Structure of a double ubiquitin-like domain in the talin head: A role in integrin activation

EMBO Journal

Volumn 29, Issue 6, 2010, Pages 1069-1080

  Goult, Benjamin T ^a   Bouaouina, Mohamed ^b   Elliott, Paul R ^c   Bate, Neil ^a   Patel, Bipin ^a   Gingras, Alexandre R ^a   Grossmann, J Günter ^c   Roberts, Gordon C K ^a   Calderwood, David A ^b   Critchley, David R ^a   Barsukov, Igor L ^c  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Focal adhesions; Integrins; NMR; Phospholipids; Talin

Indexed keywords

BETA1 INTEGRIN; INTEGRIN; MEMBRANE PHOSPHOLIPID; TALIN; UBIQUITIN;

ARTICLE; BINDING SITE; LIPID BILAYER; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; BINDING SITES; CELL ADHESION; INTEGRINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; TALIN; UBIQUITIN;

EID: 77949566587     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.4     Document Type: Article

References (62)

1. Anthis NJ, Wegener KL, Ye F, Kim C, Goult BT, Lowe ED, Vakonakis I, Bate N, Critchley DR, Ginsberg MH, Campbell ID (2009) The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 28: 3623-3632
2. Aszodi A, Legate KR, Nakchbandi I, Fassler R (2006) What mouse mutants teach us about extracellular matrix function. Annu Rev Cell Dev Biol 22: 591-621
3. Barsukov IL, Prescot A, Bate N, Patel B, Floyd DN, Bhanji N, Bagshaw CR, Letinic K, Di Paolo G, De Camilli P, Roberts GC, Critchley DR (2003) Phosphatidylinositol phosphate kinase type 1gamma and beta1-integrin cytoplasmic domain bind to the same region in the talin FERM domain. J Biol Chem 278: 31202-31209
4. Baxter NJ, Hosszu LL, Waltho JP, Williamson MP (1998) Characterisation of low free-energy excited states of folded proteins. J Mol Biol 284: 1625-1639
5. Bouaouina M, Lad Y, Calderwood DA (2008) The N-terminal domains of talin cooperate with the phosphotyrosine bindinglike domain to activate beta1 and beta3 integrins. J Biol Chem 283: 6118-6125
6. Bretscher A, Edwards K, Fehon RG (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599
7. Brown PJ, Juliano RL (1985) Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science 228: 1448-1451
8. Calderwood DA (2004a) Integrin activation. J Cell Sci 117: 657-666
9. Calderwood DA (2004b) Talin controls integrin activation. Biochem Soc Trans 32: 434-437
10. Calderwood DA, Tai V, Di Paolo G, De Camilli P, Ginsberg MH (2004) Competition for talin results in trans-dominant inhibition of integrin activation. J Biol Chem 279: 28889-28895
11. Calderwood DA, Yan B, de Pereda JM, Alvarez BG, Fujioka Y, Liddington RC, Ginsberg MH (2002) The phosphotyrosine binding-like domain of talin activates integrins. J Biol Chem 277: 21749-21758
12. Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH (1999) The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274: 28071-28074
13. Ceccarelli DF, Song HK, Poy F, Schaller MD, Eck MJ (2006) Crystal structure of the FERM domain of focal adhesion kinase. J Biol Chem 281: 252-259
14. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302
15. Critchley DR (2009) Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu Rev Biophys 38: 235-254
16. Critchley DR, Gingras AR (2008) Talin at a glance. J Cell Sci 121: 1345-1347
17. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, Voronov S, Chang S, Guo J, Wenk MR, De Camilli P (2002) Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 420: 85-89
18. Diaz-Gonzalez F, Forsyth J, Steiner B, Ginsberg MH (1996) Trans-dominant inhibition of integrin function. Mol Biol Cell 7: 1939-1951
