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On the move: endocytic trafficking in cell migration

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Abstract

Directed cell migration is a fundamental process underlying diverse physiological and pathophysiological phenomena ranging from wound healing and induction of immune responses to cancer metastasis. Recent advances reveal that endocytic trafficking contributes to cell migration in multiple ways. (1) At the level of chemokines and chemokine receptors: internalization of chemokines by scavenger receptors is essential for shaping chemotactic gradients in tissue, whereas endocytosis of chemokine receptors and their subsequent recycling is key for maintaining a high responsiveness of migrating cells. (2) At the level of integrin trafficking and focal adhesion dynamics: endosomal pathways do not only modulate adhesion by delivering integrins to their site of action, but also by supplying factors for focal adhesion disassembly. (3) At the level of extracellular matrix reorganization: endosomal transport contributes to tumor cell migration not only by targeting integrins to invadosomes but also by delivering membrane type 1 matrix metalloprotease to the leading edge facilitating proteolysis-dependent chemotaxis. Consequently, numerous endocytic and endosomal factors have been shown to modulate cell migration. In fact key modulators of endocytic trafficking turn out to be also key regulators of cell migration. This review will highlight the recent progress in unraveling the contribution of cellular trafficking pathways to cell migration.

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References

  1. Majumdar R, Sixt M, Parent CA (2014) New paradigms in the establishment and maintenance of gradients during directed cell migration. Curr Opin Cell Biol 30C:33–40

    Google Scholar 

  2. Rot A (1993) Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur J Immunol 23(1):303–306

    CAS  PubMed  Google Scholar 

  3. Sarris M, Masson JB, Maurin D, Van der Aa LM, Boudinot P, Lortat-Jacob H, Herbomel P (2012) Inflammatory chemokines direct and restrict leukocyte migration within live tissues as glycan-bound gradients. Current Biol CB 22(24):2375–2382

    CAS  Google Scholar 

  4. Weber M, Hauschild R, Schwarz J, Moussion C, de Vries I, Legler DF, Luther SA, Bollenbach T, Sixt M (2013) Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 339(6117):328–332

    CAS  PubMed  Google Scholar 

  5. Shulman Z, Cohen SJ, Roediger B, Kalchenko V, Jain R, Grabovsky V, Klein E, Shinder V, Stoler-Barak L, Feigelson SW, Meshel T, Nurmi SM, Goldstein I, Hartley O, Gahmberg CG, Etzioni A, Weninger W, Ben-Baruch A, Alon R (2012) Transendothelial migration of lymphocytes mediated by intraendothelial vesicle stores rather than by extracellular chemokine depots. Nat Immunol 13(1):67–76

    CAS  Google Scholar 

  6. Wolf M, Albrecht S, Marki C (2008) Proteolytic processing of chemokines: implications in physiological and pathological conditions. Int J Biochem Cell Biol 40(6–7):1185–1198

    CAS  PubMed  Google Scholar 

  7. Van den Steen PE, Proost P, Wuyts A, Van Damme J, Opdenakker G (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 96(8):2673–2681

    PubMed  Google Scholar 

  8. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132(3):463–473

    CAS  PubMed  Google Scholar 

  9. Dona E, Barry JD, Valentin G, Quirin C, Khmelinskii A, Kunze A, Durdu S, Newton LR, Fernandez-Minan A, Huber W, Knop M, Gilmour D (2013) Directional tissue migration through a self-generated chemokine gradient. Nature 503:285–289

    CAS  PubMed  Google Scholar 

  10. Venkiteswaran G, Lewellis SW, Wang J, Reynolds E, Nicholson C, Knaut H (2013) Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue. Cell 155(3):674–687

    CAS  PubMed  Google Scholar 

  11. Ulvmar MH, Werth K, Braun A, Kelay P, Hub E, Eller K, Chan L, Lucas B, Novitzky-Basso I, Nakamura K, Rulicke T, Nibbs RJ, Worbs T, Forster R, Rot A (2014) The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes. Nat Immunol 15(7):623–630

