubMed  Google Scholar 

  • Govero J, Doray B, Bai H, Kornfeld S (2012) Analysis of Gga null mice demonstrates a non-redundant role for mammalian GGA2 during development. PLoS ONE 7:e30184

    CAS  PubMed  PubMed Central  Google Scholar 

  • He X, Chang WP, Koelsch G, Tang J (2002) Memapsin 2 (beta-secretase) cytosolic domain binds to the VHS domains of GGA1 and GGA2: implications on the endocytosis mechanism of memapsin 2. FEBS Lett 524:183–187

    CAS  PubMed  Google Scholar 

  • He X, Zhu G, Koelsch G, Rodgers KK, Zhang XC, Tang J (2003) Biochemical and structural characterization of the interaction of memapsin 2 (beta-secretase) cytosolic domain with the VHS domain of GGA proteins. Biochemistry 42:12174–12180

    CAS  PubMed  Google Scholar 

  • He X, Li F, Chang WP, Tang J (2005) GGA proteins mediate the recycling pathway of memapsin 2 (BACE). J Biol Chem 280:11696–11703

    CAS  PubMed  Google Scholar 

  • Herskowitz JH, Offe K, Deshpande A, Kahn RA, Levey AI, Lah JJ (2012) GGA1-mediated endocytic traffic of LR11/SorLA alters APP intracellular distribution and amyloid-beta production. Mol Biol Cell 23:2645–2657

    CAS  PubMed  PubMed Central  Google Scholar 

  • Herzberg I, Jasinska A, Garcia J et al (2006) Convergent linkage evidence from two Latin-American population isolates supports the presence of a susceptibility locus for bipolar disorder in 5q31-34. Hum Mol Genet 15:3146–3153

    CAS  PubMed  Google Scholar 

  • Hirst J, Lui WW, Bright NA, Totty N, Seaman MN, Robinson MS (2000) A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J Cell Biol 149:67–80

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Lindsay MR, Robinson MS (2001) GGAs: roles of the different domains and comparison with AP-1 and clathrin. Mol Biol Cell 12:3573–3588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Motley A, Harasaki K, Peak Chew SY, Robinson MS (2003) EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol Biol Cell 14:625–641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Borner GH, Harbour M, Robinson MS (2005) The aftiphilin/p200/gamma-synergin complex. Mol Biol Cell 16:2554–2565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Seaman MN, Buschow SI, Robinson MS (2007) The role of cargo proteins in GGA recruitment. Traffic 8:594–604

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Sahlender DA, Choma M et al (2009) Spatial and functional relationship of GGAs and AP-1 in Drosophila and HeLa cells. Traffic 10:1696–1710

    CAS  PubMed  Google Scholar 

  • Hirst J, Borner GH, Antrobus R et al (2012) Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr Biol 22:1711–1716

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J, Edgar JR, Borner GH et al (2015) Contributions of epsinR and gadkin to clathrin-mediated intracellular trafficking. Mol Biol Cell 26:3085–3103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Isobe M, Lee S, Waguri S, Kametaka S (2018) Clathrin adaptor GGA1 modulates myogenesis of C2C12 myoblasts. PLoS ONE 13:e0209441

    PubMed  PubMed Central  Google Scholar 

  • Jacobsen L, Madsen P, Nielsen MS et al (2002) The sorLA cytoplasmic domain interacts with GGA1 and -2 and defines minimum requirements for GGA binding. FEBS Lett 511:155–158

    CAS  PubMed  Google Scholar 

  • Kametaka S, Moriyama K, Burgos PV et al (2007) Canonical interaction of cyclin G associated kinase with adaptor protein 1 regulates lysosomal enzyme sorting. Mol Biol Cell 18:2991–3001

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang EL, Cameron AN, Piazza F, Walker KR, Tesco G (2010) Ubiquitin regulates GGA3-mediated degradation of BACE1. J Biol Chem 285:24108–24119

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim W, Ma L, Lomoio S et al (2018) BACE1 elevation engendered by GGA3 deletion increases beta-amyloid pathology in association with APP elevation and decreased CHL1 processing in 5XFAD mice. Mol Neurodegener 13:6