19. Garcia-Alvarez B, de Pereda JM, Calderwood DA, Ulmer TS, Critchley D, Campbell ID, Ginsberg MH, Liddington RC (2003 Structural determinants of integrin recognition by talin. Mol Cell 11: 49-58
20. Gingras AR, Bate N, Goult BT, Hazelwood L, Canestrelli I, Grossmann JG, Liu H, Putz NS, Roberts GC, Volkmann N, Hanein D, Barsukov IL, Critchley DR (2008) The structure of the C-terminal actin-binding domain of talin. EMBO J 27: 458-469
21. Gingras AR, Ziegler WH, Bobkov AA, Joyce MG, Fasci D, Himmel M, Rothemund S, Ritter A, Grossmann JG, Patel B, Bate N, Goult BT, Emsley J, Barsukov IL, Roberts GC, Liddington RC, Ginsberg MH, Critchley DR (2009) Structural determinants of integrin binding to the talin rod. J Biol Chem 284: 8866-8876
22. Goldfinger LE, Ptak C, Jeffery ED, Shabanowitz J, Han J, Haling JR, Sherman NE, Fox JW, Hunt DF, Ginsberg MH (2007) An experimentally derived database of candidate Ras-interacting proteins. J Proteome Res 6: 1806-1811
23. Goult BT, Bouaouina M, Harburger DS, Bate N, Patel B, Anthis NJ, Campbell ID, Calderwood DA, Barsukov IL, Roberts GC, Critchley DR (2009) The structure of the N-terminus of kindlin-1: a domain important for alphaIIbbeta3 integrin activation. J Mol Biol 394: 944-956
24. Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T (2000) Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J 19: 4449-4462
25. Han J, Lim CJ, Watanabe N, Soriani A, Ratnikov B, Calderwood DA, Puzon-McLaughlin W, Lafuente EM, Boussiotis VA, Shattil SJ, Ginsberg MH (2006) Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr Biol 16: 1796-1806
26. Herrmann T, Guntert P, Wuthrich K (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J Biomol NMR 24: 171-189
27. Holm L, Sander C (1995) Dali: a network tool for protein structure comparison. Trends Biochem Sci 20: 478-480
28. Huang L, Hofer F, Martin GS, Kim SH (1998) Structural basis for the interaction of Ras with RalGDS. Nat Struct Biol 5: 422-426
29. Hubbard SJ, Thornton JM (1993) 'NACCESS', Computer Program, Department of Biochemistry and Molecular Biology, University College London
30. Hughes PE, Oertli B, Hansen M, Chou FL, Willumsen BM, Ginsberg MH (2002) Suppression of integrin activation by activated Ras or Raf does not correlate with bulk activation of ERK MAP kinase. Mol Biol Cell 13: 2256-2265
31. Hughes PE, Renshaw MW, Pfaff M, Forsyth J, Keivens VM, Schwartz MA, Ginsberg MH (1997) Suppression of integrin activation: a novel function of a Ras/Raf-initiated MAP kinase pathway. Cell 88: 521-530
32. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 11 0: 673-687
33. Kiel C, Wohlgemuth S, Rousseau F, Schymkowitz J, Ferkinghoff-Borg J, Wittinghofer F, Serrano L (2005) Recognizing and defining true Ras binding domains II: in silico prediction based on homology modelling and energy calculations. J Mol Biol 348: 759-775
34. Konarev PV, Petoukhov MV, Volkov VV, Svergun DI (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J Appl Cryst 39: 277-286
35. Lad Y, Harburger DS, Calderwood DA (2007) Integrin cytoskeletal interactions. Methods Enzymol 426: 69-84
36. Larjava H, Plow EF, Wu C (2008) Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep 9: 1203-1208
37. Lau TL, Kim C, Ginsberg MH, Ulmer TS (2009) The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J 28: 1351-1361
38. Lee HS, Lim CJ, Puzon-McLaughlin W, Shattil SJ, Ginsberg MH (2009) RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J Biol Chem 284: 5119-5127
39. Legate KR, Montanez E, Kudlacek O, Fassler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7: 20-31
40. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA (2002) Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93
