Integrin traffic-the update

Journal of Cell Science

Volumn 128, Issue 5, 2015, Pages 839-852

  de Franceschi, Nicola ^a   Hamidi, Hellyeh ^a   Alanko, Jonna ^a   Sahgal, Pranshu ^a   Ivaska, Johanna ^a  

^a TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

Author keywords

Integrin; Invasion; Migration; Rab GTPases; Signalling crosstalk; Trafficking

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; CYTOSKELETON PROTEIN; EARLY ENDOSOME ANTIGEN 1; FIBRONECTIN; GUANOSINE TRIPHOSPHATASE; HETERODIMER; INTEGRIN; INTEGRIN RECEPTOR; PROTEIN P53; RAB PROTEIN; RAB11 PROTEIN; SCATTER FACTOR; SYNDECAN 4; VITRONECTIN RECEPTOR; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN POLYMERIZATION; CELL ADHESION; CELL FATE; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CYTOKINESIS; ENDOCYTOSIS; ENZYME SPECIFICITY; HUMAN; INTRACELLULAR SIGNALING; MICROTUBULE; NOTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; EXTRACELLULAR MATRIX; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

VERTEBRATA;

ANIMALS; CELL ADHESION; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84924912028     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.161653     Document Type: Note

References (129)

1. Arjonen, A., Alanko, J., Veltel, S. and Ivaska, J. (2012). Distinct recycling of active and inactive β1 integrins. Traffic 13, 610-625.
2. Arjonen, A., Kaukonen, R., Mattila, E., Rouhi, P., Högnäs, G., Sihto, H., Miller, B. W., Morton, J. P., Bucher, E., Taimen, P. et al. (2014). Mutant p53- associated myosin-X upregulation promotes breast cancer invasion and metastasis. J. Clin. Invest. 124, 1069-1082.
3. Askari, J. A., Buckley, P. A., Mould, A. P. and Humphries, M. J. (2009). Linking integrin conformation to function. J. Cell Sci. 122, 165-170.
4. Bai, M., Pang, X., Lou, J., Zhou, Q., Zhang, K., Ma, J., Li, J., Sun, F. and Hsu, V. W. (2012). Mechanistic insights into regulated cargo binding by ACAP1 protein. J. Biol. Chem. 287, 28675-28685.
5. Bates, R. C., Bellovin, D. I., Brown, C., Maynard, E., Wu, B., Kawakatsu, H., Sheppard, D., Oettgen, P. and Mercurio, A. M. (2005). Transcriptional activation of integrin beta6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma. J. Clin. Invest. 115, 339-347.
6. Bogdanović, O., Delfino-Machín, M., Nicolás-Pérez, M., Gavilán, M. P., Gago- Rodrigues, I., Fernández-Minãn, A., Lillo, C., Ríos, R. M., Wittbrodt, J. and Martínez-Morales, J. R. (2012). Numb/Numbl-Opo antagonism controls retinal epithelium morphogenesis by regulating integrin endocytosis. Dev. Cell 23, 782- 795.
7. Böttcher, R. T., Stremmel, C., Meves, A., Meyer, H., Widmaier, M., Tseng, H. Y. and Fässler, R. (2012). Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail. Nat. Cell Biol. 14, 584-592.
8. Bridgewater, R. E., Norman, J. C. and Caswell, P. T. (2012). Integrin trafficking at a glance. J. Cell Sci. 125, 3695-3701.
9. Byron, A., Humphries, J. D., Askari, J. A., Craig, S. E., Mould, A. P. and Humphries, M. J. (2009). Anti-integrin monoclonal antibodies. J. Cell Sci. 122, 4009-4011.
10. Cao, R., Chen, J., Zhang, X., Zhai, Y., Qing, X., Xing, W., Zhang, L., Malik, Y. S., Yu, H. and Zhu, X. (2014). Elevated expression of myosin X in tumours contributes to breast cancer aggressiveness and metastasis. Br. J. Cancer 111, 539-550.
