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Activation of Factor X by Snake Venom Proteases

  • Jüri SiigurEmail author
  • Ene Siigur
Chapter

Abstract

Human coagulation factor X is a serine protease zymogen, which circulates in blood as a two-chain molecule. A variety of factor X activators have been detected in snake venoms. About 15 activators have been isolated from Viperidae, Crotalidae and Elapidae venoms. Viperidae and Crotalidae venom activators are mainly metalloproteases. Only two factor X activators are characterized from Elapidae venoms, both belonging to serine proteases. Most thoroughly investigated snake venom factor X activators are from Vipera russellii (now renamed Daboia russellii) - RVV-X, and Vipera lebetina (now renamed Macrovipera lebetina) - VLFXA. RVV-X is a heterotrimeric metalloproteinase with a mammalian ADAM-like heavy chain and two lectin-like light chains. The crystal structure of RVV-X has recently been determined. VLFXA is the first factor X activator that was cloned and sequenced and its primary structure was deduced from the cDNA sequences. Both activators consist of a heavy chain and two C-type lectin–like light chains which are held together by disulfide bonds. Heavy chains of RVV-X and VLFXA contain metalloprotease, disintegrin-like and cysteine-rich domains. All chains of VLFXA and RVV-X are synthesized from different genes. The primary structures of factor X activating snake venom serine proteases are unknown up to now.

Keywords

Light Chain Heavy Chain Sialic Acid Snake Venom Tenase Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The work was financially supported by Estonian Science Foundation grant No. 7251 and by target financing SF0180114Bs08.

