Interplay between Rab35 and Arf6 controls cargo recycling to coordinate cell adhesion and migration

Journal of Cell Science

Volumn 126, Issue 3, 2013, Pages 722-731

  Allaire, Patrick D ^a   Sadr, Mohamed Seyed ^a   Chaineau, Mathilde ^a   Sadr, Emad Seyed ^a   Konefal, Sarah ^a   Fotouhi, Maryam ^a   Maret, Deborah ^a   Ritter, Brigitte ^a   Del Maestro, Rolando F ^a   McPherson, Peter S ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

ACAP2; Cadherin; Cancer; EGF receptor; EMT; Epithelial mesenchymal transition; Erk; Glioma; Integrin; Tumor invasiveness

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BETA1 INTEGRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; INTEGRIN RECEPTOR; RAB PROTEIN; RAB35 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SELECTION; CELL SURFACE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; DESMOSOMAL CADHERINS; EPIDERMAL GROWTH FACTOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; NEOPLASM INVASIVENESS; RAB GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84876323150     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.112375     Document Type: Article

References (78)

1. Allaire, P. D., Ritter, B., Thomas, S., Burman, J. L., Denisov, A. Y., Legendre-Guillemin, V., Harper, S. Q., Davidson, B. L., Gehring, K. and McPherson, P. S. (2006). Connecdenn, a novel DENN domain-containing protein of neuronal clathrincoated vesicles functioning in synaptic vesicle endocytosis. J. Neurosci. 26, 13202-13212.
2. Allaire, P. D., Marat, A. L., Dall'Armi, C., Di Paolo, G., McPherson, P. S. and Ritter, B. (2010). The Connecdenn DENN domain: a GEF for Rab35 mediating cargo-specific exit from early endosomes. Mol. Cell 37, 370-382.
3. Arjonen, A., Alanko, J., Veltel, S. and Ivaska, J. (2012). Distinct recycling of active and inactive b1 integrins. Traffic [Epub ahead of print] doi: 10.1111/j.1600-0854.2012.01327.
4. Blindt, R., Bosserhoff, A. K., Dammers, J., Krott, N., Demircan, L., Hoffmann, R., Hanrath, P., Weber, C. and Vogt, F. (2004). Downregulation of N-cadherin in the neointima stimulates migration of smooth muscle cells by RhoA deactivation. Cardiovasc. Res. 62, 212-222.
5. Cancer Genome Atlas Research Network (2008). Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061-1068.
6. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G. and Bonifacino, J. S. (2002). A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 21, 2557-2567.
7. Caswell, P. T., Chan, M., Lindsay, A. J., McCaffrey, M. W., Boettiger, D. and Norman, J. C. (2008). Rab-coupling protein coordinates recycling of α5β1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183, 143-155.
8. Chen, X. L., Nam, J. O., Jean, C., Lawson, C., Walsh, C. T., Goka, E., Lim, S. T., Tomar, A., Tancioni, I., Uryu, S. et al. (2012). VEGF-induced vascular permeability is mediated by FAK. Dev. Cell 22, 146-157.
9. Chesneau, L., Dambournet, D., Machicoane, M., Kouranti, I., Fukuda, M., Goud, B. and Echard, A. (2012). An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr. Biol. 22, 147-153.
10. Dambournet, D., Machicoane, M., Chesneau, L., Sachse, M., Rocancourt, M., El Marjou, A., Formstecher, E., Salomon, R., Goud, B. and Echard, A. (2011). Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell Biol. 13, 981-988.
11. Delva, E. and Kowalczyk, A. P. (2009). Regulation of cadherin trafficking. Traffic 10, 259-267.
12. Frasa, M. A., Maximiano, F. C., Smolarczyk, K., Francis, R. E., Betson, M. E., Lozano, E., Goldenring, J., Seabra, M. C., Rak, A., Ahmadian, M. R. et al. (2010). Armus is a Rac1 effector that inactivates Rab7 and regulates E-cadherin degradation. Curr. Biol. 20, 198-208.
13. Funakoshi, Y., Hasegawa, H. and Kanaho, Y. J. (2011). Regulation of PIP5K activity by Arf6 and its physiological significance. J. Cell Physiol. 226, 888-895.
