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Biophysics

, Volume 62, Issue 2, pp 291–300 | Cite as

The mechanisms and kinetics of initiation of blood coagulation by the extrinsic tenase complex

  • T. A. KovalenkoEmail author
  • M. A. Panteleev
  • A. N. Sveshnikova
Complex Systems Biophysics

Abstract

The system of hemostasis includes coagulation of blood plasma and formation of platelet aggregate. Plasma clotting is a cascade of proteolytic reactions, triggered by the contact of blood plasma with any tissue except the normal vessel endothelium. During the contact an enzymatic complex is formed of the soluble blood plasma protein, factor VIIa, and a membrane-anchored protein, tissue factor. This complex is called extrinsic tenase; it is the key initiator of blood coagulation. The main substrates of extrinsic tenase are blood plasma factors X and IX. During the reaction they undergo proteolytic cleavage and become active serine proteases, factors Xa and IXa, respectively. Factor Xa in complex with its cofactor factor Va catalyzes formation of the key coagulation enzyme, thrombin, which leads to fibrin polymerization and plasma gelation. Although all of the proteins that participate in this process have been known for a long time, several questions remain unanswered. As an example, what is the role of the reaction surface on which the complex is formed, what is the role of membrane-bound multimeres of factor X (Xa), and in what way does the activation of the factor VII proceed? Here, we review recent theoretical and experimental works focused on the biophysical mechanisms of extrinsic tenase functioning and discuss some of these problems.