41. Linge JP, O'Donoghue SI, Nilges M (2001) Automated assignment of ambiguous nuclear overhauser effects with ARIA. Methods Enzymol 339: 71-90
42. Luo BH, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25: 619-647
43. Moes M, Rodius S, Coleman SJ, Monkley SJ, Goormaghtigh E, Tremuth L, Kox C, van der Holst PP, Critchley DR, Kieffer N (2007) The integrin binding site 2 (IBS2) in the talin rod domain is essential for linking integrin beta subunits to the cytoskeleton. J Biol Chem 282: 17280-17288
44. Moser M, Legate KR, Zent R, Fassler R (2009) The tail of integrins, talin, and kindlins. Science 324: 895-899
45. Narasimhan J, Wang M, Fu Z, Klein JM, Haas AL, Kim JJ (2005) Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J Biol Chem 280: 27356-27365
46. O'Toole TE, Katagiri Y, Faull RJ, Peter K, Tamura R, Quaranta V, Loftus JC, Shattil SJ, Ginsberg MH (1994) Integrin cytoplasmic domains mediate inside-out signal transduction. J Cell Biol 124: 1047-1059
47. O'Toole TE, Ylanne J, Culley BM (1995) Regulation of integrin affinity states through an NPXY motif in the beta subunit cyto-plasmic domain. J Biol Chem 270: 8553-8558
48. Petrich BG, Marchese P, Ruggeri ZM, Spiess S, Weichert RA, Ye F, Tiedt R, Skoda RC, Monkley SJ, Critchley DR, Ginsberg MH (2007) Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J Exp Med 204: 3103-3111
49. Pfaff M, Liu S, Erle DJ, Ginsberg MH (1998) Integrin beta cytoplas-mic domains differentially bind to cytoskeletal proteins. J Biol Chem 273: 6104-6109
50. Plow EF, Qin J, Byzova T (2009) Kindling the flame of integrin activation and function with kindlins. Curr Opin Hematol 16: 323-328
51. Ramage R, Green J, Muir TW, Ogunjobi OM, Love S, Shaw K (1994) Synthetic, structural and biological studies of the ubiquitin system: the total chemical synthesis of ubiquitin. Biochem J 299 (Pt 1): 151-158
52. Ratnikov B, Ptak C, Han J, Shabanowitz J, Hunt DF, Ginsberg MH (2005) Talin phosphorylation sites mapped by mass spectrometry. J Cell Sci 118: 4921-4923
53. Roberts GC, Critchley DR (2009) Structural and biophysical properties of the integrin-associated cytoskeletal protein talin. Biophys Rev 1: 61-69
54. Saltel F, Mortier E, Hytonen VP, Jacquier MC, Zimmermann P, Vogel V, Liu W, Wehrle-Haller B (2009) New PI(4,5)P2-and membrane proximal integrin-binding motifs in the talin head control beta3-integrin clustering. J Cell Biol 187: 715-731
55. Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95: 5857-5864
56. Shoemaker BA, Portman JJ, Wolynes PG (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci USA 97: 8868-8873
57. Svergun DI, Petoukhov MV, Koch MH (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80: 2946-2953
58. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA (2003) Talin binding to integrin beta tails: a final common step in integrin activation. Science 302: 103-106
59. Tremuth L, Kreis S, Melchior C, Hoebeke J, Ronde P, Plancon S, Takeda K, Kieffer N (2004) A fluorescence cell biology approach to map the second integrin-binding site of talin to a 130-amino acid sequence within the rod domain. J Biol Chem 279: 22258-22266
60. Wegener KL, Partridge AW, Han J, Pickford AR, Liddington RC, Ginsberg MH, Campbell ID (2007) Structural basis of integrin activation by talin. Cell 128: 171-182
61. Xing B, Jedsadayanmata A, Lam SC (2001) Localization of an integrin binding site to the C terminus of talin. J Biol Chem 276: 44373-44378
62. Zhong L, Johnson Jr WC (1992) Environment affects amino acid preference for secondary structure. Proc Natl Acad Sci USA 89: 4462-4465