Advertisement

Origin and Evolution of Snake Venom Prothrombin Activators

  • Md. Abu RezaEmail author
  • R. Manjunatha Kini
Chapter

Abstract

Snake venom is a mixture of various proteins and peptides with distinct pharmacological properties. They have the unique aptitude to attack specific physiological systems of the prey with remarkable specificity and thereby obstruct the natural function culminating in death and debilitation of the victim. The origin of snake venom toxins is one of the most interesting question that intrigued scientists for a long time. In this chapter, we will discuss the origin of a particular group of venom proteins, namely prothrombin activators. The results from our recent studies provide molecular evidence that this class of deadly toxins have evolved by gene duplication and recruitment of blood coagulation factor gene. Thus a new toxin has evolved after recruitment from a simple body protein that is involved in its own lifesaving haemostasis.

Keywords

Snake Venom Venom Gland Prothrombin Activator Blood Coagulation Factor Venom Protein 
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.

References

  1. Allen, G.C., Hall, G., Jr., Michalowski, S., Newman, W., Spiker, S., Weissinger, A.K., Thompson, W.F., 1996. High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. Plant Cell 8, 899–913.PubMedGoogle Scholar
  2. Blasquez, V.C., Xu, M., Moses, S.C., Garrard, W.T., 1989. Immunoglobulin kappa gene expression after stable integration. I. Role of the intronic MAR and enhancer in plasmacytoma cells. J. Biol. Chem. 264, 21183–21189.PubMedGoogle Scholar
  3. Bode, J., Kohwi, Y., Dickinson, L., Joh, T., Klehr, D., Mielke, C., Kohwi-Shigematsu, T., 1992. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science 255, 195–197.PubMedCrossRefGoogle Scholar
  4. Braud, S., Bon, C., Wisner, A., 2000. Snake venom proteins acting on hemostasis. Biochimie 82, 851–859.PubMedCrossRefGoogle Scholar
  5. Chester, A., Crawford, G.P., 1982. In vitro coagulant properties of venoms from Australian snakes. Toxicon 20, 501–504.PubMedCrossRefGoogle Scholar
  6. Chow, G., Kini, R.M., 2001. Exogenous factors from animal sources that induce platelet aggregation. Thromb. Haemost. 85, 177–178.PubMedGoogle Scholar
  7. Esmon, C.T., 2001. Role of coagulation inhibitors in inflammation. Thromb. Haemost. 86, 51–56.PubMedGoogle Scholar
  8. Foster, W.B., Nesheim, M.E., Mann, K.G., 1983. The factor Xa-catalyzed activation of factor V. J. Biol. Chem. 258, 13970–13977.PubMedGoogle Scholar
  9. Fujimi, T.J., Kariya, Y., Tsuchiya, T., Tamiya, T., 2002. Nucleotide sequence of phospholipase A2 gene expressed in snake pancreas reveals the molecular evolution of toxic phospholipase A2 genes. Gene 292, 225–231.PubMedCrossRefGoogle Scholar
  10. Fujimi, T.J., Nakajyo, T., Nishimura, E., Ogura, E., Tsuchiya, T., Tamiya, T., 2003. Molecular evolution and diversification of snake toxin genes, revealed by analysis of intron sequences. Gene 313, 111–118.PubMedCrossRefGoogle Scholar
  11. Gao, R., Kini, R.M., Gopalakrishnakone, P., 2002. A novel prothrombin activator from the venom of Micropechis ikaheka: isolation and characterization. Arch. Biochem. Biophys. 408, 87–92.PubMedCrossRefGoogle Scholar
  12. Guinto, E.R., Esmon, C.T., Mann, K.G., MacGillivray, R.T., 1992. The complete cDNA sequence of bovine coagulation factor V. J. Biol. Chem. 267, 2971–2978.PubMedGoogle Scholar
  13. Hasson, S.S., Theakston, R.D., Harrison, R.A., 2003. Cloning of a prothrombin activator-like metalloproteinase from the West African saw-scaled viper, Echis ocellatus. Toxicon 42, 629–634.PubMedCrossRefGoogle Scholar
  14. Hortin, G.L., 1990. Sulfation of tyrosine residues in coagulation factor V. Blood 76, 946–952.PubMedGoogle Scholar
  15. Hung, H.L., High, K.A., 1996. Liver-enriched transcription factor HNF-4 and ubiquitous factor NF-Y are critical for expression of blood coagulation factor X. J. Biol. Chem. 271, 2323–2331.PubMedCrossRefGoogle Scholar
