Conformational Changes in Talin on Binding to Anionic Phospholipid Membranes Facilitate Signaling by Integrin Transmembrane Helices

PLoS Computational Biology

Volumn 9, Issue 10, 2013, Pages

  Kalli, Antreas C ^a   Campbell, Iain D ^a   Sansom, Mark S P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CHEMICAL ACTIVATION; CRYSTAL STRUCTURE; GLYCOPROTEINS; LIPID BILAYERS; MOLECULAR DYNAMICS; PHOSPHOLIPIDS; PROTEINS;

AFFINITY STATE; ANIONIC PHOSPHOLIPIDS; CATIONICS; CELL SURFACE RECEPTORS; CONFORMATIONAL CHANGE; HIGH AFFINITY; INTEGRINS; PHOSPHOLIPID MEMBRANE; SUBDOMAIN; TRANSMEMBRANE HELIX;

DIMERS;

ALPHA INTEGRIN; ANION; BETA INTEGRIN; INTEGRIN; TALIN;

ANION TRANSPORT; ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ACTIVATION; MEMBRANE BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; PHOSPHOLIPID MEMBRANE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STATIC ELECTRICITY;

INTEGRINS; MOLECULAR DYNAMICS SIMULATION; PHOSPHOLIPIDS; PROTEIN STRUCTURE, TERTIARY; TALIN;

EID: 84887300788     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003316     Document Type: Article

References (72)