Keywords

blood coagulation extrinsic tenase factor X dimerization mathematical modeling 

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References

  1. 1.
    M. A. Panteleev, N. M. Dashkevich, and F. I. Ataullakhanov, Thromb. Res. 136, 699 (2015).CrossRefGoogle Scholar
  2. 2.
    H. H. Versteeg, J. W. M. Heemskerk, M. Levi, and P. H. Reitsma, Physiol. Rev. 93, 327 (2013).CrossRefGoogle Scholar
  3. 3.
    E. W. Davie and O. D. Ratnoff, Science 145, 1310 (1964).ADSCrossRefGoogle Scholar
  4. 4.
    R. G. Macfarlane, Nature 202, 498 (1964).ADSCrossRefGoogle Scholar
  5. 5.
    M. Hoffman and D. M. Monroe 3rd, Thromb. Haemost. 85, 958 (2001).Google Scholar
  6. 6.
    J. H. Morrissey, H. Fakhrai, and T. S. Edgington, Cell 50, 129 (1987).CrossRefGoogle Scholar
  7. 7.
    L. R. Paborsky, I. W. Caras, K. L. Fisher, and C. M. Gorman, J. Biol. Chem. 266, 21911 (1991).Google Scholar
  8. 8.
    B. Osterud, A. Tindall, J. H. Brox, and J. O. Olsen, Thromb. Res. 42, 323 (1986).CrossRefGoogle Scholar
  9. 9.
    T. A. Drake, J. H. Morrissey, and T. S. Edgington, Am. J. Pathol. 134, 1087 (1989).Google Scholar
  10. 10.
    R. A. Fleck, L. V. Rao, S. I. Rapaport, and N. Varki, Thromb. Res. 59, 421 (1990).CrossRefGoogle Scholar
  11. 11.
    S. Butenas, B. A. Bouchard, K. E. Brummel-Ziedins, et al., Blood 105, 2764 (2005).CrossRefGoogle Scholar
  12. 12.
    P. L. Giesen, U. Rauch, B. Bohrmann, et al., Proc. Natl. Acad. Sci. U. S. A. 96, 2311 (1999).ADSCrossRefGoogle Scholar
  13. 13.
    V. Y. Bogdanov, V. Balasubramanian, J. Hathcock, et al., Nat. Med. 9, 458 (2003).CrossRefGoogle Scholar
  14. 14.
    R. F. Zwaal, P. Comfurius, and E. M. Bevers, Biochim. Biophys. Acta 1376, 433 (1998).CrossRefGoogle Scholar
  15. 15.
    J. F. McDonald, A. M. Shah, R. A. Schwalbe, et al., Biochemistry 36, 5120 (1997).CrossRefGoogle Scholar
  16. 16.
    M. Koren-Michowitz, N. Rahimi-Levene, Y. Volcheck, et al., Isr. Med. Assoc. J. 8, 53 (2006).Google Scholar
  17. 17.
    G. J. J. Broze and P. W. Majerus, J. Biol. Chem. 255, 1242 (1980).Google Scholar
  18. 18.
    K. Kurachi and E. W. Davie, Proc. Natl. Acad. Sci. USA. 79, 6461 (1982).ADSCrossRefGoogle Scholar
  19. 19.
    S. P. Leytus, D. W. Chung, W. Kisiel, et al., Proc. Natl. Acad. Sci. USA. 81, 3699 (1984).ADSCrossRefGoogle Scholar
  20. 20.
    C. Vermeer, Biochem. J. 266, 625 (1990).CrossRefGoogle Scholar
  21. 21.
    G. L. Nelsestuen, W. Kisiel, and R. G. Di Scipio, Biochemistry 17, 2134 (1978).CrossRefGoogle Scholar
  22. 22.
    C. D. McCallum, R. C. Hapak, P. F. Neuenschwander, et al., J. Biol. Chem. 271, 28168 (1996).CrossRefGoogle Scholar
  23. 23.
    E. J. Husten, C. T. Esmon, and A. E. Johnson, J. Biol. Chem. 262, 12953 (1987).Google Scholar
  24. 24.
    S. Yegneswaran, G. M. Wood, C. T. Esmon, and A. E. Johnson, J. Biol. Chem. 272, 25013 (1997).CrossRefGoogle Scholar
  25. 25.
    C. M. Colina, D. Venkateswarlu, R. Duke, et al., J. Thromb. Haemost. 4, 2726 (2006).CrossRefGoogle Scholar
  26. 26.
    S. H. Qureshi, L. Yang, S. Yegneswaran, and A. R. Rezaie, Biochem. J. 407, 427 (2007).CrossRefGoogle Scholar
  27. 27.
    D. Venkateswarlu, L. Perera, T. Darden, and L. G. Pedersen, Biophys. J. 82, 1190 (2002).CrossRefGoogle Scholar
  28. 28.
    Y. Z. Ohkubo and E. Tajkhorshid, Structure 16, 72 (2008).CrossRefGoogle Scholar
  29. 29.
    G. L. Nelsestuen and M. Broderius, Biochemistry 16, 4172 (1977).CrossRefGoogle Scholar
  30. 30.
    G. A. Cutsforth, R. N. Whitaker, J. Hermans, and B. R. Lentz, Biochemistry 28, 7453 (1989).CrossRefGoogle Scholar
  31. 31.
    G. van Dieijen, G. Tans, J. van Rijn, et al., Biochemistry 20, 7096 (1981).CrossRefGoogle Scholar
  32. 32.
    A. W. Shaw, V. S. Pureza, S. G. Sligar, and J. H. Morrissey, J. Biol. Chem. 282, 6556 (2007).CrossRefGoogle Scholar
  33. 33.
    V. J. Bom and R. M. Bertina, Biochem. J. 265, 327 (1990).CrossRefGoogle Scholar
  34. 34.
    R. Bach, R. Gentry, and Y. Nemerson, Biochemistry 25, 4007 (1986).CrossRefGoogle Scholar
  35. 35.
    D. P. O’Brien, G. Kemball-Cook, A. M. Hutchinson, et al., Biochemistry 33, 14162 (1994).CrossRefGoogle Scholar
  36. 36.
    L. V. Rao and S. I. Rapaport, Proc. Natl. Acad. Sci. USA. 85, 6687 (1988).ADSCrossRefGoogle Scholar
  37. 37.
    P. Sen, P. F. Neuenschwander, U. R. Pendurthi, and L. V. M. Rao, Blood Coagul. Fibrinolysis 21, 376 (2010).CrossRefGoogle Scholar
  38. 38.
