The GTPase-activating protein RN-tre controls focal adhesion turnover and cell migration

Current Biology

Volumn 23, Issue 23, 2013, Pages 2355-2364

  Palamidessi, Andrea ^a   Frittoli, Emanuela ^a   Ducano, Nadia ^b   Offenhauser, Nina ^a   Sigismund, Sara ^a   Kajiho, Hiroaki ^a   Parazzoli, Dario ^a   Oldani, Amanda ^a   Gobbi, Marco ^c   Serini, Guido ^b   Di Fiore, Pier Paolo ^a,d,e   Scita, Giorgio ^a,e   Lanzetti, Letizia ^b  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^d EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; DOXYCYCLINE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAB PROTEIN; RAB11 PROTEIN; RAB30 PROTEIN, MOUSE; RN TRE PROTEIN, MOUSE; RN-TRE PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL ADHESION; CELL CULTURE; CELL MOTION; ENDOCYTOSIS; FOCAL ADHESION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; DOXYCYCLINE; ENDOCYTOSIS; FOCAL ADHESIONS; GTPASE-ACTIVATING PROTEINS; INTEGRIN BETA3; MICE; MICE, KNOCKOUT; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84889587778     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.09.060     Document Type: Article

References (45)

1. R. Zaidel-Bar, S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger Functional atlas of the integrin adhesome Nat. Cell Biol. 9 2007 858 867
2. A.J. Ridley, M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, and A.R. Horwitz Cell migration: integrating signals from front to back Science 302 2003 1704 1709
3. D. Valdembri, and G. Serini Regulation of adhesion site dynamics by integrin traffic Curr. Opin. Cell Biol. 24 2012 582 591
4. T. Pellinen, A. Arjonen, K. Vuoriluoto, K. Kallio, J.A. Fransen, and J. Ivaska Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins J. Cell Biol. 173 2006 767 780
5. E.J. Ezratty, C. Bertaux, E.E. Marcantonio, and G.G. Gundersen Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells J. Cell Biol. 187 2009 733 747
6. D. Valdembri, P.T. Caswell, K.I. Anderson, J.P. Schwarz, I. König, E. Astanina, F. Caccavari, J.C. Norman, M.J. Humphries, F. Bussolino, and G. Serini Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells PLoS Biol. 7 2009 e25
7. E.J. Ezratty, M.A. Partridge, and G.G. Gundersen Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase Nat. Cell Biol. 7 2005 581 590
8. W.T. Chao, and J. Kunz Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins FEBS Lett. 583 2009 1337 1343
9. A. Mai, S. Veltel, T. Pellinen, A. Padzik, E. Coffey, V. Marjomäki, and J. Ivaska Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration J. Cell Biol. 194 2011 291 306
10. M. Zerial, and H. McBride Rab proteins as membrane organizers Nat. Rev. Mol. Cell Biol. 2 2001 107 117
11. P.T. Caswell, S. Vadrevu, and J.C. Norman Integrins: masters and slaves of endocytic transport Nat. Rev. Mol. Cell Biol. 10 2009 843 853
12. L. Yuan, M.J. Fairchild, A.D. Perkins, and G. Tanentzapf Analysis of integrin turnover in fly myotendinous junctions J. Cell Sci. 123 2010 939 946
13. P. Mendoza, R. Ortiz, J. Díaz, A.F. Quest, L. Leyton, D. Stupack, and V.A. Torres Rab5 activation promotes focal adhesion disassembly, migration and invasiveness of tumor cells J Cell Sci 2013
14. C. Sandri, F. Caccavari, D. Valdembri, C. Camillo, S. Veltel, M. Santambrogio, L. Lanzetti, F. Bussolino, J. Ivaska, and G. Serini The R-Ras/RIN2/Rab5 complex controls endothelial cell adhesion and morphogenesis via active integrin endocytosis and Rac signaling Cell Res. 22 2012 1479 1501
15. G. Jékely, H.H. Sung, C.M. Luque, and P. Rørth Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration Dev. Cell 9 2005 197 207
16. A. Palamidessi, E. Frittoli, M. Garré, M. Faretta, M. Mione, I. Testa, A. Diaspro, L. Lanzetti, G. Scita, and P.P. Di Fiore Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration Cell 134 2008 135 147
17. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat. Rev. Mol. Cell Biol. 10 2009 513 525
18. M.A. Frasa, K.T. Koessmeier, M.R. Ahmadian, and V.M. Braga Illuminating the functional and structural repertoire of human TBC/RABGAPs Nat. Rev. Mol. Cell Biol. 13 2012 67 73
19. L. Lanzetti, V. Rybin, M.G. Malabarba, S. Christoforidis, G. Scita, M. Zerial, and P.P. Di Fiore The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5 Nature 408 2000 374 377
20. L. Lanzetti, A. Palamidessi, L. Areces, G. Scita, and P.P. Di Fiore Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases Nature 429 2004 309 314