    CAS  PubMed  Google Scholar 

  12. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8(11):1255–1265

    CAS  PubMed  Google Scholar 

  13. Bachelerie F, Ben-Baruch A, Burkhardt AM, Combadiere C, Farber JM, Graham GJ, Horuk R, Sparre-Ulrich AH, Locati M, Luster AD, Mantovani A, Matsushima K, Murphy PM, Nibbs R, Nomiyama H, Power CA, Proudfoot AE, Rosenkilde MM, Rot A, Sozzani S, Thelen M, Yoshie O, Zlotnik A (2014) International Union of Pharmacology. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol Rev 66(1):1–79

    PubMed Central  PubMed  Google Scholar 

  14. Volpe S, Cameroni E, Moepps B, Thelen S, Apuzzo T, Thelen M (2012) CCR2 acts as scavenger for CCL2 during monocyte chemotaxis. PLoS One 7(5):e37208

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Neel NF, Schutyser E, Sai J, Fan GH, Richmond A (2005) Chemokine receptor internalization and intracellular trafficking. Cytokine Growth Factor Rev 16(6):637–658

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Borroni EM, Mantovani A, Locati M, Bonecchi R (2010) Chemokine receptors intracellular trafficking. Pharmacol Ther 127(1):1–8

    CAS  PubMed  Google Scholar 

  17. 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

    CAS  PubMed  Google Scholar 

  18. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525

    CAS  PubMed  Google Scholar 

  19. Otero C, Groettrup M, Legler DF (2006) Opposite fate of endocytosed CCR7 and its ligands: recycling versus degradation. J Immunol 177(4):2314–2323

    CAS  PubMed  Google Scholar 

  20. Charest-Morin X, Pepin R, Gagne-Henley A, Morissette G, Lodge R, Marceau F (2013) C-C chemokine receptor-7 mediated endocytosis of antibody cargoes into intact cells. Front Pharmacol 4:122

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Schaeuble K, Hauser MA, Rippl AV, Bruderer R, Otero C, Groettrup M, Legler DF (2012) Ubiquitylation of the chemokine receptor CCR7 enables efficient receptor recycling and cell migration. J Cell Sci 125(Pt 19):4463–4474

    CAS  PubMed  Google Scholar 

  22. Fan GH, Lapierre LA, Goldenring JR, Sai J, Richmond A (2004) Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol Biol Cell 15(5):2456–2469

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Raman D, Sai J, Hawkins O, Richmond A (2014) Adaptor protein2 (AP2) orchestrates CXCR2-mediated cell migration. Traffic 15(4):451–469

    PubMed Central  CAS  PubMed  Google Scholar 

  24. Lagane B, Chow KY, Balabanian K, Levoye A, Harriague J, Planchenault T, Baleux F, Gunera-Saad N, Arenzana-Seisdedos F, Bachelerie F (2008) CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood 112(1):34–44

    CAS  PubMed  Google Scholar 

  25. Roland J, Murphy BJ, Ahr B, Robert-Hebmann V, Delauzun V, Nye KE, Devaux C, Biard-Piechaczyk M (2003) Role of the intracellular domains of CXCR4 in SDF-1-mediated signaling. Blood 101(2):399–406

    CAS  PubMed  Google Scholar 

  26. Minina S, Reichman-Fried M, Raz E (2007) Control of receptor internalization, signaling level, and precise arrival at the target in guided cell migration. Curr Biol 17(13):1164–1172

    CAS  PubMed  Google Scholar 

  27. Marchese A, Raiborg C, Santini F, Keen JH, Stenmark H, Benovic JL (2003) The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev Cell 5(5):709–722

    CAS  PubMed  Google Scholar 

  28. Jekely G, Sung HH, Luque CM, Rorth P (2005) Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev Cell 9(2):197–207

    CAS  PubMed  Google Scholar 

  29. Rorth P (2002) Initiating and guiding migration: lessons from border cells. Trends Cell Biol 12(7):325–331

    CAS  PubMed  Google Scholar 

  30. Duchek P, Rorth P (2001) Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291(5501):131–133

    CAS  PubMed  Google Scholar 

  31. Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P (2001) Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107(1):17–26

    CAS  PubMed  Google Scholar 

  32. Assaker G, Ramel D, Wculek SK, Gonzalez-Gaitan M, Emery G (2010) Spatial restriction of receptor tyrosine kinase activity through a polarized endocytic cycle controls border cell migration. Proc Natl Acad Sci USA 107(52):22558–22563

