On the mechanism of αc polymer formation in fibrin

Biochemistry

Volumn 51, Issue 12, 2012, Pages 2526-2538

  Tsurupa, Galina ^a   Pechik, Igor ^b,f   Litvinov, Rustem I ^c   Hantgan, Roy R ^d   Tjandra, Nico ^e   Weisel, John W ^c   Medved, Leonid ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^f Venenum Biodesign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; DISULFIDE BONDS; FORCE SPECTROSCOPY; MOLECULAR MECHANISM; N-TERMINALS; POLYMER FORMATION; POLYMER STRUCTURE; SELF-ASSOCIATIONS; SHEET STRUCTURE; SITE DIRECTED MUTAGENESIS; STERIC HINDRANCES; SUB-DOMAINS; SUBDOMAIN; WILD TYPES;

ASSOCIATION REACTIONS; CONFORMATIONS; COVALENT BONDS; EXPERIMENTS; OLIGOMERIZATION; OLIGOMERS; SIZE EXCLUSION CHROMATOGRAPHY;

POLYMERS;

BLOOD CLOTTING FACTOR 13A; FIBRIN; MUTANT PROTEIN; POLYMER;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHEMICAL INTERACTION; CIRCULAR DICHROISM; CONTROLLED STUDY; DNA HAIRPIN; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR MODEL; MUTATION; OLIGOMERIZATION; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN CONFORMATION; SPECTROSCOPY;

ANIMALS; CATTLE; DISULFIDES; FIBRIN; FIBRINOGEN; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

BOVINAE;

EID: 84859178020     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2017848     Document Type: Article

References (54)

