The platelet integrin αiIbβ3 differentially interacts with fibrin versus fibrinogen

Journal of Biological Chemistry

Volumn 291, Issue 15, 2016, Pages 7858-7867

  Litvinov, Rustem I ^a   Farrell, David H ^b   Weisel, John W ^a   Bennett, Joel S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; LASER BEAMS; PLATELETS;

BINDING ACTIVITIES; BINDING STRENGTH; COATED SURFACE; DIFFERENTIAL EFFECT; FORCE HISTOGRAMS; PLATELET AGGREGATION; PLATELET INTEGRIN; RELATIVE CONTRIBUTION;

BINDING SITES;

ARGINYLGLYCYLASPARTIC ACID; FIBRIN; FIBRINOGEN; GAMMA C DODECAPEPTIDE; INTEGRIN; INTEGRIN ALPHA2BBETA3; POLYPEPTIDE; UNCLASSIFIED DRUG; FIBRINOGEN RECEPTOR;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; LIGAND BINDING; MATERIAL COATING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; CYTOLOGY; HUMAN; METABOLISM; THROMBOCYTE; THROMBOCYTE AGGREGATION;

BLOOD PLATELETS; FIBRIN; FIBRINOGEN; HUMANS; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN INTERACTION MAPS;

EID: 84964587751     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.706861     Document Type: Article

References (43)

