The NPIY motif in the integrin β1 tail dictates the requirement for talin-1 in outside-in signaling

Journal of Cell Science

Volumn 123, Issue 8, 2010, Pages 1216-1226

  Nieves, Bethsaida ^a   Jones, Christopher W ^a   Ward, Rachel ^a   Ohta, Yasutaka ^b   Reverte, Carlos G ^a   LaFlamme, Susan E ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b KITASATO UNIVERSITY   (Japan)

Author keywords

Cytoplasmic domain; FLNa; Integrin; Microtubule; Talin

Indexed keywords

ALANINE; BETA1 INTEGRIN; FILAMIN A; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN FILGAP; INTEGRIN; RAC PROTEIN; SMALL INTERFERING RNA; TALIN; TALIN 1; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL SPREADING; CONTROLLED STUDY; FOCAL ADHESION; MICROTUBULE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; STRESS FIBER;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL MOVEMENT; CHO CELLS; CONTRACTILE PROTEINS; CRICETINAE; CRICETULUS; FOCAL ADHESIONS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; STRESS FIBERS; STRUCTURE-ACTIVITY RELATIONSHIP; TALIN;

EID: 77951189703     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.056549     Document Type: Article

References (59)

1. Akhmanova, A. and Steinmetz, M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309-322.
2. 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.
3. Baldassarre, M., Razinia, Z., Burande, C. F., Lamsoul, I., Lutz, P. G. and Calderwood, D. A. (2009). Filamins regulate cell spreading and initiation of cell migration. PLoS One 4, e7830.
4. Berrier, A. L., Mastrangelo, A. M., Downward, J., Ginsberg, M. and LaFlamme, S. E. (2000). Activated R-ras, Rac1, PI 3-kinase and PKCepsilon can each restore cell spreading inhibited by isolated integrin beta1 cytoplasmic domains. J. Cell Biol. 151, 1549-1560.
5. Berrier, A. L., Martinez, R., Bokoch, G. M. and LaFlamme, S. E. (2002). The integrin beta tail is required and sufficient to regulate adhesion signaling to Rac1. J. Cell Sci. 115, 4285-4291.
6. Berrier, A. L., Jones, C. W. and LaFlamme, S. E. (2008). Tac-beta1 inhibits FAK activation and Src signaling. Biochem. Biophys. Res. Commun. 368, 62-67.
7. Bodeau, A. L., Berrier, A. L., Mastrangelo, A. M., Martinez, R. and LaFlamme, S. E. (2001). A functional comparison of mutations in integrin beta cytoplasmic domains: effects on the regulation of tyrosine phosphorylation, cell spreading, cell attachment and beta1 integrin conformation. J. Cell Sci. 114, 2795-2807.
8. Brown, P. J. and Juliano, R. L. (1985). Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science 228, 1448-1451.
9. Calderwood, D. A., Zent, R., Grant, R., Rees, D. J., Hynes, R. O. and Ginsberg, M. H. (1999). The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274, 28071-28074.
10. Calderwood, D. A., Huttenlocher, A., Kiosses, W. B., Rose, D. M., Woodside, D. G., Schwartz, M. A. and Ginsberg, M. H. (2001). Increased filamin binding to beta-integrin cytoplasmic domains inhibits cell migration. Nat. Cell Biol. 3, 1060-1068.
11. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C. and Ginsberg, M. H. (2003). Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 100, 2272-2277.
12. Critchley, D. R. (2004). Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem. Soc. Trans. 32, 831-836.
13. Gahmberg, C. G., Fagerholm, S. C., Nurmi, S. M., Chavakis, T., Marchesan, S. and Gronholm, M. (2009). Regulation of integrin activity and signalling. Biochim. Biophys. Acta 1790, 431-444.
14. Gehler, S., Baldassarre, M., Lad, Y., Leight, J. L., Wozniak, M. A., Riching, K. M., Eliceiri, K. W., Weaver, V. M., Calderwood, D. A. and Keely, P. J. (2009). Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol. Biol. Cell 20, 3224-3238.
15. Gingras, A. R., Ziegler, W. H., Bobkov, A. A., Joyce, M. G., Fasci, D., Himmel, M., Rothemund, S., Ritter, A., Grossmann, J. G., Patel, B. et al. (2009). Structural determinants of integrin binding to the talin rod. J. Biol. Chem 284, 8866-8876.