1. Medved, L. V., Gorkun, O. V., Manyakov, V. F., and Belitser, V. A. (1985) The role of fibrinogen αC-domains in the fibrin assembly process FEBS Lett. 181, 109-112
2. Gorkun, O. V., Veklich, Y. I., Medved, L. V., Henschen, A. H., and Weisel, J. W. (1994) Role of the αC domains of fibrin in clot formation Biochemistry 33, 6986-6997
3. Collet, J. P., Moen, J. L., Veklich, Y. I., Gorkun, O. V., Lord, S. T., Montalescot, G., and Weisel, J. W. (2005) The αC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis Blood 106, 3824-3830
4. Smith, K. A., Adamson, P. J., Pease, R. J., Brown, J. M., Balmforth, A. J., Cordell, P. A., Ariëns, R. A., Philippou, H., and Grant, P. J. (2011) Interactions between factor XIII and the αC region of fibrinogen Blood 117, 3460-3468
5. Credo, R. B., Curtis, C. G., and Lorand, L. (1981) α-chain domain of fibrinogen controls generation of fibrinoligase (coagulation factor XIIIa). Calcium ion regulatory aspects Biochemistry 20, 3770-3778
6. Tsurupa, G. and Medved, L. (2001) Identification and characterization of novel tPA- and plasminogen- binding sites within fibrin(ogen) αC-domains Biochemistry 40, 801-808
7. Medved, L. and Nieuwenhuizen, W. (2003) Molecular mechanisms of initiation of fibrinolysis by fibrin Thromb. Haemost. 89, 409-419
8. 2-antiplasmin-binding sites Biochemistry 49, 7643-7651
9. Cheresh, D. A., Berliner, S. A., Vicente, V., and Ruggeri, Z. M. (1989) Recognition of distinct adhesive sites on fibrinogen by related integrins on platelets and endothelial cells Cell 58, 945-953
10. Belkin, A. M., Tsurupa, G., Zemskov, E., Veklich, Y., Weisel, J. W., and Medved, L. (2005) Transglutaminase-mediated oligomerization of the fibrin(ogen) αC domains promotes integrin-dependent cell adhesion and signaling Blood 105, 3561-3568
11. Kaijzel, E. L., Koolwijk, P., Van Erck, M. G. M., Van Hinsbergh, V. W. M., and De Maat, M. P. M. (2006) Molecular weight fibrinogen variants determine angiogenesis rate in a fibrin matrix in vitro and in vivo J. Thromb. Haemost. 4, 1975-1981
12. Tsurupa, G., Ho-Tin-Noe, B., Angles-Cano, E., and Medved, L. (2003) Identification and characterization of novel lysine-independent apolipoprotein(a)-binding sites in fibrin(ogen) αC-domains J. Biol. Chem. 278, 37154-37159
13. Medved, L. and Weisel, J. W. on behalf of Fibrinogen and Factor XIII Subcommittee of Scientific Standardization Committee of International Society on Thrombosis and Haemostasis (2009) Recommendations for nomenclature on fibrinogen and fibrin. J. Thromb. Haemost. 7, 355-359.
14. Privalov, P. L. and Medved, L. V. (1982) Domains in the fibrinogen molecule J. Mol. Biol. 159, 665-683
15. Medved, L. V., Gorkun, O. V., and Privalov, P. L. (1983) Structural organization of C-terminal parts of fibrinogen Aα-chains FEBS Lett. 160, 291-295
16. Tsurupa, G., Tsonev, L., and Medved, L. (2002) Structural organization of the fibrin(ogen) αC-domain Biochemistry 41, 6449-6459
17. Erickson, H. P. and Fowler, W. E. (1983) Electron microscopy of fibrinogen, its plasmic fragments and small polymers Ann. N.Y. Acad. Sci. 408, 146-163
18. Weisel, J. W., Stauffacher, C. V., Bullitt, E., and Cohen, C. (1985) A model for fibrinogen: domains and sequence Science 230, 1388-1391
19. Veklich, Y. I., Gorkun, O. V., Medved, L. V., Nieuwenhuizen, W., and Weisel, J. W. (1993) Carboxyl-terminal portions of the α chains of fibrinogen and fibrin. Localization by electron microscopy and the effects of isolated αC fragments on polymerization J. Biol. Chem. 268, 13577-13585
20. Tsurupa, G., Hantgan, R. R., Burton, R. A., Pechik, I., Tjandra, N., and Medved, L. (2009) Structure, stability, and interaction of the fibrin(ogen) αC-domains Biochemistry 48, 12191-12201
21. Burton, R. A., Tsurupa, G., Medved, L., and Tjandra, N. (2006) Identification of an ordered compact structure within the recombinant bovine fibrinogen αC-domain fragment by NMR Biochemistry 45, 2257-2266
22. Burton, R., Tsurupa, G., Hantgan, R. R., Tjandra, N., and Medved, L. (2007) NMR solution structure, stability, and interaction of the recombinant bovine fibrinogen αC-domain fragment Biochemistry 46, 8550-8560
23. Weisel, J. W. and Medved, L. (2001) The structure and function of the αC domains of fibrinogen Ann. N.Y. Acad. Sci. 936, 312-327
24. Litvinov, R. I., Yakovlev, S. V., Tsurupa, G., Gorkun, O. V., Medved, L., and Weisel, J. (2007) Direct evidence for specific interactions of the fibrinogen αC-domains with the central E region and with each other Biochemistry 46, 9133-9142
25. Tsurupa, G., Mahid, A., Veklich, Y., Weisel, J. W., and Medved, L. (2011) Structure, stability, and interaction of fibrin αC-domain polymers Biochemistry 50, 8028-8037
26. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein Identification and Analysis Tools on the ExPASy Server, in The Proteomics Protocols Handbook (Walker, J. M., Ed.) pp 571-607, Humana Press, Totowa, NJ.
