Structural basis of transmembrane domain interactions in integrin signaling

Cell Adhesion and Migration

Volumn 4, Issue 2, 2010, Pages 243-248

  Ulmer, Tobias S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cell adhesion; Integrin; Membrane protein; Platelet; Transmembrane complex; Transmembrane signaling

Indexed keywords

ALPHA2 INTEGRIN; ARGININE; GLYCINE; INTEGRIN; INTEGRIN ALPHA2B BETA3; MEMBRANE PROTEIN; TALIN; UNCLASSIFIED DRUG; ALPHA INTEGRIN; BETA INTEGRIN;

ALPHA HELIX; COMPLEX FORMATION; CROSS COUPLING REACTION; HUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ANIMAL; CELL MEMBRANE; CHEMISTRY; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL MEMBRANE; HUMANS; INTEGRIN ALPHA CHAINS; INTEGRIN BETA CHAINS; INTEGRINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 77953561717     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.4.2.10592     Document Type: Review

References (55)

1. Hynes RO. Integrins: Bidirectional, allosteric signaling machines. Cell 2002; 110:673-87.
2. Askari JA, Buckley PA, Mould AP, Humphries MJ. Linking integrin conformation to function. J Cell Sci 2009; 122:165-70.
3. Harburger DS, Calderwood DA. Integrin signalling at a glance. J Cell Sci 2009; 122:159-63.
4. Ginsberg MH, Partridge A, Shattil SJ. Integrin regulation. Curr Opin Cell Biol 2005; 17:509-16.
5. Bennett JS, Berger BW, Billings PC. The structure and function of platelet integrins. J Thromb Haemost 2009; 7:200-5.
6. Hughes PE, DiazGonzalez F, Leong L, Wu CY, McDonald JA, Shattil SJ, et al. Breaking the integrin hinge - A defined structural constraint regulates integrin signaling. J Biol Chem 1996; 271:6571-4.
7. Kim M, Carman CV, Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 2003; 301:1720-5.
8. Zhu JQ, Carman CV, Kim M, Shimaoka M, Springer TA, Luo BH. Requirement of alpha and beta subunit transmembrane helix separation for integrin outside-in signaling. Blood 2007; 110:2475-83.
9. Li W, Metcalf DG, Gorelik R, Li RH, Mitra N, Nanda V, et al. A push-pull mechanism for regulating integrin function. Proc Natl Acad Sci USA 2005; 102:1424-9.
10. Partridge AW, Liu SC, Kim S, Bowie JU, Ginsberg MH. Transmembrane domain helix packing stabilizes integrin aIIbbeta3 in the low affinity state. J Biol Chem 2005; 280:7294-300.
11. Otoole TE, Katagiri Y, Faull RJ, Peter K, Tamura R, Quaranta V, et al. Integrin Cytoplasmic Domains Mediate Inside-Out Signal-Transduction. J Cell Biol 1994; 124:1047-59.
12. Lau T-L, Dua V, Ulmer TS. Structure of the integrin alphaIIb transmembrane segment. J Biol Chem 2008; 283:16162-8.
13. Lau T-L, Partridge AP, Ginsberg MH, Ulmer TS. Structure of the Integrin beta3 Transmembrane Segment in Phospholipid Bicelles and Detergent Micelles. Biochemistry 2008; 47:4008-16.
14. Luo BH, Carman CV, Takagi J, Springer TA. Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc Natl Acad Sci USA 2005; 102:3679-84.
15. Luo BH, Springer TA, Takagi J. A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol 2004; 2:776-86.
16. Lau T-L, Kim C, Ginsberg MH, Ulmer TS. The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J 2009; 28:1351-61.
17. Zhu J, Luo BH, Barth P, Schonbrun J, Baker D, Springer TA. The Structure of a Receptor with Two Associating Transmembrane Domains on the Cell Surface: Integrin alpha(IIb)beta(3). Mol Cell 2009; 34:234-49.
18. Stefansson A, Armulik A, Nilsson IM, von Heijne G, Johansson S. Determination of N- and C-terminal borders of the transmembrane domain of integrin subunits. J Biol Chem 2004; 279:21200-5.
19. Armulik A, Nilsson I, von Heijne G, Johansson S. Determination of the border between the transmembrane and cytoplasmic domains of human integrin subunits. J Biol Chem 1999; 274:37030-4.