    PubMed  PubMed Central  Google Scholar 

  • Kzhyshkowska J, Gratchev A, Martens JH et al (2004) Stabilin-1 localizes to endosomes and the trans-Golgi network in human macrophages and interacts with GGA adaptors. J Leukoc Biol 76:1151–1161

    CAS  PubMed  Google Scholar 

  • Kzhyshkowska J, Gratchev A, Goerdt S (2006) Stabilin-1, a homeostatic scavenger receptor with multiple functions. J Cell Mol Med 10:635–649

    CAS  PubMed  Google Scholar 

  • Law IK, Bakirtzi K, Polytarchou C et al (2015) Neurotensin-regulated miR-133alpha is involved in proinflammatory signalling in human colonic epithelial cells and in experimental colitis. Gut 64:1095–1104

    CAS  PubMed  Google Scholar 

  • Li X, Lavigne P, Lavoie C (2015) GGA3 mediates TrkA endocytic recycling to promote sustained Akt phosphorylation and cell survival. Mol Biol Cell 26:4412–4426

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lippe R, Miaczynska M, Rybin V, Runge A, Zerial M (2001) Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex. Mol Biol Cell 12:2219–2228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lui WW, Collins BM, Hirst J et al (2003) Binding partners for the COOH-terminal appendage domains of the GGAs and gamma-adaptin. Mol Biol Cell 14:2385–2398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lui-Roberts WW, Ferraro F, Nightingale TD, Cutler DF (2008) Aftiphilin and gamma-synergin are required for secretagogue sensitivity of Weibel-Palade bodies in endothelial cells. Mol Biol Cell 19:5072–5081

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mardones GA, Burgos PV, Brooks DA, Parkinson-Lawrence E, Mattera R, Bonifacino JS (2007) The trans-Golgi network accessory protein p56 promotes long-range movement of GGA/clathrin-containing transport carriers and lysosomal enzyme sorting. Mol Biol Cell 18:3486–3501

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maritzen T, Zech T, Schmidt MR, Krause E, Machesky LM, Haucke V (2012) Gadkin negatively regulates cell spreading and motility via sequestration of the actin-nucleating ARP2/3 complex. Proc Natl Acad Sci USA 109:10382–10387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mattera R, Arighi CN, Lodge R, Zerial M, Bonifacino JS (2003) Divalent interaction of the GGAs with the Rabaptin-5-Rabex-5 complex. EMBO J 22:78–88

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer C, Zizioli D, Lausmann S et al (2000) mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J 19:2193–2203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer C, Eskelinen EL, Guruprasad MR, von Figura K, Schu P (2001) Mu 1A deficiency induces a profound increase in MPR300/IGF-II receptor internalization rate. J Cell Sci 114:4469–4476

    CAS  PubMed  Google Scholar 

  • Morgan DO, Edman JC, Standring DN et al (1987) Insulin-like growth factor II receptor as a multifunctional binding protein. Nature 329:301–307

    CAS  PubMed  Google Scholar 

  • Morris NJ, Ross SA, Lane WS (1998) Sortilin is the major 110-kDa protein in GLUT4 vesicles from adipocytes. J Biol Chem 273:3582–3587

    CAS  PubMed  Google Scholar 

  • Nakajima M, Takahashi A, Tsuji T et al (2014) A genome-wide association study identifies susceptibility loci for ossification of the posterior longitudinal ligament of the spine. Nat Genet 46:1012–1016

    CAS  PubMed  Google Scholar 

  • Nakayama K, Wakatsuki S (2003) The structure and function of GGAs, the traffic controllers at the TGN sorting crossroads. Cell Struct Funct 28:431–442

    CAS  PubMed  Google Scholar 

  • Navarro Negredo P, Edgar JR, Wrobel AG et al (2017) Contribution of the clathrin adaptor AP-1 subunit micro1 to acidic cluster protein sorting. J Cell Biol 216:2927–2943

    PubMed  PubMed Central  Google Scholar 

  • Neubrand VE, Will RD, Mobius W et al (2005) Gamma-BAR, a novel AP-1-interacting protein involved in post-Golgi trafficking. EMBO J 24:1122–1133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen MS, Madsen P, Christensen EI et al (2001) The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J 20:2180–2190

