Resolving two-dimensional kinetics of the integrin, αIIβ3- fibrinogen interactions using binding-unbinding correlation spectroscopy

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35275-35285

  Litvinov, Rustem I ^a   Mekler, Andrey ^a   Shuman, Henry ^a   Bennett, Joel S ^a   Barsegov, Valeri ^b   Weisel, John W ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b University of Massachusetts Lowell   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY STATE; BINDING MODES; BOND LIFETIME; CONFORMATIONAL TRANSITIONS; CORRELATION SPECTROSCOPY; DISSOCIATION CONSTANT; FIBRINOGEN COMPLEXES; FORCE CLAMP; HIGH AFFINITY; INTEGRIN ACTIVATION; INTEGRINS; INTERACTION TIME; KINETIC RATES; LIGAND BINDING ACTIVITY; LIGAND-RECEPTOR PAIR; OPTICAL TRAP; PLATELET ADHESION; QUANTITATIVE ESTIMATES; SINGLE MOLECULE LEVEL; THEORETICAL APPROACH; TIME-DEPENDENT; TWO-STATE;

BINDING ENERGY; CHEMICAL ACTIVATION; DISSOCIATION; KINETICS; LIGANDS; MANGANESE; MANGANESE COMPOUNDS; MOLECULES; TWO DIMENSIONAL;

CONFORMATIONS;

BINDING PROTEIN; FIBRINOGEN; INTEGRIN; VERY LATE ACTIVATION ANTIGEN 1;

ARTICLE; BINDING AFFINITY; CELL ADHESION; DISSOCIATION CONSTANT; LIGAND BINDING; LIPID BILAYER; METHODOLOGY; OPTICAL TWEEZERS; PIEZOELECTRICITY; PRIORITY JOURNAL; PROBABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; SPECTROSCOPY; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION;

BLOOD PLATELETS; FIBRINOGEN; HEMOSTASIS; HUMANS; KINETICS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MULTIPROTEIN COMPLEXES; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; THROMBOSIS;

EID: 84867411479     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.404848     Document Type: Article

References (46)

