Talin activates integrins by altering the topology of the β transmembrane domain

Journal of Cell Biology

Volumn 197, Issue 5, 2012, Pages 605-611

  Kim, Chungho ^a   Ye, Feng ^a   Hu, Xiaohui ^a   Ginsberg, Mark H ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; TALIN;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; MOTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS;

ANIMALS; CHO CELLS; CRICETINAE; HEK293 CELLS; HUMANS; INTEGRIN BETA CHAINS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TALIN;

EID: 84862598504     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201112141     Document Type: Article

References (35)

1. Anthis, N.J., K.L. Wegener, F. Ye, C. Kim, B.T. Goult, E.D. Lowe, I. Vakonakis, N. Bate, D.R. Critchley, M.H. Ginsberg, and I.D. Campbell. 2009. The structure of an integrin/talin complex reveals the basis of insideout signal transduction. EMBO J. 28:3623-3632. http://dx.doi.org/10.1038/emboj.2009.287
2. Cordes, F.S., J.N. Bright, and M.S. Sansom. 2002. Proline-induced distortions of transmembrane helices. J. Mol. Biol. 323:951-960. http://dx.doi.org/10.1016/S0022-2836(02)01006-9
3. Denisov, I.G., Y.V. Grinkova, A.A. Lazarides, and S.G. Sligar. 2004. Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J. Am. Chem. Soc. 126:3477-3487. http://dx.doi.org/10.1021/ja0393574
4. Elliott, P.R., B.T. Goult, P.M. Kopp, N. Bate, J.G. Grossmann, G.C. Roberts, D.R. Critchley, and I.L. Barsukov. 2010. The structure of the talin head reveals a novel extended conformation of the FERM domain. Structure. 18:1289-1299. http://dx.doi.org/10.1016/j.str.2010.07.011
5. García-Guerra, R., J.A. García-Domínguez, and J. González-Rodríguez. 1996. A new look at the lipid composition of the plasma membrane of human blood platelets relative to the GPIIb/IIIa (integrin cxIIβ3) content. Platelets. 7:195-205. http://dx.doi.org/10.3109/09537109609023579
6. Ginsberg, M.H., A. Partridge, and S.J. Shattil. 2005. Integrin regulation. Curr. Opin. Cell Biol. 17:509-516. http://dx.doi.org/10.1016/j.ceb.2005.08.010
7. Han, J., C.J. Lim, N. Watanabe, A. Soriani, B. Ratnikov, D.A. Calderwood, W. Puzon-McLaughlin, E.M. Lafuente, V.A. Boussiotis, S.J. Shattil, and M.H. Ginsberg. 2006. Reconstructing and deconstructing agonistinduced activation of integrin alphaIIbbeta3. Curr. Biol. 16:1796-1806. http://dx.doi.org/10.1016/j.cub.2006.08.035
8. Hynes, R.O. 2002. Integrins: Bidirectional, allosteric signaling machines. Cell. 110: 673-687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6
9. Kalli, A.C., K.L. Wegener, B.T. Goult, N.J. Anthis, I.D. Campbell, and M.S. Sansom. 2010. The structure of the talin/integrin complex at a lipid bilayer: An NMR and MD simulation study. Structure. 18:1280-1288. http://dx.doi.org/10.1016/j.str.2010.07.012
10. Kalli, A.C., I.D. Campbell, and M.S. Sansom. 2011. Multiscale simulations suggest a mechanism for integrin inside-out activation. Proc. Natl. Acad. Sci. USA. 108:11890-11895. http://dx.doi.org/10.1073/pnas.1104505108
11. Kim, C., T.L. Lau, T.S. Ulmer, and M.H. Ginsberg. 2009. Interactions of platelet integrin alphaIIb and beta3 transmembrane domains in mammalian cell membranes and their role in integrin activation. Blood. 113:4747-4753. http://dx.doi.org/10.1182/blood-2008-10-186551
12. Kim, C., F. Ye, and M.H. Ginsberg. 2011a. Regulation of integrin activation. Annu. Rev. Cell Dev. Biol. 27:321-345. http://dx.doi.org/10.1146/annurev-cellbio-100109-104104
13. Kim, C., T. Schmidt, E.G. Cho, F. Ye, T.S. Ulmer, and M.H. Ginsberg. 2011b. Basic amino-acid side chains regulate transmembrane integrin signalling. Nature. 481:209-213. http://dx.doi.org/10.1038/nature10697
14. Kosower, N.S., E.M. Kosower, G.L. Newton, and H.M. Ranney. 1979. Bimane fluorescent labels: Labeling of normal human red cells under physiological conditions. Proc. Natl. Acad. Sci. USA. 76:3382-3386. http://dx.doi.org/10.1073/pnas.76.7.3382
15. Lau, T.L., A.W. Partridge, M.H. Ginsberg, and T.S. Ulmer. 2008. Structure of the integrin beta3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry. 47:4008-4016. http://dx.doi.org/10.1021/bi800107a
16. Lau, T.L., C. Kim, M.H. Ginsberg, and T.S. Ulmer. 2009. The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J. 28:1351-1361. http://dx.doi.org/10.1038/emboj.2009.63