    CAS  PubMed  PubMed Central  Google Scholar 

  • O'farrell H, Harbourne B, Kurlawala Z et al (2019) Integrative genomic analyses identifies GGA2 as a cooperative driver of EGFR-mediated lung tumorigenesis. J Thorac Oncol 14:656–671

    PubMed  Google Scholar 

  • Pak Y, Glowacka WK, Bruce MC, Pham N, Rotin D (2006) Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. J Cell Biol 175:631–645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parachoniak CA, Luo Y, Abella JV, Keen JH, Park M (2011) GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev Cell 20:751–763

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pohlkamp T, Wasser CR, Herz J (2017) Functional roles of the interaction of APP and lipoprotein receptors. Front Mol Neurosci 10:54

    PubMed  PubMed Central  Google Scholar 

  • Poussu A, Lohi O, Lehto VP (2000) Vear, a novel Golgi-associated protein with VHS and gamma-adaptin "ear" domains. J Biol Chem 275:7176–7183

    CAS  PubMed  Google Scholar 

  • Puertollano R, Bonifacino JS (2004) Interactions of GGA3 with the ubiquitin sorting machinery. Nat Cell Biol 6:244–251

    CAS  PubMed  Google Scholar 

  • Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS (2001a) Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292:1712–1716

    CAS  PubMed  Google Scholar 

  • Puertollano R, Randazzo PA, Presley JF, Hartnell LM, Bonifacino JS (2001b) The GGAs promote ARF-dependent recruitment of clathrin to the TGN. Cell 105:93–102

    CAS  PubMed  Google Scholar 

  • Puertollano R, van Der Wel NN, Greene LE, Eisenberg E, Peters PJ, Bonifacino JS (2003) Morphology and dynamics of clathrin/GGA1-coated carriers budding from the trans-Golgi network. Mol Biol Cell 14:1545–1557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ratcliffe CD, Sahgal P, Parachoniak CA, Ivaska J, Park M (2016) Regulation of cell migration and beta1 integrin trafficking by the endosomal adaptor GGA3. Traffic 17:670–688

    CAS  PubMed  Google Scholar 

  • Robinson MS, Sahlender DA, Foster SD (2010) Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev Cell 18:324–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sahgal P, Alanko J, Icha J et al (2019) GGA2 and RAB13 promote activity-dependent beta1-integrin recycling. J Cell Sci 2019:132

    Google Scholar 

  • Santonico E, Mattioni A, Panni S et al (2015) RNF11 is a GGA protein cargo and acts as a molecular adaptor for GGA3 ubiquitination mediated by Itch. Oncogene 34:3377–3390

    CAS  PubMed  Google Scholar 

  • Schmidt MR, Maritzen T, Kukhtina V et al (2009) Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc Natl Acad Sci USA 106:15344–15349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scott PM, Bilodeau PS, Zhdankina O et al (2004) GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat Cell Biol 6:252–259

    CAS  PubMed  Google Scholar 

  • Shi J, Huang G, Kandror KV (2008) Self-assembly of Glut4 storage vesicles during differentiation of 3T3-L1 adipocytes. J Biol Chem 283:30311–30321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shiba Y, Katoh Y, Shiba T et al (2004) GAT (GGA and Tom1) domain responsible for ubiquitin binding and ubiquitination. J Biol Chem 279:7105–7111

    CAS  PubMed  Google Scholar 

  • Stauber T, Jentsch TJ (2010) Sorting motifs of the endosomal/lysosomal CLC chloride transporters. J Biol Chem 285:34537–34548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takatsu H, Yoshino K, Nakayama K (2000) Adaptor gamma ear homology domain conserved in gamma-adaptin and GGA proteins that interact with gamma-synergin. Biochem Biophys Res Commun 271:719–725

    CAS  PubMed  Google Scholar 

  • Takatsu H, Katoh Y, Shiba Y, Nakayama K (2001) Golgi-localizing, gamma-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J Biol Chem 276:28541–28545

    CAS  PubMed  Google Scholar 

  • Talbot H, Saada S, Naves T, Gallet PF, Fauchais AL, Jauberteau MO (2018) Regulatory roles of sortilin and SorLA in immune-related processes. Front Pharmacol 9:1507

