Thrombosis and hemostasis: Three-dimensional reconstruction of intact human integrin αiIbβ3: New implications for activation-dependent ligand binding

Blood

Volumn 122, Issue 26, 2013, Pages 4165-4171

  Choi, Won Seok ^a,b   Rice, William J ^c   Stokes, David L ^c,d   Coller, Barry S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Osong Medical Innovation Foundation   (South Korea)

^c NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAIIBBETA3 INTEGRIN; BETA3 INTEGRIN EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR; INTEGRIN; MONOCLONAL ANTIBODY; NANODISC; UNCLASSIFIED DRUG; FIBRINOGEN RECEPTOR; LIGAND; NANOMATERIAL; LIPID BILAYER; PROTEIN BINDING;

ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; LIGAND BINDING; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN PURIFICATION; THREE DIMENSIONAL IMAGING; VALIDATION PROCESS; CHEMICAL MODEL; CHEMISTRY; ELECTRON MICROSCOPY; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; HUMANS; IMAGING, THREE-DIMENSIONAL; LIGANDS; LIPID BILAYERS; MICROSCOPY, ELECTRON; MODELS, CHEMICAL; NANOSTRUCTURES; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84891285054     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-04-499194     Document Type: Article

References (37)

1. Campbell ID, Humphries MJ. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol. 2011;3(3).
2. Cox D, Brennan M, Moran N. Integrins as therapeutic targets: lessons and opportunities. Nat Rev Drug Discov. 2010;9(10):804-820.
3. Coller BS. Historical perspective and future directions in platelet research. J Thromb Haemost. 2011;9(suppl 1):374-395.
4. Xiong JP, Stehle T, Diefenbach B, et al. Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science. 2001;294(5541):339-345. (Pubitemid 32963395)
5. 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(6):849-861.
6. 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(5):599-611. (Pubitemid 35247840)
7. Adair BD, Xiong JP, Maddock C, Goodman SL, Arnaout MA, Yeager M. Three-dimensional EM structure of the ectodomain of integrin alphaVbeta3 in a complex with fibronectin. J Cell Biol. 2005;168(7):1109-1118.
8. Adair BD, Yeager M. Three-dimensional model of the human platelet integrin alpha IIbbeta 3 based on electron cryomicroscopy and x-ray crystallography. Proc Natl Acad Sci USA. 2002; 99(22):14059-14064. (Pubitemid 35257624)
9. Nogales A, García C, Pérez J, Callow P, Ezquerra TA, Gonźalez-Rodríguez J. Three-dimensional model of human platelet integrin alphaIIb beta3 in solution obtained by small angle neutron scattering. J Biol Chem. 2010;285(2):1023-1031.
10. Eng ET, Smagghe BJ, Walz T, Springer TA. Intact alphaIIbbeta3 integrin is extended after activation as measured by solution x-ray scattering and electron microscopy. J Biol Chem. 2011;286(40): 35218-35226.
11. Ye F, Hu G, Taylor D, et al. Recreation of the terminal events in physiological integrin activation. J Cell Biol. 2010;188(1):157-173.
12. Ritchie TK, Grinkova YV, Bayburt TH, et al. Chapter 11-reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 2009;464:211-231.
13. Shattil SJ, Hoxie JA, Cunningham M, Brass LF. Changes in the platelet membrane glycoprotein IIb.IIIa complex during platelet activation. J Biol Chem. 1985;260(20):11107-11114. (Pubitemid 16253272)
14. Roseman AM. Docking structures of domains into maps from cryo-electron microscopy using local correlation. Acta Crystallogr D Biol Crystallogr. 2000;56(Pt 10):1332-1340.
15. Volkmann N, Hanein D. Docking of atomic models into reconstructions from electron microscopy. Methods Enzymol. 2003;374:204-225. (Pubitemid 37547910)
16. Lasker K, Topf M, Sali A, Wolfson HJ. Inferential optimization for simultaneous fitting of multiple components into a CryoEM map of their assembly. J Mol Biol. 2009;388(1):180-194.
17. Xiao T, Takagi J, Coller BS, Wang JH, Springer TA. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature. 2004;432(7013):59-67. (Pubitemid 39490825)