11. Caswell, P. T. and Norman, J. C. (2006). Integrin trafficking and the control of cell migration. Traffic 7, 14-21.
12. Caswell, P. and Norman, J. (2008). Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 18, 257-263.
13. Caswell, P. T., Spence, H. J., Parsons, M., White, D. P., Clark, K., Cheng, K. W., Mills, G. B., Humphries, M. J., Messent, A. J., Anderson, K. I. et al. (2007). Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13, 496-510.
14. Caswell, P. T., Vadrevu, S. and Norman, J. C. (2009). Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853.
15. Chao, W. T. and Kunz, J. (2009). Focal adhesion disassembly requires clathrindependent endocytosis of integrins. FEBS Lett. 583, 1337-1343.
16. Chao, W. T., Ashcroft, F., Daquinag, A. C., Vadakkan, T., Wei, Z., Zhang, P., Dickinson, M. E. and Kunz, J. (2010). Type I phosphatidylinositol phosphate kinase beta regulates focal adhesion disassembly by promoting beta1 integrin endocytosis. Mol. Cell. Biol. 30, 4463-4479.
17. Chen, P. W., Luo, R., Jian, X. and Randazzo, P. A. (2014). The Arf6 GTPaseactivating proteins ARAP2 and ACAP1 define distinct endosomal compartments that regulate integrin α5β1 traffic. J. Biol. Chem. 289, 30237-30248.
18. Cheng, K. W., Lahad, J. P., Kuo, W. L., Lapuk, A., Yamada, K., Auersperg, N., Liu, J., Smith-McCune, K., Lu, K. H., Fishman, D. et al. (2004). The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat. Med. 10, 1251-1256.
19. Cheng, J. M., Volk, L., Janaki, D. K., Vyakaranam, S., Ran, S. and Rao, K. A. (2010). Tumor suppressor function of Rab25 in triple-negative breast cancer. Int. J. Cancer 126, 2799-2812.
20. Christoforides, C., Rainero, E., Brown, K. K., Norman, J. C. and Toker, A. (2012). PKD controls αvβ3 integrin recycling and tumor cell invasive migration through its substrate Rabaptin-5. Dev. Cell 23, 560-572.
21. Dai, J., Li, J., Bos, E., Porcionatto, M., Premont, R. T., Bourgoin, S., Peters, P. J. and Hsu, V. W. (2004). ACAP1 promotes endocytic recycling by recognizing recycling sorting signals. Dev. Cell 7, 771-776.
22. Dai, Y., Liu, Y., Huang, D., Yu, C., Cai, G., Pi, L., Ren, C., Chen, G. Z., Tian, Y. and Zhang, X. (2012). Increased expression of Rab coupling protein in squamous cell carcinoma of the head and neck and its clinical significance. Oncol. Lett. 3, 1231-1236.
23. Danen, E. H., van Rheenen, J., Franken, W., Huveneers, S., Sonneveld, P., Jalink, K. and Sonnenberg, A. (2005). Integrins control motile strategy through a Rho-cofilin pathway. J. Cell Biol. 169, 515-526.
24. De Bock, K., Georgiadou, M. and Carmeliet, P. (2013). Role of endothelial cell metabolism in vessel sprouting. Cell Metab. 18, 634-647.
25. Dozynkiewicz, M. A., Jamieson, N. B., Macpherson, I., Grindlay, J., van den Berghe, P. V., von Thun, A., Morton, J. P., Gourley, C., Timpson, P., Nixon, C. et al. (2012). Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev. Cell 22, 131-145.
26. Duleh, S. N. and Welch, M. D. (2012). Regulation of integrin trafficking, cell adhesion, and cell migration by WASH and the Arp2/3 complex. Cytoskeleton (Hoboken) 69, 1047-1058.
27. Dunphy, J. L., Moravec, R., Ly, K., Lasell, T. K., Melancon, P. and Casanova, J. E. (2006). The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr. Biol. 16, 315-320.
28. Eiseler, T., Döppler, H., Yan, I. K., Goodison, S. and Storz, P. (2009). Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion. Breast Cancer Res. 11, R13.