27. 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
28. Litvinov, R. I., Bennett, J. S., Weisel, J. W., and Shuman, H. (2005) Multi-step fibrinogen binding to the integrin αIIbβ3 detected using force spectroscopy Biophys. J. 89, 2824-2834
29. 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
30. Pecora, R. (1983) Quasi-elastic light scattering of macromolecules and particles in solution and suspension, in Measurement of Suspended Particles by Quasi-Elastic Light Scattering (Dahneke, B. E., Ed.) 1 st ed., pp 3-30, John Wiley, New York.
31. Hantgan, R. R., Stahle, M. C., Connor, J. H., Lyles, D. S., Horita, D. A., Rocco, M., Nagaswami, C., Weisel, J. W., and McLane, M. A. (2004) The disintegrin Echistatin stabilizes integrin αIIbβ3′s open conformation and promotes its oligomerization J. Mol. Biol. 342, 1625-1636
32. Provencher, S. W. (1982) CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations Comput. Phys. Commun. 27, 229-242
33. Kawahara, K. and Tanford, C. (1966) Viscosity and density of aqueous solutions of urea and guanidine hydrochloride J. Biol. Chem. 241, 3228-3232
34. Cantor, C. R. and Schimmel, P. R. (1980) Size and shape of macromolecules, in Biophysical Chemistry. Part II: Techniques for the Study of Biological Structure and Function, pp 539-590, W.H. Freeman and Company, San Francisco.
35. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38, 16424-16431
36. Stafford, III, W. F. (1996) Hydrodynamic parameters-some rules of thumb, in Analytical Ultracentrifugation Workshop: Theory and Practice, p 20, National Analytical Ultracentrifugation Facility, Biotechnology Center, University of Connecticut, Storrs, CT.
37. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nigels, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system (CNS): A new software system for macromolecular structure determination Acta Crystallogr. D54, 905-921
38. Brunger, A. T. (1992) X-PLOR. A System for X-ray Crystallography and NMR, Yale University Press, New Haven, CT.
39. Matsuka, Y. V., Medved, L. V., Migliorini, M. M., and Ingham, K. C. (1996) Factor XIIIa-catalyzed cross-linking of recombinant αC fragments of human fibrinogen Biochemistry 35, 5810-5816
40. Zhang, C. and Kim, S. H. (2000) The anatomy of protein β-sheet topology J. Mol. Bol. 299, 1075-1089
41. Ellman, G. L. (1959) Tissue sulfhydryl groups Arch. Biochem. Biophys. 82, 70-77
42. Francis, C. W. and Marder, V. J. (1987) Rapid formation of large molecular weight α-polymers in cross-linked fibrin induced by high factor XIII concentrations. Role of platelet factor XIII J. Clin. Invest. 80, 1459-1465
43. Knoll, D., Hantgan, R., Williams, J., McDonagh, J., and Hermans, J. (1984) Characterization of soluble polymerized fibrin formed in the presence of excess fibrinogen fragment D Biochemistry 23, 3708-3715
44. Cottrell, B. A., Strong, D. D., Watt, K. W., and Doolittle, R. F. (1979) Amino acid sequence studies on the α chain of human fibrinogen. Exact location of cross-linking acceptor sites Biochemistry 18, 5405-5410
45. Corcoran, D. H., Ferguson, E. W., Fretto, L. J., and McKee, P. A. (1980) Localization of a cross-link donor site in the alpha-chain of human fibrin Thromb. Res. 19, 883-888
46. Marx, J., Hudry-Clergeon, G., Capet-Antonini, F., and Bernard, L. (1979) Laser Raman spectroscopy study of bovine fibrinogen and fibrin Biochim. Biophys. Acta 578, 107-115
47. Hudry-Clergeon, G. and Freyssinet, J.-M. (1983) Orientation of fibrin in strong magnetic fields Ann. N.Y. Acad. Sci. 408, 380-387
48. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A., Gough, T. S., Höök, M., Campbell, I. D., and Potts, J. R. (2003) Pathogenic bacteria attach to human fibronectin through a tandem β-zipper Nature 423, 171-181
49. Schwarz-Linek, U., Höök, M., and Potts, J. R. (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells Mol. Microbiol. 52, 631-641
50. Schwarz-Linek, U., Höök, M., and Potts, J. R. (2006) Fibronectin-binding proteins of gram-positive cocci Microbes Infect. 8, 2291-2298
51. Raibaud, S., Schwarz-Linek, U., Kim, J. H., Jenkins, H. T., Baines, E. R., Gurusiddappa, S., Höök, M., and Potts, J. R. (2005) Borrelia burgdorferi binds fibronectin through a tandem β-zipper, a common mechanism of fibronectin binding in Staphylococci, Streptococci, and Spirochetes J. Biol. Chem. 280, 18803-18809
52. Bingham, R. J., Rudino-Pinera, E., Meenan, N. A. G., Schwarz-Linek, U., Turkenburg, J. P., Hook, M., Garman, E. F., and Potts, J. R. (2008) Crystal structure of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains Proc. Natl. Acad. Sci. U. S. A. 105, 12254-12258
53. Doolittle, R. F., Watt, K. W. K., Cottrell, B. A., Strong, D. D., and Riley, M. (1979) The amino acid sequence of the α-chain of human fibrinogen Nature 280, 464-468
54. DeLano, W. L. (2000) PyMol, DeLano Scientific, San Carlos, CA.