18. Coller BS, Peerschke EI, Scudder LE, Sullivan CA. A murine monoclonal antibody that completely blocks the binding of fibrinogen to platelets produces a thrombasthenic-like state in normal platelets and binds to glycoproteins IIb and/or IIIa. J Clin Invest. 1983;72(1): 325-338. (Pubitemid 13025874)
19. Artoni A, Li J, Mitchell B, et al. Integrin beta3 regions controlling binding of murine mAb 7E3: implications for the mechanism of integrin alphaIIbbeta3 activation. Proc Natl Acad Sci USA. 2004;101(36):13114-13120. (Pubitemid 39209628)
20. Kutok JL, Coller BS. Partial inhibition of platelet aggregation and fibrinogen binding by a murine monoclonal antibody to GPIIIa: requirement for antibody bivalency. Thromb Haemost. 1994; 72(6):964-972.
21. Valle M, Gruss C, Halmer L, Carazo JM, Donate LE. Large T-antigen double hexamers imaged at the simian virus 40 origin of replication. Mol Cell Biol. 2000;20(1):34-41. (Pubitemid 30002545)
22. Wilkens S, Zhou J, Nakayama R, Dunn SD, Capaldi RA. Localization of the delta subunit in the Escherichia coli F(1)F(0)-ATPsynthase by immuno electron microscopy: the delta subunit binds on top of the F(1). J Mol Biol. 2000;295(3): 387-391.
23. Luo BH, Strokovich K, Walz T, Springer TA, Takagi J. Allosteric beta1 integrin antibodies that stabilize the low affinity state by preventing the swing-out of the hybrid domain. J Biol Chem. 2004;279(26):27466-27471. (Pubitemid 38812586)
24. Nishida N, Xie C, Shimaoka M, Cheng Y, Walz T, Springer TA. Activation of leukocyte beta2 integrins by conversion from bent to extended conformations. Immunity. 2006;25(4):583-594. (Pubitemid 44529036)
25. Taylor DW, Kelly DF, Cheng A, Taylor KA. On the freezing and identification of lipid monolayer 2-D arrays for cryoelectron microscopy. J Struct Biol. 2007;160(3):305-312. (Pubitemid 350101237)
26. Katayama H, Wang J, Tama F, et al. Threedimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc Natl Acad Sci USA. 2010;107(8):3453-3457.
27. Frank J. Three-Dimensional Electron Microscopy of Macromolecular Assemblies: Visualization of Biological Molecules in Their Native State. 2nd ed. Oxford, New York: Oxford University Press; 2006
28. Zhu J, Choi WS, McCoy JG, et al. Structureguided design of a high-affinity platelet integrin alphaIIbbeta3 receptor antagonist that disrupts Mg(2)(1) binding to the MIDAS. Sci Transl Med. 2012;4(125):125ra132.
29. Coller BS. A new murine monoclonal antibody reports an activation-dependent change in the conformation and/or microenvironment of the platelet glycoprotein IIb/IIIa complex. J Clin Invest. 1985;76(1):101-108. (Pubitemid 15240423)
30. Coller BS. Activation affects access to the platelet receptor for adhesive glycoproteins. J Cell Biol. 1986;103(2):451-456. (Pubitemid 16055041)
31. Arnaout MA, Goodman SL, Xiong JP. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol. 2007;19(5):495-507. (Pubitemid 350019555)
32. Springer TA, Dustin ML. Integrin inside-out signaling and the immunological synapse. Curr Opin Cell Biol. 2012;24(1):107-115.
33. Vinogradova O, Velyvis A, Velyviene A, et al. A structural mechanism of integrin alpha(IIb) beta(3) "inside-out" activation as regulated by its cytoplasmic face. Cell. 2002;110(5): 587-597. (Pubitemid 35247839)
34. Kim M, Carman CV, Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science. 2003;301(5640): 1720-1725. (Pubitemid 37174365)
35. Luo BH, Springer TA, Takagi J. A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol. 2004;2(6):e153.
36. Lau TL, Kim C, Ginsberg MH, Ulmer TS. The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J. 2009;28(9): 1351-1361.
37. Yang J, Ma YQ, Page RC, Misra S, Plow EF, Qin J. Structure of an integrin alphaIIb beta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc Natl Acad Sci USA. 2009;106(42): 17729-17734.