14. Gao, Y., Balut, C. M., Bailey, M. A., Patino-Lopez, G., Shaw, S. and Devor, D. C. (2010). Recycling of the Ca2+-activated K+ channel, KCa2.3, is dependent upon RME-1, Rab35/EPI64C, and an N-terminal domain. J. Biol. Chem. 285, 17938-17953.
15. 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.
16. Hanono, A., Garbett, D., Reczek, D., Chambers, D. N. and Bretscher, A. (2006). EPI64 regulates microvillar subdomains and structure. J. Cell Biol. 175, 803-813.
17. Hashimoto, S., Onodera, Y., Hashimoto, A., Tanaka, M., Hamaguchi, M., Yamada, A. and Sabe, H. (2004). Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. USA 101, 6647-6652.
18. Hashimoto, S., Hirose, M., Hashimoto, A., Morishige, M., Yamada, A., Hosaka, H., Akagi, K., Ogawa, E., Oneyama, C., Agatsuma, T. et al. (2006). Targeting AMAP1 and cortactin binding bearing an atypical src homology 3/proline interface for prevention of breast cancer invasion and metastasis. Proc. Natl. Acad. Sci. USA 103, 7036-7041.
19. Hashimoto, A., Hashimoto, S., Ando, R., Noda, K., Ogawa, E., Kotani, H., Hirose, M., Menju, T., Morishige, M., Manabe, T. et al. (2011). GEP100-Arf6-AMAP1-cortactin pathway frequently used in cancer invasion is activated by VEGFR2 to promote angiogenesis. PLoS ONE 6, e23359.
20. Heo, W. D., Inoue, T., Park, W. S., Kim, M. L., Park, B. O., Wandless, T. J. and Meyer, T. (2006). PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461.
21. Hokanson, D. E. and Bretscher, A. P. (2012). EPI64 interacts with Slp1/JFC1 to coordinate Rab8a and Arf6 membrane trafficking. Mol. Biol. Cell 23, 701-715.
22. Hsu, V. W. and Prekeris, R. (2010). Transport at the recycling endosome. Curr. Opin. Cell Biol. 22, 528-534
23. Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M. A., Bakhti, M., Grønborg, M., Möbius, W., Rhee, J. et al. (2010). Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 189, 223-232.
24. Hu, B., Shi, B., Jarzynka, M. J., Yiin, J. J., D'Souza-Schorey, C. and Cheng, S. Y. (2009). ADP-ribosylation factor 6 regulates glioma cell invasion through the IQdomain GTPase-activating protein 1-Rac1-mediated pathway. Cancer Res. 69, 794-801.
25. Hutagalung, A. H. and Novick, P. J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119-149.
26. Huttenlocher, A., Lakonishok, M., Kinder, M., Wu, S., Truong, T., Knudsen, K. A. and Horwitz, A. F. (1998). Integrin and cadherin synergy regulates contact inhibition of migration and motile activity. J. Cell Biol. 141, 515-526.
27. Jakob, T. and Udey, M. C. (1998). Regulation of E-cadherin-mediated adhesion in Langerhans cell-like dendritic cells by inflammatory mediators that mobilize Langerhans cells in vivo. J. Immunol. 160, 4067-4073.
28. Ji, H., Wang, J., Nika, H., Hawke, D., Keezer, S., Ge, Q., Fang, B., Fang, X., Fang, D., Litchfield, D. W. et al. (2009). EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-Catenin from beta-Catenin and transactivation of beta-Catenin. Mol. Cell 36, 547-559.
29. Jones, C. A., Nishiya, N., London, N. R., Zhu, W., Sorensen, L. K., Chan, A. C., Lim, C. J., Chen, H., Zhang, Q., Schultz, P. G. et al. (2009). Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 11, 1325-1331.
30. Kanno, E., Ishibashi, K., Kobayashi, H., Matsui, T., Ohbayashi, N. and Fukuda, M. (2010). Comprehensive screening for novel rab-binding proteins by GST pull-down assay using 60 different mammalian Rabs. Traffic 11, 491-507.
31. Kawasaki, M., Nakayama, K. and Wakatsuki, S. (2005). Membrane recruitment of effector proteins by Arf and Rab GTPases. Curr. Opin. Struct. Biol. 15, 681-689.
32. Kobayashi, H. and Fukuda, M. (2012). Rab35 regulates Arf6 activity through centaurin b2/ACAP2 during neurite outgrowth. J. Cell Sci. 125, 2235-2243.
33. Kong, D., Banerjee, S., Ahmad, A., Li, Y., Wang, Z., Sethi, S. and Sarkar, F. H. (2010). Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS ONE 5, e12445.