    CAS  PubMed  Google Scholar 

  • Tesco G, Koh YH, Kang EL et al (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54:721–737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Traub LM (2005) Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim Biophys Acta 1744:415–437

    CAS  PubMed  Google Scholar 

  • Trusolino L, Bertotti A, Comoglio PM (2010) MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol 11:834–848

    CAS  PubMed  Google Scholar 

  • Uemura T, Kametaka S, Waguri S (2018a) GGA2 interacts with EGFR cytoplasmic domain to stabilize the receptor expression and promote cell growth. Sci Rep 8:1368

    PubMed  PubMed Central  Google Scholar 

  • Uemura T, Sawada N, Sakaba T, Kametaka S, Yamamoto M, Waguri S (2018b) Intracellular localization of GGA accessory protein p56 in cell lines and central nervous system neurons. Biomed Res 39:179–187

    CAS  PubMed  Google Scholar 

  • von Einem B, Wahler A, Schips T et al (2015) The Golgi-localized gamma-ear-containing ARF-binding (GGA) proteins alter amyloid-beta precursor protein (APP) processing through interaction of their GAE domain with the beta-site APP cleaving enzyme 1 (BACE1). PLoS ONE 10:e0129047

    Google Scholar 

  • Wakasugi M, Waguri S, Kametaka S et al (2003) Predominant expression of the short form of GGA3 in human cell lines and tissues. Biochem Biophys Res Commun 306:687–692

    CAS  PubMed  Google Scholar 

  • Walker KR, Kang EL, Whalen MJ, Shen Y, Tesco G (2012) Depletion of GGA1 and GGA3 mediates postinjury elevation of BACE1. J Neurosci 32:10423–10437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Willnow TE, Petersen CM, Nykjaer A (2008) VPS10P-domain receptors—regulators of neuronal viability and function. Nat Rev Neurosci 9:899–909

    CAS  PubMed  Google Scholar 

  • Yogosawa S, Kawasaki M, Wakatsuki S et al (2006) Monoubiquitylation of GGA3 by hVPS18 regulates its ubiquitin-binding ability. Biochem Biophys Res Commun 350:82–90

    CAS  PubMed  Google Scholar 

  • Zhang M, Davis JE, Li C et al (2016a) GGA3 interacts with a G protein-coupled receptor and modulates its cell surface export. Mol Cell Biol 36:1152–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Huang W, Gao J, Terry AV, Wu G (2016b) Regulation of alpha2B-adrenergic receptor cell surface transport by GGA1 and GGA2. Sci Rep 6:37921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Doray B, Poussu A, Lehto VP, Kornfeld S (2001) Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 292:1716–1718

    CAS  PubMed  Google Scholar 

  • Zizioli D, Meyer C, Guhde G, Saftig P, von Figura K, Schu P (1999) Early embryonic death of mice deficient in gamma-adaptin. J Biol Chem 274:5385–5390

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the members of Department of Anatomy and Histology for their assistance with their field of work. This study was supported by JSPS KAKENHI Grant numbers 24659088 (to S. Waguri) and 26830080 (to T. Uemura), and by grants from Fukushima Medical University (to T. Uemura and S. Waguri), Takeda Science Foundation (to S. Waguri), and The Osaka Foundation for Promotion of Fundamental Medical Research (to S. Waguri).

Author information

Authors and Affiliations

  1. Department of Anatomy and Histology, Fukushima Medical University School of Medicine, 1 Hikariga-oka, Fukushima City, 960-1295, Fukushima, Japan

    Takefumi Uemura & Satoshi Waguri

Authors
  1. Takefumi Uemura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Satoshi Waguri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takefumi Uemura.

Ethics declarations

Conflict of interest

Satoshi Waguri has received research grants from Takeda Science Foundation and The Osaka Foundation for Promotion of Fundamental Medical Research.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uemura, T., Waguri, S. Emerging roles of Golgi/endosome-localizing monomeric clathrin adaptors GGAs. Anat Sci Int 95, 12–21 (2020). https://doi.org/10.1007/s12565-019-00505-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12565-019-00505-2

Keywords

Search

Navigation