References

  1. Amphlett, G.W., Byrne, R., Castellino, F.J., 1982. Cation binding properties of the multiple subforms of RVV-X, the coagulant protein from Vipera russelli. Biochemistry 21, 125–132.PubMedCrossRefGoogle Scholar
  2. Aurell, L., Friberger, P., Karlsson, G., Claeson, G., 1977. A new sensitive and highly specific chromogenic peptide substrate for Factor Xa. Thromb. Res. 11, 595–605.PubMedCrossRefGoogle Scholar
  3. Baugh, R.J., Krishnaswamy, S., 1996. Role of the activation peptide domain in human factor X activation by the extrinsic Xase complex. J. Biol. Chem. 271, 16126–16134.PubMedCrossRefGoogle Scholar
  4. Bjarnason, J.B., Fox J.W., 1995. Snake venom metalloendopeptidases: reprolysins. Meth. Enzymol. 248, 345–368.PubMedCrossRefGoogle Scholar
  5. Cerretti, D.P., DuBose, R.F., Black, R.A., Nelson, N., 1999. Isolation of two novel metalloproteinase-disintegrin (ADAM) cDNAs that show testis–specific gene expression. Biochem. Biophys. Res. Commun. 263, 810–815.PubMedCrossRefGoogle Scholar
  6. Chen, H.-S., Chen, J.-M., Lin, C.-V., Khoo, K.-H., Tsai, I.-H., 2008. New insights into the functions and N-glycan structures of factor X activator from Russell’s viper venom. FEBS J. 275, 3944–3958.PubMedCrossRefGoogle Scholar
  7. Durkee, K.H., Roh, B.H., Doellgast, G.J., 1993. Immunoaffinity chromatographic purification of Russell’s viper venom factor X activator using elution in high concentrations of magnesium chloride. Protein Expr. Purif. 4, 405–411.PubMedCrossRefGoogle Scholar
  8. El-Asmar, M.F., Shaban, E., Hagag, M., Swelam, N., Tu, A.T., 1986. Coagulant component in Cerastes cerastes (Egyptian sand viper) venom. Toxicon 24, 1037–1044.PubMedCrossRefGoogle Scholar
  9. Esnouf, M.P., 1978. Current perspectives of factor X, in: Recent Progress in Blood Coagulation and Thrombosis Research. Biblthca. Haemat. (vol. 44). Karger, Basel, pp. 75–80.Google Scholar
  10. Farid, T., Nasser, H., Zaki, K., El-Asmar, M.F., 1993. Low molecular weight factor X activator from Cerastes vipera (Sahara sand viper) venom. Toxicon 31, 1007–1017.PubMedCrossRefGoogle Scholar
  11. Fox, J.W., Serrano, S.M.T., 2008. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 275, 3016–3030.PubMedCrossRefGoogle Scholar
  12. Franssen, J.H.L., Janssen-Claessen, T., van Dieijen, G., 1983. Purification and properties of an activating enzyme of blood clotting factor X from the venom of Cerastes cerastes. Biochim. Biophys. Acta 747, 186–190.PubMedCrossRefGoogle Scholar
  13. Fujikawa, K., Coan, M.H., Legaz, M.E., Davie, E.W., 1974. The mechanism of activation of bovine factor X (Stuart factor) by intrinsic and extrinsic pathways. Biochemistry 13, 5290–5299.PubMedCrossRefGoogle Scholar
  14. Fujikawa, K., Titani, K., Davie, E.W., 1975. Activation of bovine factor X (Stuart factor): conversion of factor X to factor X. Proc. Natl. Acad. Sci. U.S.A. 72, 3359–3363.PubMedCrossRefGoogle Scholar
  15. Furie, B.C., Furie, B., 1975. Interaction of lanthanide ions with bovine factor X and their use in the affinity chromatography of the venom coagulant protein of Vipera russelli. J. Biol. Chem. 250, 601–608.PubMedGoogle Scholar
  16. Furukawa, Y., Matsunaga, Y., Hayashi, K., 1976. Purification and characterization of a coagulant protein from the venom of Russell’s viper. Biochim. Biophys. Acta 453, 48–61.PubMedCrossRefGoogle Scholar
  17. Gowda, D.C., Jackson, C.M., Hensley, P., Davidson, E.A., 1994. Factor X-activating glycoprotein of Russell’s viper venom. J. Biol. Chem. 269, 10644–10650.PubMedGoogle Scholar
  18. Gowda, D.C., Jackson, C.M., Kurzban, G.P., McPhie, P., Davidson, E.A., 1996. Core sugar residues of the N-linked oligosaccharides of Russell’s viper venom factor X-activator maintain functionally active polypeptide structure. Biochemistry 35, 5833–5837.PubMedCrossRefGoogle Scholar
  19. Grams, F., Huber, R., Kress, L.F., Moroder, L., Bode, W., 1993. Activation of snake venom metalloproteinases by a cysteine switch like mechanism. FEBS Lett. 335, 76–80.PubMedCrossRefGoogle Scholar
  20. Hertzberg, M., 1994. Biochemistry of factor X. Blood Rev. 8, 56–62.PubMedCrossRefGoogle Scholar
  21. Hofmann, H., Bon, C., 1987. Blood coagulation induced by the venom of Bothrops atrox. 2. Identification, purification and properties of two factor X activators. Biochemistry 26, 780–787.PubMedCrossRefGoogle Scholar
