Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration

Journal of Cell Biology

Volumn 194, Issue 2, 2011, Pages 291-306

  Mai, Anja ^a,b,d   Veltel, Stefan ^a,b   Pellinen, Teijo ^b   Padzik, Artur ^a   Coffey, Eleanor ^a   Marjomäki, Varpu ^c   Ivaska, Johanna ^a,b,d  

^a TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; BETA1 INTEGRIN; EARLY ENDOSOME ANTIGEN 1; INTEGRIN; PROTEIN P120; PROTEIN P120RASGAP; PROTEIN RAB21; RAB PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE REGULATION; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

ANIMALS; BINDING, COMPETITIVE; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CYTOPLASM; ENDOSOMES; HUMANS; INTEGRINS; MICE; MODELS, BIOLOGICAL; P120 GTPASE ACTIVATING PROTEIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RAB GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 79961101608     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201012126     Document Type: Article

References (45)

1. Anand, S., B.K. Majeti, L.M. Acevedo, E.A. Murphy, R. Mukthavaram, L. Scheppke, M. Huang, D.J. Shields, J.N. Lindquist, P.E. Lapinski, et al. 2010. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat. Med. 16:909-914.
2. Bradley, W.D., S.E. Hernández, J. Settleman, and A.J. Koleske. 2006. Integrin signaling through Arg activates p190RhoGAP by promoting its binding to p120RasGAP and recruitment to the membrane. Mol. Biol. Cell. 17:4827-4836.
3. Caswell, P.T., and J.C. Norman. 2006. Integrin trafficking and the control of cell migration. Traffic. 7:14-21.
4. Caswell, P., and J. Norman. 2008. Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 18:257-263.
5. Caswell, P.T., H.J. Spence, M. Parsons, D.P. White, K. Clark, K.W. Cheng, G.B. Mills, M.J. Humphries, A.J. Messent, K.I. Anderson, et al. 2007. Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell. 13:496-510.
6. Caswell, P.T., M. Chan, A.J. Lindsay, M.W. McCaffrey, D. Boettiger, and J.C. Norman. 2008. Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183:143-155.
7. Caswell, P.T., S. Vadrevu, and J.C. Norman. 2009. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10:843-853.
8. Cooper, J.A., and A. Kashishian. 1993. In vivo binding properties of SH2 domains from GTPase-activating protein and phosphatidylinositol 3-kinase. Mol. Cell. Biol. 13:1737-1745.
9. Huang, D.C., C.J. Marshall, and J.F. Hancock. 1993. Plasma membrane-targeted ras GTPase-activating protein is a potent suppressor of p21ras function. Mol. Cell. Biol. 13:2420-2431.
10. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
11. Jones, R.B., A. Gordus, J.A. Krall, and G. MacBeath. 2006. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature. 439:168-174.
12. Kazlauskas, A., C. Ellis, T. Pawson, and J.A. Cooper. 1990. Binding of GAP to activated PDGF receptors. Science. 247:1578-1581.
13. Kikuchi, Y., M. Miyauchi, I. Kizawa, K. Oomori, and K. Kato. 1986. Establishment of a cisplatin-resistant human ovarian cancer cell line. J. Natl. Cancer Inst. 77:1181-1185.
14. Kraemer, A., H.R. Rehmann, R.H. Cool, C. Theiss, J. de Rooij, J.L. Bos, and A. Wittinghofer. 2001. Dynamic interaction of cAMP with the Rap guanine-nucleotide exchange factor Epac1. J. Mol. Biol. 306:1167-1177.
15. Kulkarni, S.V., G. Gish, P. van der Geer, M. Henkemeyer, and T. Pawson. 2000. Role of p120 Ras-GAP in directed cell movement. J. Cell Biol. 149:457-470.
16. Legate, K.R., S.A. Wickström, and R. Fässler. 2009. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 23:397-418.
17. Liu, K., and G. Li. 1998. Catalytic domain of the p120 Ras GAP binds to RAb5 and stimulates its GTPase activity. J. Biol. Chem. 273:10087-10090.
18. Liu, S., D.A. Calderwood, and M.H. Ginsberg. 2000. Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113:3563-3571.
19. Muller, P.A., P.T. Caswell, B. Doyle, M.P. Iwanicki, E.H. Tan, S. Karim, N. Lukashchuk, D.A. Gillespie, R.L. Ludwig, P. Gosselin, et al. 2009. Mutant p53 drives invasion by promoting integrin recycling. Cell. 139:1327-1341.
20. Ohya, T., M. Miaczynska, U. Coskun, B. Lommer, A. Runge, D. Drechsel, Y. Kalaidzidis, and M. Zerial. 2009. Reconstitution of Rab- and SNAREdependent membrane fusion by synthetic endosomes. Nature. 459:1091-1097.