1. Bennett, J. S. (2001) Platelet-fibrinogen interactions. Ann. N.Y. Acad. Sci. 936, 340-354
2. Dai, A., Ye, F., Taylor, D. W., Hu, G., Ginsberg, M. H., and Taylor, K. A. (2015) The structure of a full-length membrane-embedded integrin bound to a physiological ligand. J. Biol. Chem. 290, 27168-27175
3. Collet, J. P., Montalescot, G., Lesty, C., and Weisel, J. W. (2002) A structural and dynamic investigation of the facilitating effect of glycoprotein IIb/IIIa inhibitors in dissolving platelet-rich clots. Circ. Res. 90, 428-434
4. Carr, M. E., Jr. (2003) Development of platelet contractile force as a research and clinical measure of platelet function. Cell Biochem. Biophys. 38, 55-78
5. Hantgan, R. R., and Mousa, S. A. (1998) Inhibition of platelet-mediated clot retraction by integrin antagonists. Thromb. Res. 89, 271-279
6. Hantgan, R. R. (1988) Fibrin protofibril and fibrinogen binding to ADPstimulated platelets: evidence for a common mechanism. Biochim. Biophys. Acta 968, 24-35
7. Bennett, J. S., and Vilaire, G. (1979) Exposure of platelet fibrinogen receptors by ADP and epinephrine. J. Clin. Invest. 64, 1393-1401
8. Kloczewiak, M., Timmons, S., Lukas, T. J., and Hawiger, J. (1984) Platelet receptor recognition site on human fibrinogen. Synthesis and structurefunction relationship of peptides corresponding to the carboxy-terminal segment of the γ chain. Biochemistry 23, 1767-1774
9. Kloczewiak, M., Timmons, S., and Hawiger, J. (1983) Recognition site for the platelet receptor is present on the 15-residue carboxy-terminal fragment of the γ chain of human fibrinogen and is not involved in the fibrin polymerization reaction. Thromb. Res. 29, 249-255
10. Weisel, J. W., Nagaswami, C., Vilaire, G., and Bennett, J. S. (1992) Examination of the platelet membrane glycoprotein IIb-IIIa complex and its interaction with fibrinogen and other ligands by electron microscopy. J. Biol. Chem. 267, 16637-16643
11. Farrell, D. H., Thiagarajan, P., Chung, D. W., and Davie, E. W. (1992) Role of fibrinogen α and γ chain sites in platelet aggregation. Proc. Natl. Acad. Sci. U.S.A. 89, 10729-10732
12. Springer, T. A., Zhu, J., and Xiao, T. (2008) Structural basis for distinctive recognition of fibrinogen γCpeptide by the platelet integrin αIIbβ3. J. Cell Biol. 182, 791-800
13. Martínez-Sales, V., Vila, V., Réganon, E., and Aznar, J. (1995) Unstimulated and thrombin-stimulated platelets binding to immobilized fibrinogen and fibrin on polystyrene supports. Haemostasis 25, 158-165
14. Jirousková, M., Dyr, J. E., Suttnar, J., Holada, K., and Trnková, B. (1997) Platelet adhesion to fibrinogen, fibrin monomer, and fibrin protofibrils in flowing blood: the effect of fibrinogen immobilization and fibrin formation. Thromb. Haemost. 78, 1125-1131
15. Cho, J., Degen, J. L., Coller, B. S., and Mosher, D. F. (2005) Fibrin but not adsorbed fibrinogen supports fibronectin assembly by spread platelets. Effects of the interaction of αIIbβ3 with the C terminus of the fibrinogen γ-chain. J. Biol. Chem. 280, 35490-35498
16. Cohen, I., Gerrard, J. M., and White, J. G. (1982) Ultrastructure of clots during isometric contraction. J. Cell Biol. 93, 775-787
17. Hantgan, R. R., Taylor, R. G., and Lewis, J. C. (1985) Platelets interact with fibrin only after activation. Blood 65, 1299-1311
18. Gartner, T. K., and Ogilvie, M. L. (1988) Peptides and monoclonal antibodies which bind to platelet glycoproteins IIb and/or IIIa inhibit clot retraction. Thromb. Res. 49, 43-53
19. Rooney, M. M., Parise, L. V., and Lord, S. T. (1996) Dissecting clot retraction and platelet aggregation: clot retraction does not require an intact fibrinogen γ chain C terminus. J. Biol. Chem. 271, 8553-8555
20. Holmbäck, K., Danton, M. J., Suh, T. T., Daugherty, C. C., and Degen, J. L. (1996) Impaired platelet aggregation and sustained bleeding in mice lacking the fibrinogen motif bound by integrin αIIbβ3. EMBO J. 15, 5760-5771
21. Rooney, M. M., Farrell, D. H., van Hemel, B. M., de Groot, P. G., and Lord, S. T. (1998) The contribution of the three hypothesized integrin-binding sites in fibrinogen to platelet-mediated clot retraction. Blood 92, 2374-2381
22. Hamaguchi, M., Bunce, L. A., Sporn, L. A., and Francis, C. W. (1993) Spreading of platelets on fibrin is mediated by the amino terminus of the γ chain including peptide β15-42. Blood 81, 2348-2356