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Kawada K, Upadhyay G, Ferandon S, Janarthanan S, Hall M, Vilardaga JP, Yajnik V (2009) Cell migration is regulated by platelet-derived growth factor receptor endocytosis. Mol Cell Biol 29(16):4508–4518

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Sadowski L, Jastrzebski K, Kalaidzidis Y, Heldin CH, Hellberg C, Miaczynska M (2013) Dynamin inhibitors impair endocytosis and mitogenic signaling of PDGF. Traffic 14(6):725–736

    PubMed Central  PubMed  Google Scholar 

  35. Hellberg C, Schmees C, Karlsson S, Ahgren A, Heldin CH (2009) Activation of protein kinase C alpha is necessary for sorting the PDGF beta-receptor to Rab4a-dependent recycling. Mol Biol Cell 20(12):2856–2863

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Belleudi F, Scrofani C, Torrisi MR, Mancini P (2011) Polarized endocytosis of the keratinocyte growth factor receptor in migrating cells: role of SRC-signaling and cortactin. PLoS One 6(12):e29159

    PubMed Central  CAS  PubMed  Google Scholar 

  37. Mutch LJ, Howden JD, Jenner EP, Poulter NS, Rappoport JZ (2014) Polarised clathrin-mediated endocytosis of EGFR during chemotactic invasion. Traffic 15(6):648–664

    PubMed Central  CAS  PubMed  Google Scholar 

  38. Runkle KB, Meyerkord CL, Desai NV, Takahashi Y, Wang HG (2012) Bif-1 suppresses breast cancer cell migration by promoting EGFR endocytic degradation. Cancer Biol Ther 13(10):956–966

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Li MY, Lai PL, Chou YT, Chi AP, Mi YZ, Khoo KH, Chang GD, Wu CW, Meng TC, Chen GC (2014) Protein tyrosine phosphatase PTPN3 inhibits lung cancer cell proliferation and migration by promoting EGFR endocytic degradation. Oncogene. doi:10.1038/onc.2014.312

    Google Scholar 

  40. de Graauw M, Cao L, Winkel L, van Miltenburg MH, le Devedec SE, Klop M, Yan K, Pont C, Rogkoti VM, Tijsma A, Chaudhuri A, Lalai R, Price L, Verbeek F, van de Water B (2014) Annexin A2 depletion delays EGFR endocytic trafficking via cofilin activation and enhances EGFR signaling and metastasis formation. Oncogene 33(20):2610–2619

  41. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC (2008) Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 183(1):143–155

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP (2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134(1):135–147

    CAS  PubMed  Google Scholar 

  43. Ramel D, Wang X, Laflamme C, Montell DJ, Emery G (2013) Rab11 regulates cell-cell communication during collective cell movements. Nat Cell Biol 15(3):317–324

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Osmani N, Peglion F, Chavrier P, Etienne-Manneville S (2010) Cdc42 localization and cell polarity depend on membrane traffic. J Cell Biol 191(7):1261–1269

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Bretscher MS (1996) Moving membrane up to the front of migrating cells. Cell 85(4):465–467

    CAS  PubMed  Google Scholar 

  46. Palecek SP, Schmidt CE, Lauffenburger DA, Horwitz AF (1996) Integrin dynamics on the tail region of migrating fibroblasts. J Cell Sci 109(Pt 5):941–952

    CAS  PubMed  Google Scholar 

  47. Wieffer M, Maritzen T, Haucke V (2009) SnapShot: endocytic trafficking. Cell 137(2):382 (e381–383)

    CAS  PubMed  Google Scholar 

  48. Rappoport JZ, Simon SM (2003) Real-time analysis of clathrin-mediated endocytosis during cell migration. J Cell Sci 116(Pt 5):847–855

    CAS  PubMed  Google Scholar 

  49. Nishimura T, Kaibuchi K (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13(1):15–28

    CAS  PubMed  Google Scholar 

  50. Howes MT, Kirkham M, Riches J, Cortese K, Walser PJ, Simpson F, Hill MM, Jones A, Lundmark R, Lindsay MR, Hernandez-Deviez DJ, Hadzic G, McCluskey A, Bashir R, Liu L, Pilch P, McMahon H, Robinson PJ, Hancock JF, Mayor S, Parton RG (2010) Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol 190(4):675–691