29. Eskova, A., Knapp, B., Matelska, D., Reusing, S., Arjonen, A., Lisauskas, T., Pepperkok, R., Russell, R., Eils, R., Ivaska, J. et al. (2014). An RNAi screen identifies KIF15 as a novel regulator of the endocytic trafficking of integrin. J. Cell Sci. 127, 2433-2447.
30. Eva, R. and Fawcett, J. (2014). Integrin signalling and traffic during axon growth and regeneration. Curr. Opin. Neurobiol. 27, 179-185.
31. Eva, R., Crisp, S., Marland, J. R., Norman, J. C., Kanamarlapudi, V., ffrench- Constant, C. and Fawcett, J. W. (2012). ARF6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. J. Neurosci. 32, 10352-10364.
32. Ezratty, E. J., Partridge, M. A. and Gundersen, G. G. (2005). Microtubuleinduced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590.
33. Ezratty, E. J., Bertaux, C., Marcantonio, E. E. and Gundersen, G. G. (2009). Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J. Cell Biol. 187, 733-747.
34. Fan, Y., Xin, X. Y., Chen, B. L. and Ma, X. (2006). Knockdown of RAB25 expression by RNAi inhibits growth of human epithelial ovarian cancer cells in vitro and in vivo. Pathology 38, 561-567.
35. Frittoli, E., Palamidessi, A., Marighetti, P., Confalonieri, S., Bianchi, F., Malinverno, C., Mazzarol, G., Viale, G., Martin-Padura, I., Garre, M. et al. (2014). A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination. J. Cell Biol. 206, 307-328.
36. Gebhardt, C., Breitenbach, U., Richter, K. H., Fürstenberger, G., Mauch, C., Angel, P. and Hess, J. (2005). c-Fos-dependent induction of the small rasrelated GTPase Rab11a in skin carcinogenesis. Am. J. Pathol. 167, 243-253.
37. Goldenring, J. R. and Nam, K. T. (2011). Rab25 as a tumour suppressor in colon carcinogenesis. Br. J. Cancer 104, 33-36.
38. Goldenring, J. R., Ray, G. S. and Lee, J. R. (1999). Rab11 in dysplasia of Barrett's epithelia. Yale J. Biol. Med. 72, 113-120.
39. Goley, E. D. and Welch, M. D. (2006). The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713-726.
40. Gu, Z., Noss, E. H., Hsu, V. W. and Brenner, M. B. (2011). Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J. Cell Biol. 193, 61-70.
41. Högnäs, G., Tuomi, S., Veltel, S., Mattila, E., Murumägi, A., Edgren, H., Kallioniemi, O. and Ivaska, J. (2012). Cytokinesis failure due to derailed integrin traffic induces aneuploidy and oncogenic transformation in vitro and in vivo. Oncogene 31, 3597-3606.
42. Holly, S. P., Larson, M. K. and Parise, L. V. (2005). The unique N-terminus of Rras is required for Rac activation and precise regulation of cell migration. Mol. Biol. Cell 16, 2458-2469.
43. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
44. Jacquemet, G., Green, D. M., Bridgewater, R. E., von Kriegsheim, A., Humphries, M. J., Norman, J. C. and Caswell, P. T. (2013). RCP-driven α5β1 recycling suppresses Rac and promotes RhoA activity via the RacGAP1- IQGAP1 complex. J. Cell Biol. 202, 917-935.
45. Jaggi, M., Rao, P. S., Smith, D. J., Hemstreet, G. P. and Balaji, K. C. (2003). Protein kinase C mu is down-regulated in androgen-independent prostate cancer. Biochem. Biophys. Res. Commun. 307, 254-260.
46. Kaksonen, M., Toret, C. P. and Drubin, D. G. (2006). Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7, 404-414.
47. Kanerva, K., Uronen, R. L., Blom, T., Li, S., Bittman, R., Lappalainen, P., Peränen, J., Raposo, G. and Ikonen, E. (2013). LDL cholesterol recycles to the plasma membrane via a Rab8a-Myosin5b-actin-dependent membrane transport route. Dev. Cell 27, 249-262.