  16. Hung, H.L., Pollak, E.S., Kudaravalli, R.D., Arruda, V., Chu, K., High, K.A., 2001. Regulation of human coagulation factor X gene expression by GATA-4 and the Sp family of transcription factors. Blood 97, 946–951.PubMedCrossRefGoogle Scholar
  17. Hutton, R.A., Warrell, D.A., 1993. Action of snake venom components on the haemostatic system. Blood Rev. 7, 176–189.PubMedCrossRefGoogle Scholar
  18. Inoue, K., Morita, T., 1993. Identification of O-linked oligosaccharide chains in the activation peptides of blood coagulation factor X. The role of the carbohydrate moieties in the activation of factor X. Eur. J. Biochem. 218, 153–163.PubMedCrossRefGoogle Scholar
  19. Jeyaseelan, K., Armugam, A., Donghui, M., Tan, N.H., 2000. Structure and phylogeny of the venom group I phospholipase A2 gene. Mol. Biol. Evol. 17, 1010–1021.PubMedCrossRefGoogle Scholar
  20. Jobin, F., Esnouf, M.P., 1966. Coagulant activity of tiger snake (Notechis scutatus scutatus) venom. Nature 211, 873–875.PubMedCrossRefGoogle Scholar
  21. Joseph, J.S., Chung, M.C., Jeyaseelan, K., Kini, R.M., 1999. Amino acid sequence of trocarin, a prothrombin activator from Tropidechis carinatus venom: its structural similarity to coagulation factor Xa. Blood 94, 621–631.PubMedGoogle Scholar
  22. Joseph, J.S., Kini, R.M., 2001. Snake venom prothrombin activators homologous to blood coagulation factor Xa. Haemostasis 31, 234–240.PubMedGoogle Scholar
  23. Joseph, J.S., Thirumangalathu, S., Tsang, F., Wong, F.W., Kini, R.M., 2003. Trocarin, a blood coagulation factor Xa homologue from snake venom, causes inflammation and mitogenesis. Toxicon 42, 769–776.PubMedCrossRefGoogle Scholar
  24. Kalafatis, M., 1998. Identification and partial characterization of factor Va heavy chain kinase from human platelets. J. Biol. Chem. 273, 8459–8466.PubMedCrossRefGoogle Scholar
  25. Kalafatis, M., Mann, K.G., 1993. Role of the membrane in the inactivation of factor Va by activated protein C. J. Biol. Chem. 268, 27246–27257.PubMedGoogle Scholar
  26. Kalafatis, M., Rand, M.D., Mann, K.G., 1994. The mechanism of inactivation of human factor V and human factor Va by activated protein C. J. Biol. Chem. 269, 31869–31880.PubMedGoogle Scholar
  27. Kane, W.H., Devore-Carter, D., Ortel, T.L., 1990. Expression and characterization of recombinant human factor V and a mutant lacking a major portion of the connecting region. Biochemistry 29, 6762–6768.PubMedCrossRefGoogle Scholar
  28. Kini, R.M., 2004. Platelet aggregation and exogenous factors from animal sources. Curr. Drug Targets Cardiovasc. Haematol. Disord. 4, 301–325.PubMedCrossRefGoogle Scholar
  29. Kini, R.M., Chow, G., 2001. Exogenous inhibitors of platelet aggregation from animal sources. Thromb. Haemost. 85, 179–181.PubMedGoogle Scholar
  30. Kini, R.M., Evans, H.J., 1990. Effects of snake venom proteins on blood platelets. Toxicon 28, 1387–1422.PubMedCrossRefGoogle Scholar
  31. Kini, R.M., Morita, T., Rosing, J., 2001a. Classification and nomenclature of prothrombin activators isolated from snake venoms. Thromb. Haemost. 86, 710–711.Google Scholar
  32. Kini, R.M., Rao, V.S., Joseph, J.S., 2001b. Procoagulant proteins from snake venoms. Haemostasis 31, 218–224.PubMedGoogle Scholar
  33. Kornalik, F., Blomback, B., 1975. Prothrombin activation induced by Ecarin – a prothrombin converting enzyme from Echis carinatus venom. Thromb. Res. 6, 57–63.PubMedCrossRefGoogle Scholar
  34. Kwong, S., Woods, A.E., Mirtschin, P.J., Ge, R., Kini, R.M., 2009. The recruitment of blood coagulation factor X into snake venom gland as a toxin: the role of promoter cis-elements in its expression. Thromb. Haemost. 102, 469–478.PubMedGoogle Scholar
  35. Lavin, M.F., Masci, P.P., 2009. Prothrombinase complexes with different physiological roles. Thromb. Haemost. 102, 421–423.PubMedGoogle Scholar