  22. Hofmann, H., Dumarey, C., Bon, C., 1983. Blood coagulation induced by Bothrops atrox venom. Identification and properties of a factor X activator. Biochimie 65, 201–210.PubMedCrossRefGoogle Scholar
  23. Jackson, C.M., Gordon, J.G., Hanahan, D.J., 1971, Separation of the tosyl arginine esterase activity from the factor X activating enzyme of Russell’s viper venom. Biochim. Biophys. Acta 252, 255–261.PubMedCrossRefGoogle Scholar
  24. Jesty, J., 1986. Analysis of the generation and inhibition of activated coagulation factor X in pure systems and in human plasma. J. Biol. Chem. 261, 8695–8702.PubMedGoogle Scholar
  25. Kishimoto, M., Takahashi, T., 2002. Molecular cloning of HR1a and HR1b, high molecular hemorrhagic factors, from Trimeresurus flavoviridis venom. Toxicon 40, 1369–1375.PubMedCrossRefGoogle Scholar
  26. Kisiel, W., Hermodson, M.A., Davie, E.W., 1976. Factor X activating enzyme from Russell’s viper venom: isolation and characterization. Biochemistry 15, 4901–4906.PubMedCrossRefGoogle Scholar
  27. Komori, Y., Nikai, T., Sugihara, H., 1990. Isolation and characterization of factor X activator from the venom of Vipera aspis aspis. Int. J. Biochem. 22, 1053–1060.PubMedCrossRefGoogle Scholar
  28. Kosow, D.P., 1976. Purification and activation of human factor X: cooperative effect of Ca2+ on the activation reaction. Thromb. Res. 9, 565–573.PubMedCrossRefGoogle Scholar
  29. Lee, W.H., Zhang, Y., Wang, W.-Y., Xiong, Y.-L., Gao, R., 1995. Isolation and properties of a blood coagulation factor X activator from the venom of king cobra (Ophiophagus hannah). Toxicon 33, 1263–1276.PubMedCrossRefGoogle Scholar
  30. Leonardi, A., Fox, J.W., Trampuš-Bakija, A., Križaj, I., 2008. Two coagulation factor X activators from Vipera a. ammodytes venom with potential to treat patients with dysfunctional factors IXa or VIIa. Toxicon 52, 628–637.PubMedCrossRefGoogle Scholar
  31. Leytus, S.P., Chung, D.W., Kisiel, W., Kurachi, K., Davie, E.W., 1984. Characterization of a cDNA coding for human factor X. Proc. Natl. Acad. Sci. U.S.A. 81, 3699–3702.PubMedCrossRefGoogle Scholar
  32. Lindhout, M.J., Kop-Klaassen, B.H.M., Hemker, H.C., 1978. Activation of decarboxyfactor X by a protein from Russell’s viper venom. Purification and partial characterization of activated decarboxyfactor X. Biochim. Biophys. Acta 533, 327–341.PubMedCrossRefGoogle Scholar
  33. Marsh, N.A., 2001. Diagnostic use of snake venoms. Haemostasis 31, 211–217.PubMedGoogle Scholar
  34. Matsui, T., Fujimura, Y., Titani, K., 2000. Snake venom proteases affecting hemostasis and thrombosis. Biochim. Biophys. Acta 1477, 146–156.PubMedCrossRefGoogle Scholar
  35. Matsuzaki, R., Yoshiara, E., Yamada, M., Shima, K., Atoda, H., Morita, T., 1996. cDNA cloning of IX/X-BP, a heterogeneous two-chain anticoagulant protein from snake venom. Biochem. Biophys. Res. Commun. 220, 382–387.Google Scholar
  36. Morita, T., 1998. Proteases which activate factor X, in: Bailey, G.S. (Ed.), Enzymes from Snake Venoms. Alaken Inc., Fort Collins, Colorado, pp. 179–208.Google Scholar
  37. Nishida, S., Fujita, T., Kohno, N., Atoda, H., Morita, T., Takeya, H., Kido, I., Paine, M.J., Kawabata, S., Iwanaga, S., 1995. cDNA cloning and deduced amino acid sequence of prothrombin activator (ecarin) from Kenyan Echis carinatus venom. Biochemistry 34, 1771–1778.PubMedCrossRefGoogle Scholar
  38. Owen, C.A., Jr., 2001. Inherited coagulation factor deficiencies, in: Nichols, W.L., Bowie, E.J.W. (Eds.), A History of Blood Coagulation. Mayo Foundation for Medical Education and Research, Rochester, MN, pp. 117–132.Google Scholar
  39. Pryzdial, E.L.G., Lavigne, N., Dupuis, N., Kessler, G.E., 1999. Plasmin converts factor X from coagulation zymogen to fibrinolysis cofactor. J. Biol. Chem. 274, 8500–8505.PubMedCrossRefGoogle Scholar
  40. Pukrittayakamee, S., Esnouf, M.P., McMichael, A.J., 1983. Purification and inactivation of the factor X activator of Russell’s viper venom with monoclonal antibodies. Mol. Biol. Med. 1, 123–135.PubMedGoogle Scholar
  41. Samel, M., Siigur, J., 1995. Medium molecular weight factor X activating enzyme from Vipera berus berus venom. Toxicon 33, 41–52.PubMedCrossRefGoogle Scholar
  42. Samel, M., Vija, H., Subbi, J., Siigur, J., 2003. Metalloproteinase with factor X activating and fibrinolytic activities from Vipera berus berus venom. Comp. Biochem. Physiol. B. 135, 575–582.PubMedCrossRefGoogle Scholar