1. Hynes, R. O. (2009) The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219
2. Weber, G. F., Bjerke, M. A., and DeSimone, D. W. (2011) Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 124, 1183-1193
3. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
4. Hynes, R. O. (2007) Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5, Suppl. 1, 32-40
5. Bergmeier, W., and Hynes, R. O. (2012) Extracellular matrix proteins in hemostasis and thrombosis. Cold Spring Harb. Perspect. Biol. 4, a005132
6. Frojmovic, M., Wong, T., and van de Ven, T. (1991) Dynamic measurements of the platelet membrane glycoprotein IIb-IIIa receptor for fibrinogen by flow cytometry. I. Methodology, theory and results for two distinct activators. Biophys. J. 59, 815-827
7. Kuroki, K., and Maenaka, K. (2011) Analysis of receptor-ligand interactions by surface plasmon resonance. Methods Mol. Biol. 748, 83-106
8. Rico, F., Chu, C., and Moy, V. T. (2011) Force-clamp measurements of receptor-ligand interactions. Methods Mol. Biol. 736, 331-353
9. Chesla, S. E., Selvaraj, P., and Zhu, C. (1998) Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75, 1553-1572 (Pubitemid 28397625)
10. Kinoshita, K., Leung, A., Simon, S., and Evans, E. (2010) Long-lived, highstrength states of ICAM-1 bonds to β2 integrin, II: lifetimes of LFA-1 bonds under force in leukocyte signaling. Biophys. J. 98, 1467-1475
11. Danilowicz, C., Greenfield, D., and Prentiss, M. (2005) Dissociation of ligand-receptor complexes using magnetic tweezers. Anal. Chem. 77, 3023-3028 (Pubitemid 40695456)
12. 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 (Pubitemid 34568707)
13. 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. 4, 84-92
14. Bell, G. I. (1978) Models for the specific adhesion of cells to cells. Science 200, 618-627
15. Mukamel, S. (1995) Principles of Nonlinear Optical Spectroscopy, Oxford University Press, New York
16. Barsegov, V., and Thirumalai, D. (2005) Probing protein-protein interactions by dynamic force correlation spectroscopy. Phys. Rev. Lett. 95, 168302
17. Barsegov, V., Klimov, D. K., and Thirumalai, D. (2006) Mapping the energy landscape of biomolecules using single molecule force correlation spectroscopy: theory and applications. Biophys. J. 90, 3827-3841 (Pubitemid 43846102)
18. Bennett, J. S. (2005) Structure and function of the platelet integrin αIIbβ3. J. Clin. Investig. 115, 3363-3369
19. Bennett, J. S., Berger, B. W., and Billings, P. C. (2009) The structure and function of platelet integrins. J. Thromb. Haemost. 7, Suppl. 1, 200-205
20. 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 (Pubitemid 41401070)
21. 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
22. Agnihotri, A., Soman, P., and Siedlecki, C. A. (2009) AFM measurements of interactions between the platelet integrin receptor GPIIbIIIa and fibrinogen. Colloids Surf. B Biointerfaces 71, 138-147
23. Litvinov, R. I., Nagaswami, C., Vilaire, G., Shuman, H., Bennett, J. S., and Weisel, J. W. (2004) Functional and structural correlations of individual αIIbβ3 molecules. Blood 104, 3979-3985 (Pubitemid 39620147)
24. Barsegov, V., and Thirumalai, D. (2005) Dynamics of unbinding of cell adhesion molecules: transition from catch to slip bonds. Proc. Natl. Acad. Sci. U.S.A. 102, 1835-1839 (Pubitemid 40261972)
25. Barsegov, V., and Thirumalai, D. (2006) Dynamic competition between catch and slip bonds in selectins bound to ligands. J. Phys. Chem. B 110, 26403-26412 (Pubitemid 46137759)
26. Zhu, C., Long, M., Chesla, S. E., and Bongrand, P. (2002) Measuring receptor/ ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Eng. 30, 305-314 (Pubitemid 34690555)
27. Coller, B. S. (1985) A new murine monoclonal antibody reports an activa-tion- dependent change in the conformation and/or microenvironment of the platelet glycoprotein IIb/IIIa complex. J. Clin. Investig. 76, 101-108
28. Eng, E. T., Smagghe, B. J., Walz, T., and Springer, T. A. (2011) Intact αIIbβ3 integrin is extended after activation as measured by solution x-ray scattering and electron microscopy. J. Biol. Chem. 286, 35218-35226
29. Bustanji, Y., Arciola, C. R., Conti, M., Mandello, E., Montanaro, L., and Samorí, B. (2003) Dynamics of the interaction between a fibronectin molecule and a living bacterium under mechanical force. Proc. Natl. Acad. Sci. U.S.A. 100, 13292-13297 (Pubitemid 37444735)
30. Zhang, F., Marcus, W. D., Goyal, N. H., Selvaraj, P., Springer, T. A., and Zhu, C. (2005) Two-dimensional kinetics regulation of αLβ2-ICAM-1 interaction by conformational changes of the αL-inserted domain. J. Biol. Chem. 280, 42207-42218 (Pubitemid 43023191)
31. Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D., and Zhu, C. (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464, 932-936
32. Edwards, L. J., Zarnitsyna, V. I., Hood, J. D., Evavold, B. D., and Zhu, C. (2012) Insights into T cell recognition of antigen: significance of twodimensional kinetic parameters. Front. Immunol. 3, 86
33. Evans, E., Kinoshita, K., Simon, S., and Leung, A. (2010) Long-lived, highstrength states of ICAM-1 bonds to β2 integrin, I: lifetimes of bonds to recombinant αLβ2 under force. Biophys. J. 98, 1458-1466
34. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796
35. Csermely, P., Palotai, R., and Nussinov, R. (2010) Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem. Sci. 35, 539-546
36. Marshall, B. T., Long, M., Piper, J. W., Yago, T., McEver, R. P., and Zhu, C. (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423, 190-193 (Pubitemid 36569544)
37. Zhu, C., Lou, J., and McEver, R. P. (2005) Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42, 443-462 (Pubitemid 43323379)
38. Huang, J., Meyer, C., and Zhu, C. (2012) T cell antigen recognition at the cell membrane. Mol. Immunol. 52, 155-164
39. Long, M., Lü, S., and Sun, G. (2006) Kinetics of receptor-ligand interactions in immune responses. Cell. Mol. Immunol. 3, 79-86
40. Hantgan, R. R., Stahle, M. C., Connor, J. H., Horita, D. A., Rocco, M., McLane, M. A., Yakovlev, S., and Medved, L. (2006) Integrin αIIbβ3: ligand interactions are linked to binding-site remodeling. Protein Sci. 15, 1893-1906 (Pubitemid 44141507)
41. Chen, W., Lou, J., and Zhu, C. (2010) Forcing switch from short- to inter-mediate- and long-lived states of the αA domain generates LFA-1/ ICAM-1 catch bonds. J. Biol. Chem. 285, 35967-35978
42. 3. PLoS Comput. Biol. 7, e1001086
43. Xiang, X., Lee, C. Y., Li, T., Chen, W., Lou, J., and Zhu, C. (2011) Structural basis and kinetics of force-induced conformational changes of an αA do-main- containing integrin. PLoS One 6, e27946
44. Wyman, J., Jr. (1964) Linked functions and reciprocal effects in hemoglobin: a second look. Adv. Protein Chem. 19, 223-286
45. Di Cera, E., Gill, S. J., and Wyman, J. (1988) Canonical formulation of linkage thermodynamics. Proc. Natl. Acad. Sci. U.S.A. 85, 5077-5081
46. Di Cera, E. (1990) Thermodynamics of local linkage effects. Contracted partition functions and the analysis of site-specific energetics. Biophys. Chem. 37, 147-164