  36. Mann, K.G., Hockin, M.F., Begin, K.J., Kalafatis, M., 1997. Activated protein C cleavage of factor Va leads to dissociation of the A2 domain. J. Biol. Chem. 272, 20678–20683.PubMedCrossRefGoogle Scholar
  37. Markland, F.S., Jr., 1997. Snake venoms. Drugs 54(Suppl3), 1–10.PubMedCrossRefGoogle Scholar
  38. Markland, F.S., 1998. Snake venoms and the hemostatic system. Toxicon 36, 1749–1800.PubMedCrossRefGoogle Scholar
  39. Marshall, L.R., Herrmann, R.P., 1983. Coagulant and anticoagulant actions of Australian snake venoms. Thromb. Haemost. 50, 707–711.PubMedGoogle Scholar
  40. McMullen, B.A., Fujikawa, K., Kisiel, W., Sasagawa, T., Howald, W.N., Kwa, E.Y., Weinstein, B., 1983. Complete amino acid sequence of the light chain of human blood coagulation factor X: evidence for identification of residue 63 as beta-hydroxyaspartic acid. Biochemistry 22, 2875–2884.PubMedCrossRefGoogle Scholar
  41. Minh, L.T., Reza, M.A., Swarup, S., Kini, R.M., 2005. Gene duplication of coagulation factor V and origin of venom prothrombin activator in Pseudonaja textilis snake. Thromb. Haemost. 93, 420–429.Google Scholar
  42. Morita, T., 2004. C-type lectin-related proteins from snake venoms. Curr. Drug Targets Cardiovasc. Haematol. Disord. 4, 357–373.PubMedCrossRefGoogle Scholar
  43. Morita, T., Iwanaga, S., 1978. Purification and properties of prothrombin activator from the venom of Echis carinatus. J. Biochem. (Tokyo) 83, 559–570.Google Scholar
  44. Nesheim, M.E., Canfield, W.M., Kisiel, W., Mann, K.G., 1982. Studies of the capacity of factor Xa to protect factor Va from inactivation by activated protein C. J. Biol. Chem. 257, 1443–1447.PubMedGoogle Scholar
  45. Nesheim, M.E., Taswell, J.B., Mann, K.G., 1979. The contribution of bovine factor V and factor Va to the activity of prothrombinase. J. Biol. Chem. 254, 10952–10962.PubMedGoogle Scholar
  46. Nicolaes, G.A., Tans, G., Thomassen, M.C., Hemker, H.C., Pabinger, I., Varadi, K., Schwarz, H.P., Rosing, J., 1995. Peptide bond cleavages and loss of functional activity during inactivation of factor Va and factor VaR506Q by activated protein C. J. Biol. Chem. 270, 21158–21166.PubMedCrossRefGoogle Scholar
  47. St. Pierre, L., Masci, P.P., Filippovich, I., Sorokina, N., Marsh, N., Miller, D.J., Lavin, M.F., 2005. Comparative analysis of prothrombin activators from the venom of Australian elapids. Mol. Biol. Evol. 22, 1853–1864.CrossRefGoogle Scholar
  48. Pittman, D.D., Tomkinson, K.N., Michnick, D., Selighsohn, U., Kaufman, R.J., 1994. Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry 33, 6952–6959.PubMedCrossRefGoogle Scholar
  49. Rao, V.S., Joseph, J.S., Kini, R.M., 2003a. Group D prothrombin activators from snake venom are structural homologues of mammalian blood coagulation factor Xa. Biochem. J. 369, 635–642.PubMedCrossRefGoogle Scholar
  50. Rao, V.S., Kini, R.M., 2002. Pseutarin C, a prothrombin activator from Pseudonaja textilis venom: its structural and functional similarity to mammalian coagulation factor Xa-Va complex. Thromb. Haemost. 88, 611–619.PubMedGoogle Scholar
  51. Rao, V.S., Swarup, S., Kini, R.M., 2003b. The non-enzymatic subunit of pseutarin C, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom, shows structural similarity to mammalian coagulation factor V. Blood 102, 1347–1354.PubMedCrossRefGoogle Scholar
  52. Rao, V.S., Swarup, S., Kini, R.M., 2004. The catalytic subunit of pseutarin C, a group C prothrombin activator from the venom of Pseudonaja textilis, is structurally similar to mammalian blood coagulation factor Xa. Thromb. Haemost. 92, 509–521.PubMedGoogle Scholar
  53. Reza, M.A., Minh, L.T., Swarup, S., Kini, R.M., 2006. Molecular evolution caught in action: gene duplication and evolution of molecular isoforms of prothrombin activators in Pseudonaja textilis (brown snake). J. Thromb. Haemost. 4, 1346–1353.PubMedCrossRefGoogle Scholar