20. Xiong JP, Mahalingham B, Alonso JL, Borrelli LA, Rui XL, Anand S, et al. Crystal structure of the complete integrin alphaVbeta3 ectodomain plus an alpha/beta. transmembrane fragment. J Cell Biol 2009; 186:589-600.
21. Anthis NJ, Wegener KL, Ye F, Kim C, Goult BT, Lowe ED, et al. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 2009; 28:3623-32.
22. Gregoriou M, Noble MEM, Watson KA, Garman EF, Krulle TM, De la Fuente C, et al. The structure of a glycogen phosphorylase glucopyranose spirohydantoin complex at 1.8 angstrom resolution and 100 K: The role of the water structure and its contribution to binding. Protein Sci 1998; 7:915-27.
23. Hunsicker-Wang LM, Pacoma RL, Chen Y, Fee JA, Stout CD. A novel cryoprotection scheme for enhancing the diffraction of crystals of recombinant cytochrome ba(3) oxidase from Thermus thermophilus. Acta Crystallogr Sect D-Biol Crystallogr 2005; 61:340-3.
24. Papiz MZ, Prince SM, Howard T, Cogdell RJ, Isaacs NW. The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 (A)overcircle resolution and 100 K: New structural features and functionally relevant motions. J Mol Biol 2003; 326:1523-38.
25. Beel AJ, Mobley CK, Kim HJ, Tian F, Hadziselimovic A, Jap B, et al. Structural studies of the transmembrane C-terminal domain of the amyloid precursor protein (APP): Does APP function as a cholesterol sensor? Biochemistry 2008; 47:9428-46.
26. Lee D, Walter KFA, Bruckner A-K, Hilty C, Becker S, Griesinger C. Bilayer in Small Bicelles Revealed by Lipid-Protein Interactions Using NMR Spectroscopy. J Am Chem Soc 2008; 130:13822-3.
27. Hoefling M, Kessler H, Gottschalk KE. The Transmembrane Structure of Integrin alphaIIbbeta3: Significance for Signal Transduction. Angew Chem-Int Edit 2009; 48:6590-3.
28. Gottschalk KE, Adams PD, Brunger AT, Kessler H. Transmembrane signal transduction of the alpha(IIb) beta(3) integrin. Protein Sci 2002; 11:1800-12.
29. Lin X, Tan SM, Law SKA, Torres J. Unambiguous prediction of human integrin transmembrane heterodimer interactions using only homologous sequences. Proteins-Structure Function And Bioinformatics 2006; 65:274-9.
30. Ulmer TS, Yaspan B, Ginsberg MH, Campbell ID. NMR analysis of structure and dynamics of the cytosolic tails of integrin alphaIIbbeta3 in aqueous solution. Biochemistry 2001; 40:7498-508.
31. Vinogradova O, Velyvis A, Velyviene A, Hu B, Haas TA, Plow EF, et al. A structural mechanism of integrin alpha(IIb)beta(3) "inside-out" activation as regulated by its cytoplasmic face. Cell 2002; 110:587-97.
32. Weljie AM, Hwang PM, Vogel HJ. Solution structures of the cytoplasmic tail complex from platelet integrin alphaIIb- and beta3-subunits. Proc Natl Acad Sci USA 2002; 99:5878-83.
33. Yang J, Ma YQ, Page RC, Misra S, Plow EF, Qin J. Structure of an integrin alphaIIbbeta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc Natl Acad Sci USA 2009; 106:17729-34.
34. GarciaGuerra R, GarciaDominguez JA, GonzalezRodriguez J. A new look at the lipid composition of the plasma membrane of human blood platelets relative to the GPIIb/IIIa (integrin alphaIIbbeta3) content. Platelets 1996; 7:195-205.
35. Kim C, Lau T-L, Ulmer TS, Ginsberg MH. Interactions of platelet integrin alphaIIb and beta3 transmembrane domains in mammalian cell membranes and their role in integrin activation. Blood 2009; 113:4747-53.
36. Metcalf DG, Kulp DW, Bennett JS, Degrado WF. Multiple approaches converge on the structure of the integrin alphaIIb/beta3 transmembrane heterodimer. J Mol Biol 2009; 392:1087-101.