    PubMed Central  CAS  PubMed  Google Scholar 

  51. Grande-Garcia A, del Pozo MA (2008) Caveolin-1 in cell polarization and directional migration. Eur J Cell Biol 87(8–9):641–647

    CAS  PubMed  Google Scholar 

  52. Beardsley A, Fang K, Mertz H, Castranova V, Friend S, Liu J (2005) Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J Biol Chem 280(5):3541–3547

    CAS  PubMed  Google Scholar 

  53. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168(3):465–476

    PubMed Central  CAS  PubMed  Google Scholar 

  54. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2(4):411–423

    CAS  PubMed  Google Scholar 

  55. Bitsikas V, Correa IR Jr, Nichols BJ (2014) Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife 3:e03970

    PubMed Central  PubMed  Google Scholar 

  56. Traynor D, Kay RR (2007) Possible roles of the endocytic cycle in cell motility. J Cell Sci 120(Pt 14):2318–2327

    CAS  PubMed  Google Scholar 

  57. Razidlo GL, Wang Y, Chen J, Krueger EW, Billadeau DD, McNiven MA (2013) Dynamin 2 potentiates invasive migration of pancreatic tumor cells through stabilization of the Rac1 GEF Vav1. Dev Cell 24(6):573–585

    PubMed Central  CAS  PubMed  Google Scholar 

  58. Gautier JJ, Lomakina ME, Bouslama-Oueghlani L, Derivery E, Beilinson H, Faigle W, Loew D, Louvard D, Echard A, Alexandrova AY, Baum B, Gautreau A (2011) Clathrin is required for scar/wave-mediated lamellipodium formation. J Cell Sci 124(Pt 20):3414–3427

    CAS  PubMed  Google Scholar 

  59. Montagnac G, Meas-Yedid V, Irondelle M, Castro-Castro A, Franco M, Shida T, Nachury MV, Benmerah A, Olivo-Marin JC, Chavrier P (2013) alphaTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature 502(7472):567–570

    PubMed Central  CAS  PubMed  Google Scholar 

  60. Maritzen T, Schmidt MR, Kukhtina V, Higman VA, Strauss H, Volkmer R, Oschkinat H, Dotti CG, Haucke V (2010) A novel subtype of AP-1-binding motif within the palmitoylated trans-Golgi network/endosomal accessory protein Gadkin/gamma-BAR. J Biol Chem 285(6):4074–4086

    PubMed Central  CAS  PubMed  Google Scholar 

  61. Schmidt MR, Maritzen T, Kukhtina V, Higman VA, Doglio L, Barak NN, Strauss H, Oschkinat H, Dotti CG, Haucke V (2009) Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc Natl Acad Sci USA 106(36):15344–15349

    PubMed Central  CAS  PubMed  Google Scholar 

  62. 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(26):10382–10387

    PubMed Central  CAS  PubMed  Google Scholar 

  63. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11(9):633–643

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Zaidel-Bar R, Geiger B (2010) The switchable integrin adhesome. J Cell Sci 123(Pt 9):1385–1388

    PubMed Central  CAS  PubMed  Google Scholar 

  65. Caswell PT, Norman JC (2006) Integrin trafficking and the control of cell migration. Traffic 7(1):14–21

    CAS  PubMed  Google Scholar 

  66. Arjonen A, Alanko J, Veltel S, Ivaska J (2012) Distinct recycling of active and inactive beta1 integrins. Traffic 13(4):610–625

    PubMed Central  CAS  PubMed  Google Scholar 

  67. Caswell P, Norman J (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18(6):257–263

    CAS  PubMed  Google Scholar 

  68. Caswell PT, Vadrevu S, Norman JC (2009) Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10(12):843–853

    CAS  PubMed  Google Scholar 

  69. Ivaska J, Heino J (2011) Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu Rev Cell Dev Biol 27:291–320

    CAS  PubMed  Google Scholar 

  70. Bridgewater RE, Norman JC, Caswell PT (2012) Integrin trafficking at a glance. J Cell Sci 125(Pt 16):3695–3701

    PubMed Central  CAS  PubMed  Google Scholar 

  71. Teckchandani A, Toida N, Goodchild J, Henderson C, Watts J, Wollscheid B, Cooper JA (2009) Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J Cell Biol 186(1):99–111