23. Remijn, J. A., Ijsseldijk, M. J., and De Groot, P. G. (2003) Role of the fibrinogen α-chain sequence γ316-322 in platelet-mediated clot retraction. J. Thromb. Haemost. 1, 2245-2246
24. Remijn, J. A., Ijsseldijk, M. J., van Hemel, B. M., Galanakis, D. K., Hogan, K. A., Lounes, K. C., Lord, S. T., Sixma, J. J., and de Groot, P. G. (2002) Reduced platelet adhesion in flowing blood to fibrinogen by alterations in segment γ316-322, part of the fibrin-specific region. Br. J. Haematol. 117, 650-657
25. Podolnikova, N. P., Gorkun, O. V., Loreth, R. M., Yee, V. C., Lord, S. T., and Ugarova, T. P. (2005) A cluster of basic amino acid residues in the γ370-381 sequence of fibrinogen comprises a binding site for platelet integrin α (IIb)β3 (glycoprotein IIb/IIIa). Biochemistry 44, 16920-16930
26. Podolnikova, N. P., Yakubenko, V. P., Volkov, G. L., Plow, E. F., and Ugarova, T. P. (2003) Identification of a novel binding site for platelet integrins αIIbβ3 (GPIIbIIIa) and α5β1 in the γC-domain of fibrinogen. J. Biol. Chem. 278, 32251-32258
27. Farrell, D. H., and Thiagarajan, P. (1994) Binding of recombinant fibrinogen mutants to platelets. J. Biol. Chem. 269, 226-231
28. Litvinov, R. I., Barsegov, V., Schissler, A. J., Fisher, A. R., Bennett, J. S., Weisel, J. W., and Shuman, H. (2011) Dissociation of bimolecular αIIbβ3-fibrinogen complex under a constant tensile force. Biophys. J. 100, 165-173
29. Litvinov, R. I., Bennett, J. S., Weisel, J. W., and Shuman, H. (2005) Multistep fibrinogen binding to the integrin αIIbβ3 detected using force spectroscopy. Biophys. J. 89, 2824-2834
30. Litvinov, R. I., Mekler, A., Shuman, H., Bennett, J. S., Barsegov, V., and Weisel, J. W. (2012) Resolving two-dimensional kinetics of the integrin αIIbβ3-fibrinogen interactions using binding-unbinding correlation spectroscopy. J. Biol. Chem. 287, 35275-35285
31. Litvinov, R. I., Shuman, H., Bennett, J. S., and Weisel, J. W. (2002) Binding strength and activation state of single fibrinogen-integrin pairs on living cells. Proc. Natl. Acad. Sci. U.S.A. 99, 7426-7431
32. Zamarron, C., Ginsberg, M. H., and Plow, E. F. (1991) A receptor-induced binding site in fibrinogen elicited by its interaction with platelet membrane glycoprotein IIb-IIIa. J. Biol. Chem. 266, 16193-16199
33. Litvinov, R. I., Gorkun, O. V., Galanakis, D. K., Yakovlev, S., Medved, L., Shuman, H., and Weisel, J. W. (2007) Polymerization of fibrin: direct observation and quantification of individual B:b knob-hole interactions. Blood 109, 130-138
34. Litvinov, R. I., Gorkun, O. V., Owen, S. F., Shuman, H., and Weisel, J. W. (2005) Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Blood 106, 2944-2951
35. Uitte de Willige, S., Standeven, K. F., Philippou, H., and Ariëns, R. A. (2009) The pleiotropic role of the fibrinogen γ′ chain in hemostasis. Blood 114, 3994-4001
36. Farrell, D. H. (2004) Pathophysiologic roles of the fibrinogen γ chain. Curr. Opin. Hematol. 11, 151-155
37. Sun, J. E., Vranic, J., Composto, R. J., Streu, C., Billings, P. C., Bennett, J. S., Weisel, J. W., and Litvinov, R. I. (2012) Bimolecular integrin-ligand interactions quantified using peptide-functionalized dextran-coated microparticles. Integr. Biol. (Camb.) 4, 84-92
38. Savage, B., and Ruggeri, Z. M. (1991) Selective recognition of adhesive sites in surface-bound fibrinogen by glycoprotein IIb-IIIa on nonactivated platelets. J. Biol. Chem. 266, 11227-11233
39. Bennett, J. S., Shattil, S. J., Power, J. W., and Gartner, T. K. (1988) Interaction of fibrinogen with its platelet receptor: differential effects of a and g chain fibrinogen peptides on the glycoprotein IIb-IIIa complex. J. Biol. Chem. 263, 12948-12953
40. Falati, S., Gross, P. L., Merrill-Skoloff, G., Sim, D., Flaumenhaft, R., Celi, A., Furie, B. C., and Furie, B. (2004) In vivo models of platelet function and thrombosis: study of real-time thrombus formation. Methods Mol. Biol. 272, 187-197
41. Podolnikova, N. P., O'Toole, T. E., Haas, T. A., Lam, S. C., Fox, J. E., and Ugarova, T. P. (2009) Adhesion-induced unclasping of cytoplasmic tails of integrin αIIbβ3. Biochemistry 48, 617-629
42. Hantgan, R. R., Stahle, M. C., and Lord, S. T. (2010) Dynamic regulation of fibrinogen: integrin αIIbβ3 binding. Biochemistry 49, 9217-9225
43. Flevaris, P., Li, Z., Zhang, G., Zheng, Y., Liu, J., and Du, X. (2009) Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood 113, 893-901