On the move: Endocytic trafficking in cell migration

Cellular and Molecular Life Sciences

Volumn 72, Issue 11, 2015, Pages 2119-2134

  Maritzen, Tanja ^a   Schachtner, Hannah ^a   Legler, Daniel F ^b  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b UNIVERSITY OF KONSTANZ   (Switzerland)

Author keywords

Cellular motility; Chemotaxis; Clathrin; Endocytosis; Signal transduction; Vesicular transport

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOTACTIC FACTOR; GROWTH FACTOR RECEPTOR; INTEGRIN;

CELL ADHESION; CELL MEMBRANE; CHEMOTAXIS; ENDOCYTOSIS; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

CELL ADHESION; CELL MEMBRANE; CHEMOKINES; CHEMOTACTIC FACTORS; CHEMOTAXIS; ENDOCYTOSIS; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HUMANS; INTEGRINS; PROTEIN TRANSPORT; RECEPTORS, CHEMOKINE; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84938080795     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1855-9     Document Type: Review

References (119)

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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
16. Borroni EM, Mantovani A, Locati M, Bonecchi R (2010) Chemokine receptors intracellular trafficking. Pharmacol Ther 127(1):1-8
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
18. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513-525
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
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
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
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
23. Raman D, Sai J, Hawkins O, Richmond A (2014) Adaptor protein2 (AP2) orchestrates CXCR2-mediated cell migration. Traffic 15(4):451-469
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
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
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
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
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
29. Rorth P (2002) Initiating and guiding migration: lessons from border cells. Trends Cell Biol 12(7):325-331
30. Duchek P, Rorth P (2001) Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291(5501):131-133
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
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
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
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
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
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
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
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
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
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
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
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
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
45. Bretscher MS (1996) Moving membrane up to the front of migrating cells. Cell 85(4):465-467
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
47. Wieffer M, Maritzen T, Haucke V (2009) SnapShot: endocytic trafficking. Cell 137(2):382 (e381-383)
48. Rappoport JZ, Simon SM (2003) Real-time analysis of clathrin-mediated endocytosis during cell migration. J Cell Sci 116(Pt 5):847-855
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
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
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
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
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
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
55. Bitsikas V, Correa IR Jr, Nichols BJ (2014) Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife 3:e03970
56. Traynor D, Kay RR (2007) Possible roles of the endocytic cycle in cell motility. J Cell Sci 120(Pt 14):2318-2327
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
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
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
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
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
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
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
64. Zaidel-Bar R, Geiger B (2010) The switchable integrin adhesome. J Cell Sci 123(Pt 9):1385-1388
65. Caswell PT, Norman JC (2006) Integrin trafficking and the control of cell migration. Traffic 7(1):14-21
66. Arjonen A, Alanko J, Veltel S, Ivaska J (2012) Distinct recycling of active and inactive beta1 integrins. Traffic 13(4):610-625
67. Caswell P, Norman J (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18(6):257-263
68. Caswell PT, Vadrevu S, Norman JC (2009) Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10(12):843-853
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
70. Bridgewater RE, Norman JC, Caswell PT (2012) Integrin trafficking at a glance. J Cell Sci 125(Pt 16):3695-3701
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
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
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
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
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
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
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
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
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
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
81. Jahn R, Scheller RH (2006) SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631-643
82. Rapaport D, Lugassy Y, Sprecher E, Horowitz M (2010) Loss of SNAP29 impairs endocytic recycling and cell motility. PLoS One 5(3):e9759
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
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
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
86. Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583(8):1337-1343
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
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
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
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
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
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
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
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
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
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
97. Delva E, Kowalczyk AP (2009) Regulation of cadherin trafficking. Traffic 10(3):259-267
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
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
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
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
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
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
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
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
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
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
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
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
110. Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77-91
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
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
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
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
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
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
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
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
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