    PubMed Central  CAS  PubMed  Google Scholar 

  72. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187(5):733–747

    PubMed Central  CAS  PubMed  Google Scholar 

  73. Zhou P, Alfaro J, Chang EH, Zhao X, Porcionatto M, Segal RA (2011) Numb links extracellular cues to intracellular polarity machinery to promote chemotaxis. Dev Cell 20(5):610–622

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Bottcher RT, Stremmel C, Meves A, Meyer H, Widmaier M, Tseng HY, Fassler R (2012) Sorting nexin 17 prevents lysosomal degradation of beta1 integrins by binding to the beta1-integrin tail. Nat Cell Biol 14(6):584–592

    PubMed  Google Scholar 

  75. Danen EH, van Rheenen J, Franken W, Huveneers S, Sonneveld P, Jalink K, Sonnenberg A (2005) Integrins control motile strategy through a Rho-cofilin pathway. J Cell Biol 169(3):515–526

    PubMed Central  CAS  PubMed  Google Scholar 

  76. Jacquemet G, Green DM, Bridgewater RE, von Kriegsheim A, Humphries MJ, Norman JC, Caswell PT (2013) RCP-driven alpha5beta1 recycling suppresses Rac and promotes RhoA activity via the RacGAP1-IQGAP1 complex. J Cell Biol 202(6):917–935

    PubMed Central  CAS  PubMed  Google Scholar 

  77. Broussard JA, Lin WH, Majumdar D, Anderson B, Eason B, Brown CM, Webb DJ (2012) The endosomal adaptor protein APPL1 impairs the turnover of leading edge adhesions to regulate cell migration. Mol Biol Cell 23(8):1486–1499

    PubMed Central  CAS  PubMed  Google Scholar 

  78. Morgan MR, Hamidi H, Bass MD, Warwood S, Ballestrem C, Humphries MJ (2013) Syndecan-4 phosphorylation is a control point for integrin recycling. Dev Cell 24(5):472–485

    PubMed Central  CAS  PubMed  Google Scholar 

  79. Theisen U, Straube E, Straube A (2012) Directional persistence of migrating cells requires Kif1C-mediated stabilization of trailing adhesions. Dev Cell 23(6):1153–1166

    CAS  PubMed  Google Scholar 

  80. Eskova A, Knapp B, Matelska D, Reusing S, Arjonen A, Lisauskas T, Pepperkok R, Russell R, Eils R, Ivaska J, Kaderali L, Erfle H, Starkuviene V (2014) An RNAi screen identifies KIF15 as a novel regulator of the endocytic trafficking of integrin. J Cell Sci 127(Pt 11):2433–2447

    CAS  PubMed  Google Scholar 

  81. Jahn R, Scheller RH (2006) SNAREs—engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631–643

    CAS  PubMed  Google Scholar 

  82. Rapaport D, Lugassy Y, Sprecher E, Horowitz M (2010) Loss of SNAP29 impairs endocytic recycling and cell motility. PLoS One 5(3):e9759

    PubMed Central  PubMed  Google Scholar 

  83. Riggs KA, Hasan N, Humphrey D, Raleigh C, Nevitt C, Corbin D, Hu C (2012) Regulation of integrin endocytic recycling and chemotactic cell migration by syntaxin 6 and VAMP3 interaction. J Cell Sci 125(Pt 16):3827–3839

    PubMed Central  CAS  PubMed  Google Scholar 

  84. Nishikimi A, Ishihara S, Ozawa M, Etoh K, Fukuda M, Kinashi T, Katagiri K (2014) Rab13 acts downstream of the kinase Mst1 to deliver the integrin LFA-1 to the cell surface for lymphocyte trafficking. Sci Signal 7(336):ra72

    PubMed  Google Scholar 

  85. Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, Critchley DR, Huttenlocher A (2004) Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat Cell Biol 6(10):977–983

    CAS  PubMed  Google Scholar 

  86. Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583(8):1337–1343

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Chao WT, Ashcroft F, Daquinag AC, Vadakkan T, Wei Z, Zhang P, Dickinson ME, Kunz J (2010) Type I phosphatidylinositol phosphate kinase beta regulates focal adhesion disassembly by promoting beta1 integrin endocytosis. Mol Cell Biol 30(18):4463–4479