48. Kaverina, I., Krylyshkina, O. and Small, J. V. (1999). Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146, 1033-1044.
49. Kaverina, I., Krylyshkina, O. and Small, J. V. (2002). Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761.
50. Kirikoshi, H. and Katoh, M. (2002). Up-regulation of GIPC2 in human gastric cancer. Int. J. Oncol. 20, 1183-1187.
51. Lakshminarayan, R., Wunder, C., Becken, U., Howes, M. T., Benzing, C., Arumugam, S., Sales, S., Ariotti, N., Chambon, V., Lamaze, C. et al. (2014). Galectin-3 drives glycosphingolipid-dependent biogenesis of clathrinindependent carriers. Nat. Cell Biol. 16, 595-606.
52. Legate, K. R., Takahashi, S., Bonakdar, N., Fabry, B., Boettiger, D., Zent, R. and Fässler, R. (2011). Integrin adhesion and force coupling are independently regulated by localized PtdIns(4,5)2 synthesis. EMBO J. 30, 4539-4553.
53. Li, Y., Feng, H. and Chen, Y. (1999). [RAB5A, a gene possibly related to metastasis of human carcinoma of the lung and stomach]. Zhonghua Zhong Liu Za Zhi 21, 178-181.
54. Linder, S., Wiesner, C. and Himmel, M. (2011). Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27, 185-211.
55. Ling, K., Doughman, R. L., Firestone, A. J., Bunce, M. W. and Anderson, R. A. (2002). Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420, 89-93.
56. Ling, K., Schill, N. J., Wagoner, M. P., Sun, Y. and Anderson, R. A. (2006). Movin' on up: the role of PtdIns(4,5)P(2) in cell migration. Trends Cell Biol. 16, 276-284.
57. Lobert, V. H. and Stenmark, H. (2012). The ESCRT machinery mediates polarization of fibroblasts through regulation of myosin light chain. J. Cell Sci. 125, 29-36.
58. Luo, B. H., Carman, C. V. and Springer, T. A. (2007). Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647.
59. Machesky, L. M. and Li, A. (2010). Fascin: Invasive filopodia promoting metastasis. Commun. Integr. Biol. 3, 263-270.
60. Macpherson, I. R., Rainero, E., Mitchell, L. E., van den Berghe, P. V., Speirs, C., Dozynkiewicz, M. A., Chaudhary, S., Kalna, G., Edwards, J., Timpson, P. et al. (2014). CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J. Cell Sci. 127, 3893- 3901.
61. Mai, A., Veltel, S., Pellinen, T., Padzik, A., Coffey, E., Marjomäki, V. and Ivaska, J. (2011). Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration. J. Cell Biol. 194, 291-306.
62. Mai, A., Muharram, G., Barrow-McGee, R., Baghirov, H., Rantala, J., Kermorgant, S. and Ivaska, J. (2014). Distinct c-Met activation mechanisms induce cell rounding or invasion through pathways involving integrins, RhoA and HIP1. J. Cell Sci. 127, 1938-1952.
63. Maiorano, E., Favia, G., Pece, S., Resta, L., Maisonneuve, P., Di Fiore, P. P., Capodiferro, S., Urbani, U. and Viale, G. (2007). Prognostic implications of NUMB immunoreactivity in salivary gland carcinomas. Int. J. Immunopathol. Pharmacol. 20, 779-789.
64. Majeed, S. R., Vasudevan, L., Chen, C. Y., Luo, Y., Torres, J. A., Evans, T. M., Sharkey, A., Foraker, A. B., Wong, N. M., Esk, C. et al. (2014). Clathrin light chains are required for the gyrating-clathrin recycling pathway and thereby promote cell migration. Nat. Commun. 5, 3891.
65. Manavski, Y., Carmona, G., Bennewitz, K., Tang, Z., Zhang, F., Sakurai, A., Zeiher, A. M., Gutkind, J. S., Li, X., Kroll, J. et al. (2014). Brag2 differentially regulates beta1- and beta3-integrin-dependent adhesion in endothelial cells and is involved in developmental and pathological angiogenesis. Basic Res. Cardiol. 109, 404.