16. Goksoy, E., Ma, Y. Q., Wang, X., Kong, X., Perera, D., Plow, E. F. and Qin, J. (2008). Structural basis for the autoinhibition of talin in regulating integrin activation. Mol. Cell 31, 124-133.
17. Hannigan, G. E., Leung-Hagesteijn, C., Fitz-Gibbon, L., Coppolino, M. G., Radeva, G., Filmus, J., Bell, J. C. and Dedhar, S. (1996). Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379, 91-96.
18. Harburger, D. S., Bouaouina, M. and Calderwood, D. A. (2009). 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, 11485-11497.
19. Hughes, P. E., Diaz-Gonzalez, F., Leong, L., Wu, C., McDonald, J. A., Shattil, S. J. and Ginsberg, M. H. (1996). Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. J. Biol. Chem. 271, 6571-6574.
20. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
21. Jaffe, A. B. and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
22. Kaapa, A., Peter, K. and Ylanne, J. (1999). Effects of mutations in the cytoplasmic domain of integrin beta(1) to talin binding and cell spreading. Exp. Cell Res. 250, 524-1234
23. Kaverina, I., Rottner, K. and Small, J. V. (1998). Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142, 181-190.
24. 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.
25. Kiema, T., Lad, Y., Jiang, P., Oxley, C. L., Baldassarre, M., Wegener, K. L., Campbell, I. D., Ylanne, J. and Calderwood, D. A. (2006). The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 21, 337-347.
26. Kim, M., Carman, C. V. and Springer, T. A. (2003). Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 301, 1720-1725.
27. Lad, Y., Kiema, T., Jiang, P., Pentikainen, O. T., Coles, C. H., Campbell, I. D., Calderwood, D. A. and Ylanne, J. (2007). Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J. 26, 3993-4004.
28. Larjava, H., Plow, E. F. and Wu, C. (2008). Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep. 9, 1203-1208.
29. Larsen, M., Artym, V. V., Green, J. A. and Yamada, K. M. (2006). The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18, 463-471.
30. Legate, K. R. and Fassler, R. (2009). Mechanisms that regulate adaptor binding to betaintegrin cytoplasmic tails. J. Cell Sci. 122, 187-198.
31. Li, R., Mitra, N., Gratkowski, H., Vilaire, G., Litvinov, R., Nagasami, C., Weisel, J. W., Lear, J. D., DeGrado, W. F. and Bennett, J. S. (2003). Activation of integrin alphaIIbbeta3 by modulation of transmembrane helix associations. Science 300, 795-798.
32. Luo, B. H., Carman, C. V., Takagi, J. and Springer, T. A. (2005). Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc. Natl. Acad. Sci. USA 102, 3679-3684.
33. Martel, V., Racaud-Sultan, C., Dupe, S., Marie, C., Paulhe, F., Galmiche, A., Block, M. R. and Albiges-Rizo, C. (2001). Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J. Biol. Chem. 276, 21217-21227.
34. Nakamura, F., Heikkinen, O., Pentikainen, O. T., Osborn, T. M., Kasza, K. E., Weitz, D. A., Kupiainen, O., Permi, P., Kilpelainen, I., Ylanne, J. et al. (2009). Molecular basis of filamin A-FilGAP interaction and its impairment in congenital disorders associated with filamin A mutations. PLoS One 4, e4928.
35. Ohta, Y., Hartwig, J. H. and Stossel, T. P. (2006). FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling. Nat. Cell Biol. 8, 803-814.
36. Otey, C. A. and Carpen, O. (2004). Alpha-actinin revisited: a fresh look at an old player. Cell Motil. Cytoskeleton 58, 104-111.
37. Otey, C. A., Vasquez, G. B., Burridge, K. and Erickson, B. W. (1993). Mapping of the alpha-actinin binding site within the beta 1 integrin cytoplasmic domain. J. Biol. Chem. 268, 21193-21197.
38. O'Toole, T. E., Katagiri, Y., Faull, R. J., Peter, K., Tamura, R., Quaranta, V., Loftus, J. C., Shattil, S. J. and Ginsberg, M. H. (1994). Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124, 1047-1059.