    PubMed Central  CAS  PubMed  Google Scholar 

  88. Ezratty EJ, Partridge MA, Gundersen GG (2005) Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7(6):581–590

    CAS  PubMed  Google Scholar 

  89. Stehbens SJ, Paszek M, Pemble H, Ettinger A, Gierke S, Wittmann T (2014) CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat Cell Biol 16(6):561–573

    PubMed Central  CAS  PubMed  Google Scholar 

  90. Schiefermeier N, Scheffler JM, de Araujo ME, Stasyk T, Yordanov T, Ebner HL, Offterdinger M, Munck S, Hess MW, Wickstrom SA, Lange A, Wunderlich W, Fassler R, Teis D, Huber LA (2014) The late endosomal p14-MP1 (LAMTOR2/3) complex regulates focal adhesion dynamics during cell migration. J Cell Biol 205(4):525–540

    PubMed Central  CAS  PubMed  Google Scholar 

  91. Biname F, Sakry D, Dimou L, Jolivel V, Trotter J (2013) NG2 regulates directional migration of oligodendrocyte precursor cells via Rho GTPases and polarity complex proteins. J Neurosci Off J Soc Neurosci 33(26):10858–10874

    CAS  Google Scholar 

  92. Morgan MR, Humphries MJ, Bass MD (2007) Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8(12):957–969

    PubMed Central  CAS  PubMed  Google Scholar 

  93. Jacquemet G, Humphries MJ, Caswell PT (2013) Role of adhesion receptor trafficking in 3D cell migration. Curr Opin Cell Biol 25(5):627–632

    PubMed Central  CAS  PubMed  Google Scholar 

  94. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, Coomans C, Schulz J, N’Kuli F, Courtoy PJ, David G (2005) Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev Cell 9(3):377–388

    CAS  PubMed  Google Scholar 

  95. Kawauchi T (2012) Cell Adhesion and Its Endocytic Regulation in Cell Migration during Neural Development and Cancer Metastasis. Int J Mol Sci 13(4):4564–4590

    PubMed Central  CAS  PubMed  Google Scholar 

  96. Baum B, Settleman J, Quinlan MP (2008) Transitions between epithelial and mesenchymal states in development and disease. Semin Cell Dev Biol 19(3):294–308

    CAS  PubMed  Google Scholar 

  97. Delva E, Kowalczyk AP (2009) Regulation of cadherin trafficking. Traffic 10(3):259–267

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Miyashita Y, Ozawa M (2007) Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J Biol Chem 282(15):11540–11548

    CAS  PubMed  Google Scholar 

  99. Sato K, Watanabe T, Wang S, Kakeno M, Matsuzawa K, Matsui T, Yokoi K, Murase K, Sugiyama I, Ozawa M, Kaibuchi K (2011) Numb controls E-cadherin endocytosis through p120 catenin with aPKC. Mol Biol Cell 22(17):3103–3119

    PubMed Central  CAS  PubMed  Google Scholar 

  100. Wang Z, Sandiford S, Wu C, Li SS (2009) Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J 28(16):2360–2373

    PubMed Central  CAS  PubMed  Google Scholar 

  101. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J, Sommer T, Birchmeier W (2002) Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 4(3):222–231

    CAS  PubMed  Google Scholar 

  102. Palacios F, Tushir JS, Fujita Y, D’Souza-Schorey C (2005) Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol 25(1):389–402

    PubMed Central  CAS  PubMed  Google Scholar 

  103. Yang DH, Cai KQ, Roland IH, Smith ER, Xu XX (2007) Disabled-2 is an epithelial surface positioning gene. J Biol Chem 282(17):13114–13122

    CAS  PubMed  Google Scholar 

  104. Kimura T, Sakisaka T, Baba T, Yamada T, Takai Y (2006) Involvement of the Ras-Ras-activated Rab5 guanine nucleotide exchange factor RIN2-Rab5 pathway in the hepatocyte growth factor-induced endocytosis of E-cadherin. J Biol Chem 281(15):10598–10609

    CAS  PubMed  Google Scholar 

  105. Palacios F, Price L, Schweitzer J, Collard JG, D’Souza-Schorey C (2001) An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 20(17):4973–4986