34. Kouranti, I., Sachse, M., Arouche, N., Goud, B. and Echard, A. (2006). Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 16, 1719-1725.
35. Lenferink, A. E. G., Pinkas-Kramarski, R., van de Poll, M. L., van Vugt, M. J., Klapper, L. N., Tzahar, E., Waterman, H., Sela, M., van Zoelen, E. J. and Yarden, Y. (1998). Differential endocytic routing of homo-and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 17, 3385-3397.
36. Li, M., Ng, S. S., Wang, J., Lai, L., Leung, S. Y., Franco, M., Peng, Y., He, M. L., Kung, H. F. and Lin, M. C. (2006). EFA6A enhances glioma cell invasion through ADP ribosylation factor 6/extracellular signal-regulated kinase signaling. Cancer Res. 66, 1583-1590.
37. Li, M., Wang, J., Ng, S. S., Chan, C. Y., He, M. L., Yu, F., Lai, L., Shi, C., Chen, Y., Yew, D. T. et al. (2009). Adenosine diphosphate-ribosylation factor 6 is required for epidermal growth factor-induced glioblastoma cell proliferation. Cancer 115, 4959-4972.
38. Lipfert, L., Haimovich, B., Schaller, M. D., Cobb, B. S., Parsons, J. T. and Brugge, J. S. (1992). Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets. J. Cell Biol. 119, 905-912.
39. Lu, Z., Ghosh, S., Wang, Z. and Hunter, T. (2003). Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 4, 499-515.
40. Marat, A. L. and McPherson, P. S. (2010). The connecdenn family, Rab35 guanine nucleotide exchange factors interfacing with the clathrin machinery. J. Biol. Chem. 285, 10627-10637.
41. Maret, D., Gruzglin, E., Sadr, M. S., Siu, V., Shan, W., Koch, A. W., Seidah, N. G., Del Maestro, R. F. and Colman, D. R. (2010). Surface expression of precursor Ncadherin promotes tumor cell invasion. Neoplasia 12, 1066-1080.
42. Margadant, C., Monsuur, H. N., Norman, J. C. and Sonnenberg, A. (2011). Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614.
43. Mattoon, D. R., Lamothe, B., Lax, I. and Schlessinger, J. (2004). The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol. 2, 24.
44. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
45. Menju, T., Hashimoto, S., Hashimoto, A., Otsuka, Y., Handa, H., Ogawa, E., Toda, Y., Wada, H., Date, H. and Sabe, H. (2011). Engagement of overexpressed Her2 with GEP100 induces autonomous invasive activities and provides a biomarker for metastases of lung adenocarcinoma. PLoS ONE 6, e25301.
46. Micalizzi, D. S., Farabaugh, S. M. and Ford, H. L. (2010). Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia 15, 117-134.
47. Miura, K., Nam, J. M., Kojima, C., Mochizuki, N. and Sabe, H. (2009). EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol. Biol. Cell 20, 1949-1959.
48. Morishige, M., Hashimoto, S., Ogawa, E., Toda, Y., Kotani, H., Hirose, M., Wei, S., Hashimoto, A., Yamada, A., Yano, H. et al. (2008). GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 10, 85-92.
49. 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.
50. Muralidharan-Chari, V., Hoover, H., Clancy, J., Schweitzer, J., Suckow, M. A., Schroeder, V., Castellino, F. J., Schorey, J. S. and D'Souza-Schorey, C. (2009). ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res. 69, 2201-2209.
51. Naslavsky, N., Boehm, M., Backlund, P. S., Jr and Caplan, S. (2004). Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane. Mol. Biol. Cell 15, 2410-2422.
52. Palacios, F., Price, L., Schweitzer, J., Collard, J. G. and D'Souza-Schorey, C. (2001). An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
53. Palacios, F., Schweitzer, J. K., Boshans, R. L. and D'Souza-Schorey, C. (2002). ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4, 929-936.
54. Patino-Lopez, G., Dong, X., Ben-Aissa, K., Bernot, K. M., Itoh, T., Fukuda, M., Kruhlak, M. J., Samelson, L. E. and Shaw, S. (2008). Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J. Biol. Chem. 283, 18323-18330.
55. Polyak, K. and Weinberg, R. A. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273.