    H. Mei, Y. Hu, H. Wang, et al., J. Huazhong Univ. Sci. Technol. Med. Sci. 30, 42 (2010).CrossRefGoogle Scholar
  39. 39.
    K. Ke, J. Yuan, and J. H. Morrissey, PLOS ONE 9, e88675 (2014).ADSCrossRefGoogle Scholar
  40. 40.
    W. Ruf, M. W. Kalnik, T. Lund-Hansen, and T. S. Edgington, J. Biol. Chem. 266, 15719 (1991).Google Scholar
  41. 41.
    Y. Z. Ohkubo, J. H. Morrissey, and E. Tajkhorshid, J. Thromb. Haemost. 8, 1044 (2010).Google Scholar
  42. 42.
    S. Butenas and K. G. Mann, Biochemistry 35, 1904 (1996).CrossRefGoogle Scholar
  43. 43.
    Y. Nemerson and D. Repke, Thromb. Res. 40, 351 (1985).CrossRefGoogle Scholar
  44. 44.
    P. F. Neuenschwander and J. H. Morrissey, J. Biol. Chem. 267, 14477 (1992).Google Scholar
  45. 45.
    P. F. Neuenschwander, M. M. Fiore, and J. H. Morrissey, J. Biol. Chem. 268, 21489 (1993).Google Scholar
  46. 46.
    W. Kisiel, K. Fujikawa, and E. W. Davie, Biochemistry 16, 4189 (1977).CrossRefGoogle Scholar
  47. 47.
    M. Zur and Y. Nemerson, J. Biol. Chem. 255, 5703 (1980).Google Scholar
  48. 48.
    R. J. Baugh, C. D. Dickinson, W. Ruf, and S. Krishnaswamy, J. Biol. Chem. 275, 28826 (2000).CrossRefGoogle Scholar
  49. 49.
    B. V Norledge, R. J. Petrovan, W. Ruf, and A. J. Olson, Proteins 53, 640 (2003).CrossRefGoogle Scholar
  50. 50.
    S. Krishnaswamy, K. A. Field, T. S. Edgington, et al., J. Biol. Chem. 267, 26110 (1992).Google Scholar
  51. 51.
    P. F. Neuenschwander, E. Bianco-Fisher, R. Rezaie, and J. H. Morrissey, Biochemistry 34, 13988 (1995).CrossRefGoogle Scholar
  52. 52.
    N. Tavoosi, R. L. Davis-Harrison, T. V. Pogorelov, et al., J. Biol. Chem. 286, 23247 (2011).CrossRefGoogle Scholar
  53. 53.
    J. J. Hathcock, E. Rusinova, H. Andree, and Y. Nemerson, Blood Cells. Mol. Dis. 36, 194 (2006).CrossRefGoogle Scholar
  54. 54.
    S. D. Forman and Y. Nemerson, Proc. Natl. Acad. Sci. USA. 83, 4675 (1986).ADSCrossRefGoogle Scholar
  55. 55.
    R. Majumder, J. Wang, and B. R. Lentz, Biophys. J. 84, 1238 (2003).ADSCrossRefGoogle Scholar
  56. 56.
    R. Chattopadhyay, R. Iacob, S. Sen, et al., Biophys. J. 96, 974 (2009).ADSCrossRefGoogle Scholar
  57. 57.
    T. Koklic, R. Majumder, G. E. Weinreb, and B. R. Lentz, Biophys. J. 97, 2232 (2009).ADSCrossRefGoogle Scholar
  58. 58.
    N. A. Podoplelova, A. N. Sveshnikova, J. H. Kurasawa, et al., Biochim. Biophys. Acta 1858, 1216 (2016).CrossRefGoogle Scholar
  59. 59.
    J. J. Hathcock, E. Rusinova, R. D. Gentry, et al., Biochemistry 44, 8187 (2005).CrossRefGoogle Scholar
  60. 60.
    K. C. Jones and K. G. Mann, J. Biol. Chem. 269, 23367 (1994).Google Scholar
  61. 61.
    R. Gentry, L. Ye, and Y. Nemerson, Biophys. J. 69, 362 (1995).ADSCrossRefGoogle Scholar
  62. 62.
    E.-M. Erb, J. Stenflo, and T. Drakenberg, Eur. J. Biochem. 269, 3041 (2002).CrossRefGoogle Scholar
  63. 63.
    P. L. Giesen, G. M. Willems, H. C. Hemker, and W. T. Hermens, J. Biol. Chem. 266, 18720 (1991).Google Scholar
  64. 64.
    H. A. Andree, P. B. Contino, D. Repke, et al., Biochemistry 33, 4368 (1994).CrossRefGoogle Scholar
  65. 65.
    G. M. Willems, M. P. Janssen, I. Salemink, et al., Biochemistry 37, 3321 (1998).CrossRefGoogle Scholar
  66. 66.
    P. van de Waart, H. Bruls, H. C. Hemker, and T. Lindhout, Biochemistry 22, 2427 (1983).CrossRefGoogle Scholar
  67. 67.
    S. Krishnaswamy, K. C. Jones, and K. G. Mann, J. Biol. Chem. 263, 3823 (1988).Google Scholar
  68. 68.
    M. A. Panteleev, N. M. Ananyeva, N. J. Greco, et al., FEBS J. 273, 374 (2006).CrossRefGoogle Scholar
  69. 69.
    A. M. Shibeko, S. S. Karamzin, A. A. Butylin, et al., Biochem. Suppl. Ser. A. Membr. Cell Biol. 3, 388 (2009).Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2017

Authors and Affiliations

  • T. A. Kovalenko
    • 1
    • 2
    Email author
  • M. A. Panteleev
    • 1
    • 2
    • 3
    • 4
  • A. N. Sveshnikova
    • 1
    • 2
    • 3
    • 5
  1. 1.Department of PhysicsMoscow State UniversityMoscowRussia
  2. 2.Center for Theoretical Problems of Physicochemical PharmacologyRussian Academy of SciencesMoscowRussia
  3. 3.Federal Research and Clinical Center of Pediatric Hematology, Oncology and ImmunologyMoscowRussia
  4. 4.Faculty of Biological and Medical PhysicsMoscow Institute of Physics and TechnologyMoscow RegionRussia
  5. 5.Therapeutic FacultyPirogov Russian National Research Medical UniversityMoscowRussia

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