Distinct roles of talin and kindlin in regulating integrin α5β1 function and trafficking

Current Biology

Volumn 22, Issue 17, 2012, Pages 1554-1563

  Margadant, Coert ^a   Kreft, Maaike ^a   De Groot, Dirk Jan ^a   Norman, Jim C ^b   Sonnenberg, Arnoud ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; KINDLIN 2 PROTEIN, MOUSE; KINDLIN-2 PROTEIN, MOUSE; MUSCLE PROTEIN; SIGNAL PEPTIDE; TALIN; TALIN PROTEIN, MOUSE; VERY LATE ACTIVATION ANTIGEN 5;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MOTION; ENDOSOME; GENETICS; LYSOSOME; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CELL MOVEMENT; CYTOSKELETAL PROTEINS; ENDOSOMES; INTEGRIN ALPHA5BETA1; LYSOSOMES; MICE; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TALIN;

EID: 84866168074     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.06.060     Document Type: Article

References (44)

1. C. Kim, F. Ye, and M.H. Ginsberg Regulation of integrin activation Annu. Rev. Cell Dev. Biol. 27 2011 321 345
2. B. Geiger, and K.M. Yamada Molecular architecture and function of matrix adhesions Cold Spring Harb. Perspect. Biol. 3 2011
3. M. Moser, K.R. Legate, R. Zent, and R. Fässler The tail of integrins, talin, and kindlins Science 324 2009 895 899
4. D.A. Law, F.R. DeGuzman, P. Heiser, K. Ministri-Madrid, N. Killeen, and D.R. Phillips Integrin cytoplasmic tyrosine motif is required for outside-in alphaIIbbeta3 signalling and platelet function Nature 401 1999 808 811
5. H. Chen, Z. Zou, K.L. Sarratt, D. Zhou, M. Zhang, E. Sebzda, D.A. Hammer, and M.L. Kahn In vivo beta1 integrin function requires phosphorylation- independent regulation by cytoplasmic tyrosines Genes Dev. 20 2006 927 932
6. A. Czuchra, H. Meyer, K.R. Legate, C. Brakebusch, and R. Fässler Genetic analysis of beta1 integrin "activation motifs" in mice J. Cell Biol. 174 2006 889 899 (Pubitemid 44373737)
7. C. Margadant, H.N. Monsuur, J.C. Norman, and A. Sonnenberg Mechanisms of integrin activation and trafficking Curr. Opin. Cell Biol. 23 2011 607 614
8. S.A. Wickström, K. Radovanac, and R. Fässler Genetic analyses of integrin signaling Cold Spring Harb. Perspect. Biol. 3 2011
9. N.H. Brown, S.L. Gregory, W.L. Rickoll, L.I. Fessler, M. Prout, R.A.H. White, and J.W. Fristrom Talin is essential for integrin function in Drosophila Dev. Cell 3 2002 569 579 (Pubitemid 35252265)
10. 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 (Pubitemid 32863188)
11. P.T. Caswell, H.J. Spence, M. Parsons, D.P. White, K. Clark, K.W. Cheng, G.B. Mills, M.J. Humphries, A.J. Messent, and K.I. Anderson Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments Dev. Cell 13 2007 496 510 (Pubitemid 47514517)
12. P.T. Caswell, M. Chan, A.J. Lindsay, M.W. McCaffrey, D. Boettiger, and J.C. Norman Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments J. Cell Biol. 183 2008 143 155
13. 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
14. T. Nishimura, and K. Kaibuchi Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3 Dev. Cell 13 2007 15 28 (Pubitemid 46972036)
15. W.-T. Chao, and J. Kunz Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins FEBS Lett. 583 2009 1337 1343
16. 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
17. 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
18. T. Pellinen, S. Tuomi, A. Arjonen, M. Wolf, H. Edgren, H. Meyer, R. Grosse, T. Kitzing, J.K. Rantala, and O. Kallioniemi Integrin trafficking regulated by Rab21 is necessary for cytokinesis Dev. Cell 15 2008 371 385
19. 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
20. A. Arjonen, J. Alanko, S. Veltel, and J. Ivaska Distinct recycling of active and inactive β1 integrins Traffic 2012 10.1111/j.1600-0854.2012. 01327.x Published online January 5, 2012
21. F. Shi, and J. Sottile Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover J. Cell Sci. 121 2008 2360 2371
22. V.H. Lobert, A. Brech, N.M. Pedersen, J. Wesche, A. Oppelt, L. Malerod, and H. Stenmark Ubiquitination of alpha 5 beta 1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes Dev. Cell 19 2010 148 159
23. M.A. Dozynkiewicz, N.B. Jamieson, I. MacPherson, J. Grindlay, P. van den Berghe, A. von Thun, J.P. Morton, C. Gourley, P. Timpson, and C. Nixon Rab25 and the CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression Dev. Cell 22 2012 131 145