66. Maurer, M. E. and Cooper, J. A. (2006). The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J. Cell Sci. 119, 4235-4246.
67. Mills, G. B., Jurisica, I., Yarden, Y. and Norman, J. C. (2009). Genomic amplicons target vesicle recycling in breast cancer. J. Clin. Invest. 119, 2123- 2127.
68. Mok, S. C., Wong, K. K., Chan, R. K., Lau, C. C., Tsao, S. W., Knapp, R. C. and Berkowitz, R. S. (1994). Molecular cloning of differentially expressed genes in human epithelial ovarian cancer. Gynecol. Oncol. 52, 247-252.
69. Montagnac, G., Meas-Yedid, V., Irondelle, M., Castro-Castro, A., Franco, M., Shida, T., Nachury, M. V., Benmerah, A., Olivo-Marin, J. C. and Chavrier, P. (2013). aTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature 502, 567-570.
70. Monteiro, P., Rossé, C., Castro-Castro, A., Irondelle, M., Lagoutte, E., Paul- Gilloteaux, P., Desnos, C., Formstecher, E., Darchen, F., Perrais, D. et al. (2013). Endosomal WASH and exocyst complexes control exocytosis of MT1- MMP at invadopodia. J. Cell Biol. 203, 1063-1079.
71. Moravec, R., Conger, K. K., D'Souza, R., Allison, A. B. and Casanova, J. E. (2012). BRAG2/GEP100/IQSec1 interacts with clathrin and regulates α5β1 integrin endocytosis through activation of ADP ribosylation factor 5 (Arf5). J. Biol. Chem. 287, 31138-31147.
72. Morgan, M. R., Byron, A., Humphries, M. J. and Bass, M. D. (2009). Giving off mixed signals-distinct functions of alpha5beta1 and alphavbeta3 integrins in regulating cell behaviour. IUBMB Life 61, 731-738.
73. Morgan, M. R., Hamidi, H., Bass, M. D., Warwood, S., Ballestrem, C. and Humphries, M. J. (2013). Syndecan-4 phosphorylation is a control point for integrin recycling. Dev. Cell 24, 472-485.
74. Muders, M. H., Dutta, S. K., Wang, L., Lau, J. S., Bhattacharya, R., Smyrk, T. C., Chari, S. T., Datta, K. and Mukhopadhyay, D. (2006). Expression and regulatory role of GAIP-interacting protein GIPC in pancreatic adenocarcinoma. Cancer Res. 66, 10264-10268.
75. Muharram, G., Sahgal, P., Korpela, T., De Franceschi, N., Kaukonen, R., Clark, K., Tulasne, D., Carpén, O. and Ivaska, J. (2014). Tensin-4-dependent MET stabilization is essential for survival and proliferation in carcinoma cells. Dev. Cell 29, 421-436.
76. Muller, P. A., Caswell, P. T., Doyle, B., Iwanicki, M. P., Tan, E. H., Karim, S., Lukashchuk, N., Gillespie, D. A., Ludwig, R. L., Gosselin, P. et al. (2009). Mutant p53 drives invasion by promoting integrin recycling. Cell 139, 1327- 1341.
77. Muller, P. A., Trinidad, A. G., Timpson, P., Morton, J. P., Zanivan, S., van den Berghe, P. V., Nixon, C., Karim, S. A., Caswell, P. T., Noll, J. E. et al. (2013). Mutant p53 enhances MET trafficking and signalling to drive cell scattering and invasion. Oncogene 32, 1252-1265.
78. Nam, K. T., Lee, H. J., Smith, J. J., Lapierre, L. A., Kamath, V. P., Chen, X., Aronow, B. J., Yeatman, T. J., Bhartur, S. G., Calhoun, B. C. et al. (2010). Loss of Rab25 promotes the development of intestinal neoplasia in mice and is associated with human colorectal adenocarcinomas. J. Clin. Invest. 120, 840- 849.