39. O'Toole, T. E., Ylanne, J. and Culley, B. M. (1995). Regulation of integrin affinity states through an NPXY motif in the beta subunit cytoplasmic domain. J. Biol. Chem. 270, 8553-8558.
40. Partridge, A. W., Liu, S., Kim, S., Bowie, J. U. and Ginsberg, M. H. (2005). Transmembrane domain helix packing stabilizes integrin alphaIIbbeta3 in the low affinity state. J. Biol. Chem. 280, 7294-7300.
41. Pentikainen, U. and Ylanne, J. (2009). The regulation mechanism for the auto-inhibition of binding of human filamin A to integrin. J. Mol. Biol. 393, 644-657.
42. Pfaff, M., Liu, S., Erle, D. J. and Ginsberg, M. H. (1998). Integrin beta cytoplasmic domains differentially bind to cytoskeletal proteins. J. Biol. Chem. 273, 6104-6109.
43. Price, L. S., Leng, J., Schwartz, M. A. and Bokoch, G. M. (1998). Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1863-1871.
44. Priddle, H., Hemmings, L., Monkley, S., Woods, A., Patel, B., Sutton, D., Dunn, G. A., Zicha, D. and Critchley, D. R. (1998). Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated embryonic stem cells. J. Cell Biol. 142, 1121-1133.
45. Rajfur, Z., Roy, P., Otey, C., Romer, L. and Jacobson, K. (2002). Dissecting the link between stress fibres and focal adhesions by CALI with EGFP fusion proteins. Nat. Cell Biol. 4, 286-293.
46. Reddy, K. B., Gascard, P., Price, M. G., Negrescu, E. V. and Fox, J. E. (1998). Identification of an interaction between the m-band protein skelemin and beta-integrin subunits. Colocalization of a skelemin-like protein with beta1- and beta3-integrins in non-muscle cells. J. Biol. Chem. 273, 35039-35047.
47. Reverte, C. G., Benware, A., Jones, C. W. and LaFlamme, S. E. (2006). Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J. Cell Biol. 174, 491-497.
48. Shi, X., Ma, Y. Q., Tu, Y., Chen, K., Wu, S., Fukuda, K., Qin, J., Plow, E. F. and Wu, C. (2007). The MIG-2/integrin interaction strengthens cell-matrix adhesion and modulates cell motility. J. Biol. Chem. 282, 20455-20466.
49. Shifrin, Y., Arora, P. D., Ohta, Y., Calderwood, D. A. and McCulloch, C. A. (2009). The role of FilGAP-filamin A interactions in mechanoprotection. Mol. Biol. Cell 20, 1269-1279.
50. Small, J. V. and Kaverina, I. (2003). Microtubules meet substrate adhesions to arrange cell polarity. Curr. Opin. Cell Biol. 15, 40-47.
51. Small, J. V., Geiger, B., Kaverina, I. and Bershadsky, A. (2002). How do microtubules guide migrating cells? Nat. Rev. Mol. Cell. Biol. 3, 957-964.
52. Stossel, T. P., Condeelis, J., Cooley, L., Hartwig, J. H., Noegel, A., Schleicher, M. and Shapiro, S. S. (2001). Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell. Biol. 2, 138-145.
53. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H. and Calderwood, D. A. (2003). Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106.
54. Takala, H., Nurminen, E., Nurmi, S. M., Aatonen, M., Strandin, T., Takatalo, M., Kiema, T., Gahmberg, C. G., Ylanne, J. and Fagerholm, S. C. (2008). Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding. Blood 112, 1853-1862.
55. van der Flier, A. and Sonnenberg, A. (2001). Structural and functional aspects of filamins. Biochim. Biophys. Acta 1538, 99-117.
56. van der Flier, A., Kuikman, I., Kramer, D., Geerts, D., Kreft, M., Takafuta, T., Shapiro, S. S. and Sonnenberg, A. (2002). Different splice variants of filamin-B affect myogenesis, subcellular distribution, and determine binding to integrin [beta] subunits. J. Cell Biol. 156, 361-376.
57. Wegener, K. L., Partridge, A. W., Han, J., Pickford, A. R., Liddington, R. C., Ginsberg, M. H. and Campbell, I. D. (2007). Structural basis of integrin activation by talin. Cell 128, 171-182.
58. Yan, B., Calderwood, D. A., Yaspan, B. and Ginsberg, M. H. (2001). Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain. J. Biol. Chem. 276, 28164-28170.
59. Zhang, X., Jiang, G., Cai, Y., Monkley, S. J., Critchley, D. R. and Sheetz, M. P. (2008). Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10, 1062-1068.