17. Li, R., C.R. Babu, K. Valentine, J.D. Lear, A.J. Wand, J.S. Bennett, and W.F. DeGrado. 2002. Characterization of the monomeric form of the transmembrane and cytoplasmic domains of the integrin beta 3 subunit by NMR spectroscopy. Biochemistry. 41:15618-15624. http://dx.doi.org/10.1021/bi026822l
18. Li, W., D.G. Metcalf, R. Gorelik, R. Li, N. Mitra, V. Nanda, P.B. Law, J.D. Lear, W.F. Degrado, and J.S. Bennett. 2005. A push-pull mechanism for regulating integrin function. Proc. Natl. Acad. Sci. USA. 102:1424-1429. http://dx.doi.org/10.1073/pnas.0409334102
19. Luo, B.H., T.A. Springer, and J. Takagi. 2004. A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol. 2:e153. http://dx.doi.org/10.1371/journal.pbio.0020153
20. Luo, B.H., C.V. Carman, J. Takagi, and T.A. Springer. 2005. Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc. Natl. Acad. Sci. USA. 102:3679-3684. http://dx.doi.org/10.1073/pnas.0409440102
21. Mayer, M.L. 2006. Glutamate receptors at atomic resolution. Nature. 440:456-462. http://dx.doi.org/10.1038/nature04709
22. Partridge, A.W., S. Liu, S. Kim, J.U. Bowie, and M.H. Ginsberg. 2005. Transmembrane domain helix packing stabilizes integrin alphaIIbbeta3 in the low affinity state. J. Biol. Chem. 280:7294-7300. http://dx.doi.org/10.1074/jbc.M412701200
23. Rosenbaum, D.M., S.G. Rasmussen, and B.K. Kobilka. 2009. The structure and function of G-protein-coupled receptors. Nature. 459:356-363. http://dx.doi.org/10.1038/nature08144
24. Sansom, M.S., and H. Weinstein. 2000. Hinges, swivels and switches: The role of prolines in signalling via transmembrane alpha-helices. Trends Pharmacol. Sci. 21:445-451. http://dx.doi.org/10.1016/S0165-6147(00)01553-4
25. Senes, A., D.E. Engel, and W.F. DeGrado. 2004. Folding of helical membrane proteins: The role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14:465-479. http://dx.doi.org/10.1016/j.sbi.2004.07.007
26. Shattil, S.J., J.A. Hoxie, M. Cunningham, and L.F. Brass. 1985. Changes in the platelet membrane glycoprotein IIb, IIIa complex during platelet activation. J. Biol. Chem. 260:11107-11114.
27. Shattil, S.J., C. Kim, and M.H. Ginsberg. 2010. The final steps of integrin activation: The end game. Nat. Rev. Mol. Cell Biol. 11:288-300. http://dx.doi.org/10.1038/nrm2871
28. Subczynski, W.K., R.N. Lewis, R.N. McElhaney, R.S. Hodges, J.S. Hyde, and A. Kusumi. 1998. Molecular organization and dynamics of 1-palmitoyl-2-oleoylphosphatidylcholine bilayers containing a transmembrane alpha-helical peptide. Biochemistry. 37:3156-3164. http://dx.doi.org/10.1021/bi972148+
29. Tadokoro, S., S.J. Shattil, K. Eto, V. Tai, R.C. Liddington, J.M. de Pereda, M.H. Ginsberg, and D.A. Calderwood. 2003. Talin binding to integrin beta tails: A final common step in integrin activation. Science. 302:103-106. http://dx.doi.org/10.1126/science.1086652
30. von Heijne, G., and D. Rees. 2008. Membranes: Reading between the lines. Curr. Opin. Struct. Biol. 18:403-405. http://dx.doi.org/10.1016/j.sbi.2008.06.003
31. Wegener, K.L., A.W. Partridge, J. Han, A.R. Pickford, R.C. Liddington, M.H. Ginsberg, and I.D. Campbell. 2007. Structural basis of integrin activation by talin. Cell. 128:171-182. http://dx.doi.org/10.1016/j.cell.2006.10.048
32. Williams, M.J., P.E. Hughes, T.E. O'Toole, and M.H. Ginsberg. 1994. The inner world of cell adhesion: Integrin cytoplasmic domains. Trends Cell Biol. 4:109-112. http://dx.doi.org/10.1016/0962-8924(94)90059-0
33. Yao, X., C. Parnot, X. Deupi, V.R. Ratnala, G. Swaminath, D. Farrens, and B. Kobilka. 2006. Coupling ligand structure to specific conformational switches in the beta2-adrenoceptor. Nat. Chem. Biol. 2:417-422. http://dx.doi.org/10.1038/nchembio801
34. Ye, F., G. Hu, D. Taylor, B. Ratnikov, A.A. Bobkov, M.A. McLean, S.G. Sligar, K.A. Taylor, and M.H. Ginsberg. 2010. Recreation of the terminal events in physiological integrin activation. J. Cell Biol. 188:157-173. http://dx.doi.org/10.1083/jcb.200908045
35. Yin, H., J.S. Slusky, B.W. Berger, R.S. Walters, G. Vilaire, R.I. Litvinov, J.D. Lear, G.A. Caputo, J.S. Bennett, and W.F. DeGrado. 2007. Computational design of peptides that target transmembrane helices. Science. 315:1817-1822. http://dx.doi.org/10.1126/science.1136782