79. Nishimura, T. and Kaibuchi, K. (2007). Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15-28.
80. Palamidessi, A., Frittoli, E., Ducano, N., Offenhauser, N., Sigismund, S., Kajiho, H., Parazzoli, D., Oldani, A., Gobbi, M., Serini, G. et al. (2013). The GTPase-activating protein RN-tre controls focal adhesion turnover and cell migration. Curr. Biol. 23, 2355-2364.
81. Pece, S., Serresi, M., Santolini, E., Capra, M., Hulleman, E., Galimberti, V., Zurrida, S., Maisonneuve, P., Viale, G. and Di Fiore, P. P. (2004). Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J. Cell Biol. 167, 215-221.
82. Pellinen, T. and Ivaska, J. (2006). Integrin traffic. J. Cell Sci. 119, 3723- 3731.
83. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J. A. and Ivaska, J. (2006). Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173, 767-780.
84. Pellinen, T., Tuomi, S., Arjonen, A., Wolf, M., Edgren, H., Meyer, H., Grosse, R., Kitzing, T., Rantala, J. K., Kallioniemi, O. et al. (2008). Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell 15, 371-385.
85. Powelka, A. M., Sun, J., Li, J., Gao, M., Shaw, L. M., Sonnenberg, A. and Hsu, V. W. (2004). Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 5, 20-36.
86. Radhakrishna, H., Al-Awar, O., Khachikian, Z. and Donaldson, J. G. (1999). ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J. Cell Sci. 112, 855-866.
87. Rainero, E., Caswell, P. T., Muller, P. A., Grindlay, J., McCaffrey, M. W., Zhang, Q., Wakelam, M. J., Vousden, K. H., Graziani, A. and Norman, J. C. (2012). Diacylglycerol kinase a controls RCP-dependent integrin trafficking to promote invasive migration. J. Cell Biol. 196, 277-295.
88. Ramsay, A. G., Keppler, M. D., Jazayeri, M., Thomas, G. J., Parsons, M., Violette, S., Weinreb, P., Hart, I. R. and Marshall, J. F. (2007). HS1-associated protein X-1 regulates carcinoma cell migration and invasion via clathrinmediated endocytosis of integrin alphavbeta6. Cancer Res. 67, 5275-5284.
89. Reverter, M., Rentero, C., Garcia-Melero, A., Hoque, M., Vilà de Muga, S., Alvarez-Guaita, A., Conway, J. R., Wood, P., Cairns, R., Lykopoulou, L. et al. (2014). Cholesterol regulates Syntaxin 6 trafficking at trans-Golgi network endosomal boundaries. Cell Reports 7, 883-897.
90. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
91. Riggs, K. A., Hasan, N., Humphrey, D., Raleigh, C., Nevitt, C., Corbin, D. and Hu, C. (2012). Regulation of integrin endocytic recycling and chemotactic cell migration by syntaxin 6 and VAMP3 interaction. J. Cell Sci. 125, 3827-3839.
92. Ristich, V. L., Bowman, P. H., Dodd, M. E. and Bollag, W. B. (2006). Protein kinase D distribution in normal human epidermis, basal cell carcinoma and psoriasis. Br. J. Dermatol. 154, 586-593.
93. Rudchenko, S., Scanlan, M., Kalantarov, G., Yavelsky, V., Levy, C., Estabrook, A., Old, L., Chan, G. L., Lobel, L. and Trakht, I. (2008). A human monoclonal autoantibody to breast cancer identifies the PDZ domain containing protein GIPC1 as a novel breast cancer-associated antigen. BMC Cancer 8, 248.
94. Sakurai, A., Gavard, J., Annas-Linhares, Y., Basile, J. R., Amornphimoltham, P., Palmby, T. R., Yagi, H., Zhang, F., Randazzo, P. A., Li, X. et al. (2010). Semaphorin 3E initiates antiangiogenic signaling through plexin D1 by regulating Arf6 and R-Ras. Mol. Cell. Biol. 30, 3086-3098.