21. Palecek, S.P., J.C. Loftus, M.H. Ginsberg, D.A. Lauffenburger, and A.F. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 385:537-540.
22. Pamonsinlapatham, P., B. Gril, S. Dufour, R. Hadj-Slimane, V. Gigoux, S. Pethe, S. L'hoste, J. Camonis, C. Garbay, F. Raynaud, and M. Vidal. 2008. Capns1, a new binding partner of RasGAP-SH3 domain in K-Ras(V12) oncogenic cells: modulation of cell survival and migration. Cell. Signal. 20:2119-2126.
23. Pamonsinlapatham, P., R. Hadj-Slimane, Y. Lepelletier, B. Allain, M. Toccafondi, C. Garbay, and F. Raynaud. 2009. P120-Ras GTPase activating protein (RasGAP): a multi-interacting protein in downstream signaling. Biochimie. 91:320-328.
24. Pawson, T. 1995. Protein modules and signalling networks. Nature. 373:573-580.
25. Peacock, J.G., A.L. Miller, W.D. Bradley, O.C. Rodriguez, D.J. Webb, and A.J. Koleske. 2007. The Abl-related gene tyrosine kinase acts through p190RhoGAP to inhibit actomyosin contractility and regulate focal adhesion dynamics upon adhesion to fibronectin. Mol. Biol. Cell. 18:3860-3872.
26. Pellinen, T., and J. Ivaska. 2006. Integrin traffic. J. Cell Sci. 119:3723-3731.
27. Pellinen, T., A. Arjonen, K. Vuoriluoto, K. Kallio, J.A. Fransen, and J. Ivaska. 2006. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173:767-780.
28. Pellinen, T., S. Tuomi, A. Arjonen, M. Wolf, H. Edgren, H. Meyer, R. Grosse, T. Kitzing, J.K. Rantala, O. Kallioniemi, et al. 2008. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell. 15:371-385.
29. Powelka, A.M., J. Sun, J. Li, M. Gao, L.M. Shaw, A. Sonnenberg, and V.W. Hsu. 2004. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic. 5:20-36.
30. Roberts, M., S. Barry, A. Woods, P. van der Sluijs, and J. Norman. 2001. PDGFregulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11:1392-1402.
31. Roberts, M.S., A.J. Woods, T.C. Dale, P. Van Der Sluijs, and J.C. Norman. 2004. Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol. Cell. Biol. 24:1505-1515.
32. Scheffzek, K., M.R. Ahmadian, W. Kabsch, L. Wiesmüller, A. Lautwein, F. Schmitz, and A. Wittinghofer. 1997. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science. 277:333-338.
33. Schwartz, S.L., C. Cao, O. Pylypenko, A. Rak, and A. Wandinger-Ness. 2007. Rab GTPases at a glance. J. Cell Sci. 120:3905-3910.
34. Scita, G., and P.P. Di Fiore. 2010. The endocytic matrix. Nature. 463:464-473.
35. Sharma, S.V. 1998. Rapid recruitment of p120RasGAP and its associated protein, p190RhoGAP, to the cytoskeleton during integrin mediated cell-substrate interaction. Oncogene. 17:271-281.
36. Slot, J.W., and H.J. Geuze. 2007. Cryosectioning and immunolabeling. Nat. Protoc. 2:2480-2491.
37. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
38. Tomar, A., and D.D. Schlaepfer. 2009. Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr. Opin. Cell Biol. 21:676-683.
39. Tomar, A., S.T. Lim, Y. Lim, and D.D. Schlaepfer. 2009. A FAK-p120RasGAPp190RhoGAP complex regulates polarity in migrating cells. J. Cell Sci. 122:1852-1862.
40. Trahey, M., G. Wong, R. Halenbeck, B. Rubinfeld, G.A. Martin, M. Ladner, C.M. Long, W.J. Crosier, K. Watt, K. Koths, et al. 1988. Molecular cloning of two types of GAP complementary DNA from human placenta. Science. 242:1697-1700.
41. Veltel, S., R. Gasper, E. Eisenacher, and A. Wittinghofer. 2008. The retinitis pigmentosa 2 gene product is a GTPase-activating protein for Arf-like 3. Nat. Struct. Mol. Biol. 15:373-380.
42. Wang, Z., P.S. Tung, and M.F. Moran. 1996. Association of p120 ras GAP with endocytic components and colocalization with epidermal growth factor (EGF) receptor in response to EGF stimulation. Cell Growth Differ. 7:123-133.
43. White, D.P., P.T. Caswell, and J.C. Norman. 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.
44. Zerial, M., and H. McBride. 2001. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2:107-117.
45. Zhu, G., J. Chen, J. Liu, J.S. Brunzelle, B. Huang, N. Wakeham, S. Terzyan, X. Li, Z. Rao, G. Li, and X.C. Zhang. 2007. Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J. 26:3484-3493.