  43. Sekiya, F., Yoshida, M., Yamashita, T., Morita, T., 1996. Magnesium (II) is a crucial constituent of the blood coagulation cascade. J. Biol. Chem. 271, 8541–8544.PubMedCrossRefGoogle Scholar
  44. Siigur, E., Aaspõllu, A., Trummal, K., Tõnismägi, K., Tammiste, I., Kalkkinen, N., Siigur, J., 2004. Factor X activator from Vipera lebetina venom is synthesized from different genes. Biochim. Biophys. Acta 1702, 41–51.PubMedCrossRefGoogle Scholar
  45. Siigur, E., Tõnismägi, K., Trummal, K., Samel, M., Vija, H., Subbi, J., Siigur, J., 2001a. Factor X activator from Vipera lebetina snake venom, molecular characterization and substrate specificity. Biochim. Biophys. Acta 1568, 90–98.PubMedCrossRefGoogle Scholar
  46. Siigur, J., Aaspõllu, A., Tõnismägi, K., Trummal, K., Samel, M., Vija, H., Subbi, J., Siigur, E., 2001b. Proteases from Vipera lebetina venom affecting coagulation and fibrinolysis. Haemostasis 31, 123–132.PubMedGoogle Scholar
  47. Siigur, J., Siigur, E., 2006. Factor X activating proteases from snake venoms. Toxin Rev. 25, 235–255.CrossRefGoogle Scholar
  48. Silva, M.B., Schattner, M., Ramos, C.R.R., Junqueira-De-Azevedo, I.L.M., Guarnieri, M.C., Lazzari, M.A., Sampaio, C.A.M., Pozner, R.G., Ventura, J.S., Ho, P.L., Chudzinski-Tavassi, A.M., 2003. A prothrombin activator from Bothrops erythromelas (Jararaca-da-seca) snake venom: characterization and molecular cloning. Biochem. J. 369, 129–139.PubMedCrossRefGoogle Scholar
  49. Sinha, U., Wolf, D.L., 1993. Carbohydrate residues modulate the activation of coagulation factor X. J. Biol. Chem. 268, 3048–3051.PubMedGoogle Scholar
  50. Skogen, W.F., Bushone, D.S., Johnson, A.E., Cox, A.C., 1983. The role of the Gla domain in the activation of bovine coagulation factor X by the snake venom protein XCP. Biochem. Biophys. Res. Commun. 111, 14–20.PubMedCrossRefGoogle Scholar
  51. Stocker, K., 1990. Snake venom proteins affecting hemostasis and fibrinolysis, in: Stocker, K. (Ed.), Medical Use of Snake Venom Proteins. CRC Press, Boca Raton, Ann Arbor, Boston, pp. 97–160.Google Scholar
  52. Stocker, K., 1998. Research, diagnostic and medicinal uses of snake venom enzymes, in: Bailey, G.S. (Ed.), Enzymes in Snake Venoms. Alaken Inc., Fort Collins, CO, pp. 705–736.Google Scholar
  53. Strachan, N.J.C., Ogden, I.D., 2000. A sensitive microsphere coagulation ELISA for Escherichia coli O157:H7 using Russell’s viper venom. FEMS Microbiol. Lett. 186, 79–84.PubMedCrossRefGoogle Scholar
  54. Takeda, S., Igarashi, T., Mori, H., 2007. Crystal structure of RVV-X: an example of evolutionary gain of specificity by ADAM proteinases. FEBS Lett. 581, 5859–5864.PubMedCrossRefGoogle Scholar
  55. Takeya, H., Nishida, S., Miyata, T., Kawada, S., Saisaka, Y., Morita, T., Iwanaga, S., 1992. Coagulation factor X activating enzyme from Russell’s viper venom (RVV-X). J. Biol. Chem. 267, 14109–14117.PubMedGoogle Scholar
  56. Tans, G., Rosing, J., 2001. Snake venom activators of factor X: an overview. Haemostasis 31, 225–233.PubMedGoogle Scholar
  57. Teng, C.-M., Chen, Y.-H., Ouyang, C., 1984. Purification and properties of the main coagulant and anticoagulant principles of Vipera russelli snake venom. Biochim. Biophys. Acta 786, 204–212.PubMedCrossRefGoogle Scholar
  58. van Dieijen, G., Tans, G., van Rijn, J., Zwaal, R.F.A., Rosing, J., 1981. Simple and rapid method to determine the binding of blood clotting factor X to phospholipid vesicles. Biochemistry 20, 7096–7101.PubMedCrossRefGoogle Scholar
  59. Wagstaff, S.C., Laing, G.D., Theakston, R.D.G., Pappaspyridis, C., Harrison, R.A., 2006. Bioinformatics and multiepitope DNA immunization to design rational snake antivenom. PloS Med. 3, e184.PubMedCrossRefGoogle Scholar
  60. Williams, W.J., Esnouf, M.P., 1962. The fractionation of Russell’s viper (Vipera russellii) venom with special reference to the coagulant protein. Biochem. J. 84, 52–62.PubMedGoogle Scholar
  61. Yamada, D., Sekiya, F., Morita, T., 1997. Prothrombin and factor X activator activities in the venoms of Viperidae snakes. Toxicon 35, 1581–1589.PubMedCrossRefGoogle Scholar
  62. Zhang, Y., Xiong, Y.-L., Bon, C., 1995. An activator of blood coagulation factor X from the venom of Bungarus fasciatus. Toxicon 33, 1277–1288.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Laboratory of Bioorganic ChemistryNational Institute of Chemical Physics and BiophysicsTallinnEstonia
  2. 2.National Institute of Chemical Physics and BiophysicsTallinnEstonia

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