95. Sakurai, A., Jian, X., Lee, C. J., Manavski, Y., Chavakis, E., Donaldson, J., Randazzo, P. A. and Gutkind, J. S. (2011). Phosphatidylinositol-4-phosphate 5-kinase and GEP100/Brag2 protein mediate antiangiogenic signaling by semaphorin 3E-plexin-D1 through Arf6 protein. J. Biol. Chem. 286, 34335- 34345.
96. Sandri, C., Caccavari, F., Valdembri, D., Camillo, C., Veltel, S., Santambrogio, M., Lanzetti, L., Bussolino, F., Ivaska, J. and Serini, G. (2012). The R-Ras/ RIN2/Rab5 complex controls endothelial cell adhesion and morphogenesis via active integrin endocytosis and Rac signaling. Cell Res. 22, 1479-1501.
97. Scita, G. and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473.
98. Shabelnik, M. Y., Kovalevska, L. M., Yurchenko, M. Y., Shlapatska, L. M., Rzepetsky, Y. and Sidorenko, S. P. (2011). Differential expression of PKD1 and PKD2 in gastric cancer and analysis of PKD1 and PKD2 function in the model system. Exp. Oncol. 33, 206-211.
99. Shi, F. and Sottile, J. (2011). MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin. J. Cell Sci. 124, 4039-4050.
100. Sönnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J. and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
101. Sottile, J. and Chandler, J. (2005). Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 16, 757-768.
102. Stehbens, S. J., Paszek, M., Pemble, H., Ettinger, A., Gierke, S. and Wittmann, T. (2014). CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat. Cell Biol. 16, 561-573.
103. Sung, B. H., Zhu, X., Kaverina, I. and Weaver, A. M. (2011). Cortactin controls cell motility and lamellipodial dynamics by regulating ECM secretion. Curr. Biol. 21, 1460-1469.
104. Takenawa, T. and Suetsugu, S. (2007). The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37-48.
105. Teckchandani, A., Mulkearns, E. E., Randolph, T. W., Toida, N. and Cooper, J. A. (2012). The clathrin adaptor Dab2 recruits EH domain scaffold proteins to regulate integrin β1 endocytosis. Mol. Biol. Cell 23, 2905-2916.
106. Theisen, U., Straube, E. and Straube, A. (2012). Directional persistence of migrating cells requires Kif1C-mediated stabilization of trailing adhesions. Dev. Cell 23, 1153-1166.
107. Tiwari, A., Jung, J. J., Inamdar, S. M., Brown, C. O., Goel, A. and Choudhury, A. (2011). Endothelial cell migration on fibronectin is regulated by syntaxin 6- mediated alpha5beta1 integrin recycling. J. Biol. Chem. 286, 36749-36761.
108. Tong, J. H., Ng, D. C., Chau, S. L., So, K. K., Leung, P. P., Lee, T. L., Lung, R. W., Chan, M. W., Chan, A. W., Lo, K. W. et al. (2010). Putative tumoursuppressor gene DAB2 is frequently down regulated by promoter hypermethylation in nasopharyngeal carcinoma. BMC Cancer 10, 253-2407- 10-253.
109. Trebinska, A., Rembiszewska, A., Ciosek, K., Ptaszynski, K., Rowinski, S., Kupryjanczyk, J., Siedlecki, J. A. and Grzybowska, E. A. (2010). HAX-1 overexpression, splicing and cellular localization in tumors. BMC Cancer 10, 76.
110. Tseng, H. Y., Thorausch, N., Ziegler, T., Meves, A., Fässler, R. and Böttcher, R. T. (2014). Sorting nexin 31 binds multiple b integrin cytoplasmic domains and regulates β1 integrin surface levels and stability. J. Mol. Biol. 426, 3180-3194.
111. Tuloup-Minguez, V., Hamaï, A., Greffard, A., Nicolas, V., Codogno, P. and Botti, J. (2013). Autophagy modulates cell migration and β1 integrin membrane recycling. Cell Cycle 12, 3317-3328.
112. Valdembri, D. and Serini, G. (2012). Regulation of adhesion site dynamics by integrin traffic. Curr. Opin. Cell Biol. 24, 582-591.