21. A.K. Haas, E. Fuchs, R. Kopajtich, and F.A. Barr A GTPase-activating protein controls Rab5 function in endocytic trafficking Nat. Cell Biol. 7 2005 887 893
22. A.K. Haas, S. Yoshimura, D.J. Stephens, C. Preisinger, E. Fuchs, and F.A. Barr Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells J. Cell Sci. 120 2007 2997 3010
23. M. Rämet, P. Manfruelli, A. Pearson, B. Mathey-Prevot, and R.A. Ezekowitz Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli Nature 416 2002 644 648
24. S. Scholpp, and M. Brand Endocytosis controls spreading and effective signaling range of Fgf8 protein Curr. Biol. 14 2004 1834 1841
25. H.B. Schiller, C.C. Friedel, C. Boulegue, and R. Fässler Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins EMBO Rep. 12 2011 259 266
26. J.C. Kuo, X. Han, C.T. Hsiao, J.R. Yates 3rd, and C.M. Waterman Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation Nat. Cell Biol. 13 2011 383 393
27. L. Lanzetti, V. Margaria, F. Melander, L. Virgili, M.H. Lee, J. Bartek, and S. Jensen Regulation of the Rab5 GTPase-activating protein RN-tre by the dual specificity phosphatase Cdc14A in human cells J. Biol. Chem. 282 2007 15258 15270
28. G. Bazzoni, D.T. Shih, C.A. Buck, and M.E. Hemler Monoclonal antibody 9EG7 defines a novel beta 1 integrin epitope induced by soluble ligand and manganese, but inhibited by calcium J. Biol. Chem. 270 1995 25570 25577
29. K. Clark, R. Pankov, M.A. Travis, J.A. Askari, A.P. Mould, S.E. Craig, P. Newham, K.M. Yamada, and M.J. Humphries A specific alpha5beta 1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation J. Cell Sci. 118 2005 291 300
30. J.D. Humphries, A. Byron, and M.J. Humphries Integrin ligands at a glance J. Cell Sci. 119 2006 3901 3903
31. A. Simonsen, R. Lippé, S. Christoforidis, J.M. Gaullier, A. Brech, J. Callaghan, B.H. Toh, C. Murphy, M. Zerial, and H. Stenmark EEA1 links PI(3)K function to Rab5 regulation of endosome fusion Nature 394 1998 494 498
32. M.A. Barbieri, R.L. Roberts, A. Gumusboga, H. Highfield, C. Alvarez-Dominguez, A. Wells, and P.D. Stahl Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a J. Cell Biol. 151 2000 539 550
33. J. Liu, D. Lamb, M.M. Chou, Y.J. Liu, and G. Li Nerve growth factor-mediated neurite outgrowth via regulation of Rab5 Mol. Biol. Cell 18 2007 1375 1384
34. C. Bucci, R.G. Parton, I.H. Mather, H. Stunnenberg, K. Simons, B. Hoflack, and M. Zerial The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway Cell 70 1992 715 728
35. H. Stenmark, R.G. Parton, O. Steele-Mortimer, A. Lütcke, J. Gruenberg, and M. Zerial Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis EMBO J. 13 1994 1287 1296
36. M.H. Ginsberg, A. Partridge, and S.J. Shattil Integrin regulation Curr. Opin. Cell Biol. 17 2005 509 516
37. M. Roberts, S. Barry, A. Woods, P. van der Sluijs, and J. Norman PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading Curr. Biol. 11 2001 1392 1402
38. A. Zeigerer, J. Gilleron, R.L. Bogorad, G. Marsico, H. Nonaka, S. Seifert, H. Epstein-Barash, S. Kuchimanchi, C.G. Peng, and V.M. Ruda Rab5 is necessary for the biogenesis of the endolysosomal system in vivo Nature 485 2012 465 470
39. A. Teckchandani, N. Toida, J. Goodchild, C. Henderson, J. Watts, B. Wollscheid, and J.A. Cooper Quantitative proteomics identifies a Dab2/integrin module regulating cell migration J. Cell Biol. 186 2009 99 111
40. E.F. Foxman, E.J. Kunkel, and E.C. Butcher Integrating conflicting chemotactic signals. The role of memory in leukocyte navigation J. Cell Biol. 147 1999 577 588
41. C.M. Laukaitis, D.J. Webb, K. Donais, and A.F. Horwitz Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells J. Cell Biol 153 2001 1427 1440
42. C. Laflamme, G. Assaker, D. Ramel, J.F. Dorn, D. She, P.S. Maddox, and G. Emery Evi5 promotes collective cell migration through its Rab-GAP activity J. Cell Biol. 198 2012 57 67
43. G. Assaker, D. Ramel, S.K. Wculek, M. González-Gaitán, and G. Emery Spatial restriction of receptor tyrosine kinase activity through a polarized endocytic cycle controls border cell migration Proc. Natl. Acad. Sci. USA 107 2010 22558 22563
44. P. Levéen, M. Pekny, S. Gebre-Medhin, B. Swolin, E. Larsson, and C. Betsholtz Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities Genes Dev. 8 1994 1875 1887
45. G. Serio, V. Margaria, S. Jensen, A. Oldani, J. Bartek, F. Bussolino, and L. Lanzetti Small GTPase Rab5 participates in chromosome congression and regulates localization of the centromere-associated protein CENP-F to kinetochores Proc. Natl. Acad. Sci. USA 108 2011 17337 17342