37. Xiong JP, Stehle T, Diefenbach B, Zhang RG, Dunker R, Scott DL, et al. Crystal structure of the extracellular segment of integrin alphaVbeta3. Science 2001; 294:339-45.
38. Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, Springer TA. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell 2008; 32:849-61.
39. Kamata T, Handa M, Sato Y, Ikeda Y, Aiso S. Membrane-proximal alpha/beta stalk interactions differentially regulate integrin activation. J Biol Chem 2005; 280:24775-83.
40. MacKenzie KR, Prestegard JH, Engelman DM. A transmembrane helix dimer: Structure and implications. Science 1997; 276:131-3.
41. Call ME, Schnell JR, Xu CQ, Lutz RA, Chou JJ, Wucherpfennig KW. The structure of the zeta zeta transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 2006; 127:355-68.
42. Bocharov EV, Mayzel ML, Volynsky PE, Goncharuk MV, Ermolyuk YS, Schulga AA, et al. Spatial Structure and pH-dependent Conformational Diversity of Dimeric Transmembrane Domain of the Receptor Tyrosine Kinase EphA1. J Biol Chem 2008; 283:29385-95.
43. Bocharov EV, Pustovalova YE, Pavlov KV, Volynsky PE, Goncharuk MV, Ermolyuk YS, et al. Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J Biol Chem 2007; 282:16256-66.
44. Calderwood DA, Yan B, de Pereda JM, Alvarez BGYF, Liddington RC, et al. The Phosphotyrosine Bindinglike Domain of Talin Activates Integrins. J Biol Chem 2002; 277:21749.
45. Bouaouina M, Lad Y, Calderwood DA. The N-terminal domains of talin cooperate with the phosphotyrosine binding-like domain to activate beta1 and beta3 integrins. J Biol Chem 2008; 283:6118-25.
46. Imai Y, Park EJ, Peer D, Peixoto A, Cheng GY, von Andrian UH, et al. Genetic perturbation of the putative cytoplasmic membrane-proximal salt bridge aberrantly activates alpha(4) integrins. Blood 2008; 112:5007-15.
47. Ghevaert C, Salsmann A, Watkins NA, Schaffner-Reckinger E, Rankin A, Garner SF, et al. A nonsynonymous SNP in the ITGB3 gene disrupts the conserved membrane-proximal cytoplasmic salt bridge in the alpha(IIb)beta(3) integrin and cosegregates dominantly with abnormal proplatelet formation and macrothrombocytopenia. Blood 2008; 111:3407-14.
48. Takagi J, Petre BM, Walz T, Springer TA. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 2002; 110:599-611.
49. Xiong JP, Stehle T, Goodman SL, Arnaout MA. New insights into the structural basis of integrin activation. Blood 2003; 102:1155-9.
50. Ye F, Liu J, Winkler H, Taylor KA. Integrin alpha(IIb) beta(3) in a membrane environment remains the same height after Mn2+ activation when observed by cryoelectron tomography. J Mol Biol 2008; 378:976-86.
51. Vararattanavech A, Lin X, Torres J, Tan SM. Disruption of the Integrin alphaLbeta2 Transmembrane Domain Interface by beta2 Thr-686 Mutation Activates alphaLbeta2 and Promotes Micro-clustering of the alphaL Subunits. J Biol Chem 2009; 284:3239-49.
52. Vararattanavech A, Tang ML, Li HY, Wong CH, Law SKA, Torres J, et al. Permissive transmembrane helix heterodimerization is required for the expression of a functional integrin. Biochem J 2008; 410:495-502.
53. Caputo GA, Litvinov RI, Li W, Bennett JS, DeGrado WF, Yin H. Computationally designed peptide inhibitors of protein-protein interactions in membranes. Biochemistry 2008; 47:8600-6.
54. Wiener MC, White SH. Structure Of A Fluid Dioleoylphosphatidylcholine Bilayer Determined By Joint Refinement Of X-Ray And Neutron-Diffraction Data.3. Complete Structure. Biophys J 1992; 61:434-47.
55. Zhao W, Rog T, Gurtovenko AA, Vattulainen I, Karttunen M. Atomic-scale structure and electrostatics of anionic palmitoyloleoylphosphatidylglycerol lipid bilayers with Na+ counterions. Biophys J 2007; 92:1114-24.