56. Poteryaev, D., Datta, S., Ackema, K., Zerial, M. and Spang, A. (2010). Identification of the switch in early-to-late endosome transition. Cell 141, 497-508.
57. Poupon, V., Girard, M., Legendre-Guillemin, V., Thomas, S., Bourbonniere, L., Philie, J., Bright, N. A. and McPherson, P. S. (2008). Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl. Acad. Sci. USA 105, 168-173.
58. 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.
59. Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., Leake, D., Godden, E. L., Albertson, D. G., Nieto, M. A. et al. (2005). Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123-127.
60. Rahajeng, J., Giridharan, S. S., Cai, B., Naslavsky, N. and Caplan, S. (2012). MICAL-L1 is a tubular endosomal membrane hub that connects Rab35 and Arf6 with Rab8a. Traffic 13, 82-93.
61. Rink, J., Ghigo, E., Kalaidzidis, Y. and Zerial, M. (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749.
62. Rodrigues, G. A., Falasca, M., Zhang, Z., Ong, S. H. and Schlessinger, J. (2000). A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20, 1448-1459.
63. Rojas, M., Yao, S. and Lin, Y. Z. (1996). Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J. Biol. Chem. 271, 27456-27461.
64. Sabe, H., Hashimoto, S., Morishige, M., Ogawa, E., Hashimoto, A., Nam, J. M., Miura, K., Yano, H. and Onodera, Y. (2009). The EGFR-GEP100-Arf6-AMAP1 signaling pathway specific to breast cancer invasion and metastasis. Traffic 10, 982-993.
65. Santy, L. C. and Casanova, J. E. (2001). Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610.
66. Schweitzer, J. K., Sedgwick, A. E. and D'Souza-Schorey, C. (2011). ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 22, 39-47.
67. Shoval, I., Ludwig, A. and Kalcheim, C. (2007). Antagonistic roles of full-length Ncadherin and its soluble BMP cleavage product in neural crest delamination. Development 134, 491-501.
68. Stepniak, E., Radice, G. L. and Vasioukhin, V. (2009). Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb. Perspect. Biol. 1, a002949.
69. Svensson, H. G., West, M. A., Mollahan, P., Prescott, A. R., Zaru, R. and Watts, C. (2008). A role for ARF6 in dendritic cell podosome formation and migration. Eur. J. Immunol. 38, 818-828.
70. Tague, S. E., Muralidharan, V. and D'Souza-Schorey, C. (2004). ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc. Natl. Acad. Sci. USA 101, 9671-9676.
71. Thiery, J. P. (2003). Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15, 740-746.
72. Thomas, S., Ritter, B., Verbich, D., Sanson, C., Bourbonnière, L., McKinney, R. A. and McPherson, P. S. (2009). Intersectin regulates dendritic spine development and somatodendritic endocytosis but not synaptic vesicle recycling in hippocampal neurons. J. Biol. Chem. 284, 12410-12419.
73. Uytterhoeven, V., Kuenen, S., Kasprowicz, J., Miskiewicz, K. and Verstreken, P. (2011). Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 145, 117-132.
74. Walseng, E., Bakke, O. and Roche, P. A. (2008). Major histocompatibility complex class II-peptide complexes internalize using a clathrin-and dynamin-independent endocytosis pathway. J. Biol. Chem. 283, 14717-14727.
75. Worthylake, R., Opresko, L. K. and Wiley, H. S. (1999). ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors. J. Biol. Chem. 274, 8865-8874.
76. Yilmaz, M. and Christofori, G. (2009). EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 28, 15-33.
77. Zhang, Q., Calafat, J., Janssen, H. and Greenberg, S. (1999). ARF6 is required for growth factor-and rac-mediated membrane ruffling in macrophages at a stage distal to rac membrane targeting. Mol. Cell. Biol. 19, 8158-8168.
78. Zwick, E., Hackel, P. O., Prenzel, N. and Ullrich, A. (1999). The EGF receptor as central transducer of heterologous signalling systems. Trends Pharmacol. Sci. 20, 408-412