113. Valdembri, D., Caswell, P. T., Anderson, K. I., Schwarz, J. P., König, I., Astanina, E., Caccavari, F., Norman, J. C., Humphries, M. J., Bussolino, F. et al. (2009). Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7, e25.
114. Wang, Y. and McNiven, M. A. (2012). Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 196, 375-385.
115. Wang, Z., Tseng, C. P., Pong, R. C., Chen, H., McConnell, J. D., Navone, N. and Hsieh, J. T. (2002). The mechanism of growth-inhibitory effect of DOC-2/DAB2 in prostate cancer. Characterization of a novel GTPase-activating protein associated with N-terminal domain of DOC-2/DAB2. J. Biol. Chem. 277, 12622-12631.
116. Westhoff, B., Colaluca, I. N., D'Ario, G., Donzelli, M., Tosoni, D., Volorio, S., Pelosi, G., Spaggiari, L., Mazzarol, G., Viale, G. et al. (2009). Alterations of the Notch pathway in lung cancer. Proc. Natl. Acad. Sci. USA 106, 22293- 22298.
117. White, D. P., Caswell, P. T. and Norman, J. C. (2007). alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 177, 515-525.
118. Woods, A. J., White, D. P., Caswell, P. T. and Norman, J. C. (2004). PKD1/ PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 23, 2531-2543.
119. Xu, S., Zhu, J. and Wu, Z. (2014). Loss of Dab2 expression in breast cancer cells impairs their ability to deplete TGF-b and induce Tregs development via TGF-b. PLoS ONE 9, e91709.
120. Yang, P. S., Yin, P. H., Tseng, L. M., Yang, C. H., Hsu, C. Y., Lee, M. Y., Horng, C. F. and Chi, C. W. (2011). Rab5A is associated with axillary lymph node metastasis in breast cancer patients. Cancer Sci. 102, 2172-2178.
121. Yavelsky, V., Rohkin, S., Shaco-Levy, R., Tzikinovsky, A., Amir, T., Kohn, H., Delgado, B., Rabinovich, A., Piura, B., Chan, G. et al. (2008). Native human autoantibodies targeting GIPC1 identify differential expression in malignant tumors of the breast and ovary. BMC Cancer 8, 247.
122. Yu, L., Hui-chen, F., Chen, Y., Zou, R., Yan, S., Chun-xiang, L., Wu-ru, W. and Li, P. (1999). Differential expression of RAB5A in human lung adenocarcinoma cells with different metastasis potential. Clin. Exp. Metastasis 17, 213-219.
123. Yue, J., Xie, M., Gou, X., Lee, P., Schneider, M. D. and Wu, X. (2014). Microtubules regulate focal adhesion dynamics through MAP4K4. Dev. Cell 31, 572-585.
124. Zaidel-Bar, R. and Geiger, B. (2010). The switchable integrin adhesome. J. Cell Sci. 123, 1385-1388.
125. Zech, T., Calaminus, S. D., Caswell, P., Spence, H. J., Carnell, M., Insall, R. H., Norman, J. and Machesky, L. M. (2011). The Arp2/3 activator WASH regulates α5β1-integrin-mediated invasive migration. J. Cell Sci. 124, 3753-3759.
126. Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.
127. Zhang, H., Berg, J. S., Li, Z., Wang, Y., Lång, P., Sousa, A. D., Bhaskar, A., Cheney, R. E. and Strömblad, S. (2004). Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat. Cell Biol. 6, 523-531.
128. Zhang, J., Liu, X., Datta, A., Govindarajan, K., Tam, W. L., Han, J., George, J., Wong, C., Ramnarayanan, K., Phua, T. Y. et al. (2009). RCP is a human breast cancer-promoting gene with Ras-activating function. J. Clin. Invest. 119, 2171-2183.
129. Zimmermann, P., Zhang, Z., Degeest, G., Mortier, E., Leenaerts, I., Coomans, C., Schulz, J., N'Kuli, F., Courtoy, P. J. and David, G. (2005). Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9, 377-388.