24. C. Gimond, A. van Der Flier, S. van Delft, C. Brakebusch, I. Kuikman, J.G. Collard, R. Fässler, and A. Sonnenberg Induction of cell scattering by expression of beta1 integrins in beta1-deficient epithelial cells requires activation of members of the rho family of GTPases and downregulation of cadherin and catenin function J. Cell Biol. 147 1999 1325 1340 (Pubitemid 30012816)
25. E.H. Danen, P. Sonneveld, C. Brakebusch, R. Fässler, and A. Sonnenberg The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis J. Cell Biol. 159 2002 1071 1086 (Pubitemid 36055761)
26. E.H. Danen, J. van Rheenen, W. Franken, S. Huveneers, P. Sonneveld, K. Jalink, and A. Sonnenberg Integrins control motile strategy through a Rho-cofilin pathway J. Cell Biol. 169 2005 515 526 (Pubitemid 40686701)
27. D.J. Webb, H. Zhang, D. Majumdar, and A.F. Horwitz alpha5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons J. Biol. Chem. 282 2007 6929 6935 (Pubitemid 47093674)
28. K. Wennerberg, L. Lohikangas, D. Gullberg, M. Pfaff, S. Johansson, and R. Fässler Beta 1 integrin-dependent and -independent polymerization of fibronectin J. Cell Biol. 132 1996 227 238
29. D.A. Calderwood, Y. Fujioka, J.M. de Pereda, B. García-Alvarez, T. Nakamoto, B. Margolis, C.J. McGlade, R.C. Liddington, and M.H. Ginsberg Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling Proc. Natl. Acad. Sci. USA 100 2003 2272 2277 (Pubitemid 36297489)
30. C.J. McCleverty, D.C. Lin, and R.C. Liddington Structure of the PTB domain of tensin1 and a model for its recruitment to fibrillar adhesions Protein Sci. 16 2007 1223 1229 (Pubitemid 46849230)
31. R. Pankov, E. Cukierman, B.Z. Katz, K. Matsumoto, D.C. Lin, S. Lin, C. Hahn, and K.M. Yamada Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis J. Cell Biol. 148 2000 1075 1090
32. C. Wu, V.M. Keivens, T.E. O'Toole, J.A. McDonald, and M.H. Ginsberg Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix Cell 83 1995 715 724
33. S.J. Monkley, X.H. Zhou, S.J. Kinston, S.M. Giblett, L. Hemmings, H. Priddle, J.E. Brown, C.A. Pritchard, D.R. Critchley, and R. Fässler Disruption of the talin gene arrests mouse development at the gastrulation stage Dev. Dyn. 219 2000 560 574
34. J. de Rooij, A. Kerstens, G. Danuser, M.A. Schwartz, and C.M. Waterman-Storer Integrin-dependent actomyosin contraction regulates epithelial cell scattering J. Cell Biol. 171 2005 153 164 (Pubitemid 41434610)
35. B. Nieves, C.W. Jones, R. Ward, Y. Ohta, C.G. Reverte, and S.E. LaFlamme The NPIY motif in the integrin beta1 tail dictates the requirement for talin-1 in outside-in signaling J. Cell Sci. 123 2010 1216 1226
36. T. Kiema, Y. Lad, P. Jiang, C.L. Oxley, M. Baldassarre, K.L. Wegener, I.D. Campbell, J. Ylänne, and D.A. Calderwood The molecular basis of filamin binding to integrins and competition with talin Mol. Cell 21 2006 337 347 (Pubitemid 43163529)
37. D.S. Harburger, M. Bouaouina, and D.A. Calderwood Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects J. Biol. Chem. 284 2009 11485 11497
38. H. Qu, Y. Tu, X. Shi, H. Larjava, M.A. Saleem, S.J. Shattil, K. Fukuda, J. Qin, M. Kretzler, and C. Wu Kindlin-2 regulates podocyte adhesion and fibronectin matrix deposition through interactions with phosphoinositides and integrins J. Cell Sci. 124 2011 879 891
39. S. Schmidt, I. Nakchbandi, R. Ruppert, N. Kawelke, M.W. Hess, K. Pfaller, P. Jurdic, R. Fässler, and M. Moser Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption J. Cell Biol. 192 2011 883 897
40. F. Steinberg, K.J. Heesom, M.D. Bass, and P.J. Cullen SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways J. Cell Biol. 197 2012 219 230
41. R.T. Böttcher, C. Stremmel, A. Meves, H. Meyer, M. Widmaier, H.Y. Tseng, and R. Fässler Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail Nat. Cell Biol. 14 2012 584 592
42. M.S. Bretscher Circulating integrins: alpha 5 beta 1, alpha 6 beta 4 and Mac-1, but not alpha 3 beta 1, alpha 4 beta 1 or LFA-1 EMBO J. 11 1992 405 410
43. 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 (Pubitemid 46165584)
44. 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