1. Wegener KL, Campbell ID, (2008) Transmembrane and cytoplasmic domains in integrin activation and protein-protein interactions (Review). Mol Mem Biol 25: 376-387.
2. Anthis NJ, Campbell ID, (2011) The tail of integrin activation. Trends Biochem Sci 36: 191-198.
3. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
4. Ginsberg MH, Partridge A, Shattil SJ, (2005) Integrin regulation. Curr Opin Cell Biol 17: 509-516.
5. Harburger DS, Calderwood DA, (2009) Integrin signalling at a glance. J Cell Sci 122: 159-163.
6. Bennett JS, Berger BW, Billings PC, (2009) The structure and function of platelet integrins. J Thromb Haemost 7: 200-205.
7. Gong H, Shen B, Flevaris P, Chow C, Lam SCT, et al. (2010) G protein subunit Gα13 binds to integrin αIIbβ3 and mediates integrin "outside-in" signaling. Science 327: 340-343.
8. Bouaouina M, Lad Y, Calderwood DA, (2008) The N-terminal domains of talin cooperate with the phosphotyrosine binding-like domain to activate β1 and β3 integrins. J Biol Chem 283: 6118-6125.
9. Calderwood DA, Zent R, Grant R, Rees DJG, Hynes RO, et al. (1999) The talin head domain binds to integrin β subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274: 28071-28074.
10. Wegener KL, Partridge AW, Han J, Pickford AR, Liddington RC, et al. (2007) Structural basis of integrin activation by talin. Cell 128: 171-182.
11. Kalli AC, Wegener KL, Goult BT, Anthis NJ, Campbell ID, et al. (2010) The structure of the talin/integrin complex at a lipid bilayer: an NMR and MD simulation study. Structure 18: 1280-1288.
12. Anthis NJ, Wegener KL, Ye F, Kim C, Goult BT, et al. (2009) The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 28: 3623-3632.
13. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, et al. (2003) Talin binding to integrin β tails: a final common step in integrin activation. Science 302: 103-106.
14. Petrich BG, Marchese P, Ruggeri ZM, Spiess S, Weichert RAM, et al. (2007) Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J Exp Med pp. jem.20071800.
15. Calderwood DA, (2004) Talin controls integrin activation. Biochem Soc Trans 32: 434-437.
16. Critchley DR, Gingras AR, (2008) Talin at a glance. J Cell Sci 121: 1345-1347.
17. Elliott PR, Goult BT, Kopp PM, Bate N, Grossmann JG, et al. (2010) The structure of the talin head reveals a novel extended conformation of the FERM domain. Structure 18: 1289-1299.
18. Frame MC, Patel H, Serrels B, Lietha D, Eck MJ, (2010) The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 11: 802-814.
19. Campbell ID, (2010) The talin FERM domain is not so FERM. Structure 18: 1222-1223.
20. Goult BT, Bouaouina M, Elliott PR, Bate N, Patel B, et al. (2010) Structure of a double ubiquitin-like domain in the talin head: a role in integrin activation. EMBO J 29: 1069-1080.
21. Saltel F, Mortier E, Hytonen VP, Jacquier M-C, Zimmermann P, et al. (2009) New PI(4,5)P2- and membrane proximal integrin-binding motifs in the talin head control β3-integrin clustering. J Cell Biol 187: 715-731.
22. Lau T-L, Kim C, Ginsberg MH, Ulmer TS, (2009) The structure of the integrin αIIbβ3 transmembrane complex explains integrin transmembrane signalling. EMBO J 28: 1351-1361.
23. Williams MJ, Hughes PE, O'Toole TE, Ginsberg MH, (1994) The inner world of cell adhesion: integrin cytoplasmic domains. Trends Cell Biol 4: 109-112.
24. Gottschalk KE, Adams PD, Brunger AT, Kessler H, (2002) Transmembrane signal transduction of the αIIbβ3 integrin. Protein Sci 11: 1800-1812.
25. Kim M, Carman CV, Springer TA, (2003) Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 301: 1720-1725.
26. Luo B-H, Carman CV, Springer TA, (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25: 619-647.
27. Partridge AW, Liu S, Kim S, Bowie JU, Ginsberg MH, (2005) Transmembrane domain helix packing stabilizes integrin αIIbβ3 in the low affinity state. J Biol Chem 280: 7294-7300.
28. Lu C, Takagi J, Springer TA, (2001) Association of the membrane proximal regions of the α and β subunit cytoplasmic domains constrains an integrin in the inactive state. J Biol Chem 276: 14642-14648.
29. Luo B-H, Springer TA, Takagi J, (2004) A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol 2: e153.
30. Stansfeld PJ, Sansom MSP, (2011) Molecular simulation approaches to membrane proteins. Structure 19: 1562-1572.
31. Bond PJ, Wee CL, Sansom MSP, (2008) Coarse-grained molecular dynamics simulations of the energetics of helix insertion into a lipid bilayer. Biochemistry 47: 11321-11331.
32. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, et al. (2008) The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput 4: 819-834.
33. Stansfeld PJ, Sansom MSP, (2011) From coarse grained to atomistic: a serial multiscale approach to membrane protein simulations. J Chem Theory Comput 7: 1157-1166.
34. Kalli AC, Campbell ID, Sansom MSP, (2011) Multiscale simulations suggest a mechanism for integrin inside-out activation. Proc Natl Acad Sci USA 108: 11890-11895.
35. Ayton GS, Noid WG, Voth GA, (2007) Multiscale modeling of biomolecular systems: in serial and in parallel. Curr Opin Cell Biol 17: 192-198.
36. Lumb CN, He J, Xue Y, Stansfeld PJ, Stahelin RV, et al. (2011) Biophysical and computational studies of membrane penetration by the GRP1 pleckstrin homology domain. Structure 19: 1338-1346.