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Palacios F, Schweitzer JK, Boshans RL, D’Souza-Schorey C (2002) ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat Cell Biol 4(12):929–936

    CAS  PubMed  Google Scholar 

  107. Georgiou M, Marinari E, Burden J, Baum B (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Current Biol CB 18(21):1631–1638

    CAS  Google Scholar 

  108. Ling K, Bairstow SF, Carbonara C, Turbin DA, Huntsman DG, Anderson RA (2007) Type I gamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J Cell Biol 176(3):343–353

    PubMed Central  CAS  PubMed  Google Scholar 

  109. Yabuta T, Shinmura K, Tani M, Yamaguchi S, Yoshimura K, Katai H, Nakajima T, Mochiki E, Tsujinaka T, Takami M, Hirose K, Yamaguchi A, Takenoshita S, Yokota J (2002) E-cadherin gene variants in gastric cancer families whose probands are diagnosed with diffuse gastric cancer. Int J Cancer 101(5):434–441

    CAS  PubMed  Google Scholar 

  110. Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77–91

    CAS  PubMed  Google Scholar 

  111. Schill NJ, Hedman AC, Choi S, Anderson RA (2014) Isoform 5 of PIPKIgamma regulates the endosomal trafficking and degradation of E-cadherin. J Cell Sci 127(Pt 10):2189–2203

    CAS  PubMed  Google Scholar 

  112. Solis GP, Hulsbusch N, Radon Y, Katanaev VL, Plattner H, Stuermer CA (2013) Reggies/flotillins interact with Rab11a and SNX4 at the tubulovesicular recycling compartment and function in transferrin receptor and E-cadherin trafficking. Mol Biol Cell 24(17):2689–2702

    PubMed Central  CAS  PubMed  Google Scholar 

  113. Allaire PD, Seyed Sadr M, Chaineau M, Seyed Sadr E, Konefal S, Fotouhi M, Maret D, Ritter B, Del Maestro RF, McPherson PS (2013) Interplay between Rab35 and Arf6 controls cargo recycling to coordinate cell adhesion and migration. J Cell Sci 126(Pt 3):722–731

    CAS  PubMed  Google Scholar 

  114. Bonnans C, Chou J, Werb Z (2014) Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 15(12):786–801

    PubMed Central  CAS  PubMed  Google Scholar 

  115. Wolf K, Te Lindert M, Krause M, Alexander S, Te Riet J, Willis AL, Hoffman RM, Figdor CG, Weiss SJ, Friedl P (2013) Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol 201(7):1069–1084

    PubMed Central  CAS  PubMed  Google Scholar 

  116. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9(8):893–904

    CAS  PubMed  Google Scholar 

  117. Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, Schwarz JP, Spence H, Futo K, Timpson P, Nixon C, Ma Y, Anton IM, Visegrady B, Insall RH, Oien K, Blyth K, Norman JC, Machesky LM (2012) N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 199(3):527–544

    PubMed Central  CAS  PubMed  Google Scholar 

  118. Frittoli E, Palamidessi A, Marighetti P, Confalonieri S, Bianchi F, Malinverno C, Mazzarol G, Viale G, Martin-Padura I, Garre M, Parazzoli D, Mattei V, Cortellino S, Bertalot G, Di Fiore PP, Scita G (2014) A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination. J Cell Biol 206(2):307–328

    PubMed Central  CAS  PubMed  Google Scholar 

  119. Poincloux R, Lizarraga F, Chavrier P (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122(Pt 17):3015–3024

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Leibniz Society to Tanja Maritzen and from the Swiss National Science Foundation (SNF 31003A_143841), the Novartis Foundation for medical-biological research, the Thurgauische Stiftung für Wissenschaft und Forschung, and the Swiss State Secretariat for Education Research and Innovation to Daniel Legler. We apologize to authors whose work could not be included due to space limitations.

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Correspondence to Tanja Maritzen or Daniel F. Legler.

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Maritzen, T., Schachtner, H. & Legler, D.F. On the move: endocytic trafficking in cell migration. Cell. Mol. Life Sci. 72, 2119–2134 (2015). https://doi.org/10.1007/s00018-015-1855-9

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  • DOI: https://doi.org/10.1007/s00018-015-1855-9

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