37. Balali-Mood K, Bond PJ, Sansom MSP, (2009) Interaction of monotopic membrane enzymes with a lipid bilayer: a coarse-grained MD simulation Study. Biochemistry 48: 2135-2145.
38. Wee CL, Balali-Mood K, Gavaghan D, Sansom MSP, (2008) The interaction of phospholipase A2 with a phospholipid bilayer: coarse-grained molecular dynamics simulations. Biophys J 95: 1649-1657.
39. Gambin Y, Lopez-Esparza R, Reffay M, Sierecki E, Gov NS, et al. (2006) Lateral mobility of proteins in liquid membranes revisited. Proc Natl Acad Sci USA 103: 2098-2102.
40. Kalli AC, Hall BA, Campbell ID, Sansom MSP, (2011) A helix heterodimer in a lipid bilayer: prediction of the structure of an integrin transmembrane domain via multiscale simulations. Structure 19: 1477-1484.
41. Sharma S, Juffer AH, (2013) An atomistic model for assembly of transmembrane domain of T cell receptor complex. J Am Chem Soc 135: 2188-2197.
42. Arkhipov A, Shan Y, Das R, Endres NF, Eastwood MP, et al. (2013) Architecture and membrane interactions of the EGF receptor. Cell 152: 557-569.
43. Fiser A, Do RKG, Šali A, (2000) Modeling of loops in protein structures. Prot Sci 9: 1753-1773.
44. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
45. Berger BW, Kulp DW, Span LM, DeGrado JL, Billings PC, et al. (2009) Consensus motif for integrin transmembrane helix association. Proc Natl Acad Sci USA.
46. Yang J, Ma Y-Q, Page RC, Misra S, Plow EF, et al. (2009) Structure of an integrin αIIbβ3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc Natl Acad Sci USA 106: 17729-17734.
47. Li W, Metcalf DG, Gorelik R, Li R, Mitra N, et al. (2005) A push-pull mechanism for regulating integrin function. Proc Natl Acad Sci USA 102: 1424-1429.
48. Luo B-H, Carman CV, Takagi J, Springer TA, (2005) Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc Natl Acad Sci USA 102: 3679-3684.
49. Hughes PE, Diaz-Gonzalez F, Leong L, Wu C, McDonald JA, et al. (1996) Breaking the integrin hinge. J Biol Chem 271: 6571-6574.
50. Hughes PE, O'Toole TE, Ylanne J, Shattil SJ, Ginsberg MH, (1995) The conserved membrane-proximal region of an integrin cytoplasmic domain specifies ligand binding affinity. J Biol Chem 270: 12411-12417.
51. O'Toole TE, Katagiri Y, Faull RJ, Peter K, Tamura R, et al. (1994) Integrin cytoplasmic domains mediate inside-out signal transduction. J Cell Biol 124: 1047-1059.
52. O'Toole TE, Mandelman D, Forsyth J, Shattil SJ, Plow EF, et al. (1991) Modulation of the affinity of integrin αIIbβ3 (GPIIb-IIIa) by the cytoplasmic domain of αIIb. Science 254: 845-847.
53. Kim C, Ye F, Hu X, Ginsberg MH, (2012) Talin activates integrins by altering the topology of the β transmembrane domain. J Cell Biol 197: 605-611.
54. Kim C, Schmidt T, Cho E-G, Ye F, Ulmer TS, et al. (2012) Basic amino-acid side chains regulate transmembrane integrin signalling. Nature 481: 209-213.
55. Lau T-L, Partridge AW, Ginsberg MH, Ulmer TS, (2008) Structure of the integrin β3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry 47: 4008-4016.
56. Moore DT, Nygren P, Jo H, Boesze-Battaglia K, Bennett JS, et al. (2011) Affinity of talin-1 for the β3-integrin cytosolic domain is modulated by its phospholipid bilayer environment. Proc Natl Acad Sci USA.
57. Bouaouina M, Goult BT, Huet-Calderwood C, Bate N, Brahme NN, et al. (2012) A conserved lipid-binding loop in the kindlin FERM F1 domain is required for kindlin-mediated αIIbβ3 integrin coactivation. J Biol Chem 287: 6979-6990.
58. Xiong JP, Mahalingham B, Alonso JL, Borrelli LA, Rui XL, et al. (2009) Crystal structure of the complete integrin αVβ3 ectodomain plus an α/β. transmembrane fragment. J Cell Biol 186: 589-600.
59. Zhu JH, Luo BH, Xiao T, Zhang CZ, Nishida N, et al. (2008) Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Molecular Cell 32: 849-861.
60. Nygaard R, Zou Y, Dror Ron O, Mildorf Thomas J, Arlow Daniel H, et al. (2013) The dynamic process of β2-adrenergic receptor activation. Cell 152: 532-542.
61. Shan Y, Eastwood MP, Zhang X, Kim ET, Arkhipov A, et al. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149: 860-870.
62. Bond PJ, Sansom MSP, (2006) Insertion and assembly of membrane proteins via simulation. J Am Chem Soc 128: 2697-2704.
63. David Van Der S, Erik L, Berk H, Gerrit G, Alan EM, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718.
64. Hess B, Kutzner C, van der Spoel D, Lindahl E, (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4: 435-447.
65. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR, (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
66. Scott WRP, Hunenberger PH, Tironi IG, Mark AE, Billeter SR, et al. (1999) The GROMOS biomolecular simulation program package. J Phys Chem A 103: 3596-3607.
67. Parrinello M, Rahman A, (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52: 7182-7190.
68. Hess B, Bekker H, Berendsen H, Fraaije J, (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
69. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys 98: 10089-10092.
70. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38.
71. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Nat Acad Sci USA 98: 10037-10041.
72. DeLano WL (2002) The PyMOL Molecular Graphics System. http://www.pymol.org.