  54. Reza, M.A., Swarup, S., Kini, R.M., 2005. Two parallel prothrombin activator systems in Australian rough-scaled snake, Tropidechis carinatus. Structural comparison of venom prothrombin activator with blood coagulation factor X. Thromb. Haemost. 93, 40–47.PubMedGoogle Scholar
  55. Reza, M.A., Swarup, S., Kini, R.M., 2007. Structure of two genes encoding parallel prothrombin activators in Tropidechis carinatus snake: gene duplication and recruitment of factor X gene to the venom gland. J. Thromb. Haemost. 5, 117–126.PubMedCrossRefGoogle Scholar
  56. Rosing, J., Tans, G., 1991. Inventory of exogenous prothrombin activators. For the subcommittee on nomenclature of exogenous hemostatic factors of the scientific and standardization committee of the international society on thrombosis and haemostasis. Thromb. Haemost. 65, 627–630.PubMedGoogle Scholar
  57. Rosing, J., Tans, G., 1992. Structural and functional properties of snake venom prothrombin activators. Toxicon 30, 1515–1527.PubMedCrossRefGoogle Scholar
  58. Schieck, A., Habermann, E., Kornalik, F., 1972. The prothrombin-activating principle from Echis carinatus venom. II. Coagulation studies in vitro and in vivo. Naunyn Schmiedebergs Arch. Pharmacol. 274, 7–17.PubMedCrossRefGoogle Scholar
  59. Silva, M.B., Schattner, M., Ramos, C.R., Junqueira-de-Azevedo, I.L., Guarnieri, M.C., Lazzari, M.A., Sampaio, C.A., 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
  60. Speijer, H., Govers-Riemslag, J.W., Zwaal, R.F., Rosing, J., 1986. Prothrombin activation by an activator from the venom of Oxyuranus scutellatus (Taipan snake). J. Biol. Chem. 261, 13258–13267.PubMedGoogle Scholar
  61. Stenflo, J., Lundwall, A., Dahlback, B., 1987. beta-Hydroxyasparagine in domains homologous to the epidermal growth factor precursor in vitamin K-dependent protein S. Proc. Natl. Acad. Sci. U.S.A. 84, 368–372.PubMedCrossRefGoogle Scholar
  62. Stocker, K., Hauer, H., Muller, C., Triplett, D.A., 1994. Isolation and characterization of Textarin, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom. Toxicon 32, 1227–1236.PubMedCrossRefGoogle Scholar
  63. Suzuki, K., Dahlback, B., Stenflo, J., 1982. Thrombin-catalyzed activation of human coagulation factor V. J. Biol. Chem. 257, 6556–6564.PubMedGoogle Scholar
  64. Tamiya, T., Fujimi, T.J., 2006. Molecular evolution of toxin genes in Elapidae snakes. Mol. Divers. 10, 529–543.PubMedCrossRefGoogle Scholar
  65. Tans, G., Govers-Riemslag, J.W., van Rijn, J.L., Rosing, J., 1985. Purification and properties of a prothrombin activator from the venom of Notechis scutatus scutatus. J. Biol. Chem. 260, 9366–9372.PubMedGoogle Scholar
  66. Thorelli, E., Kaufman, R.J., Dahlback, B., 1997. Cleavage requirements for activation of factor V by factor Xa. Eur. J. Biochem. 247, 12–20.PubMedCrossRefGoogle Scholar
  67. van der Neut, K.M., Dirven, R.J., Vos, H.L., Tans, G., Rosing, J., Bertina, R.M., 2004. Factor Va is inactivated by activated protein C in the absence of cleavage sites at Arg-306, Arg-506, and Arg-679. J. Biol. Chem. 279, 6567–6575.Google Scholar
  68. van Drunen, C.M., Oosterling, R.W., Keultjes, G.M., Weisbeek, P.J., van Driel, R., Smeekens, S.C., 1997. Analysis of the chromatin domain organisation around the plastocyanin gene reveals an MAR-specific sequence element in Arabidopsis thaliana. Nucl. Acids Res. 25, 3904–3911.PubMedCrossRefGoogle Scholar
  69. Wang, C., Eufemi, M., Turano, C., Giartosio, A., 1996. Influence of the carbohydrate moiety on the stability of glycoproteins. Biochemistry 35, 7299–7307.PubMedCrossRefGoogle Scholar
  70. Wilberding, J.A., Castellino, F.J., 2000. Characterization of the murine coagulation factor X promoter. Thromb. Haemost. 84, 1031–1038.PubMedGoogle Scholar
  71. Xu, M., Hammer, R.E., Blasquez, V.C., Jones, S.L., Garrard, W.T., 1989. Immunoglobulin kappa gene expression after stable integration. II. Role of the intronic MAR and enhancer in transgenic mice. J. Biol. Chem. 264, 21190–21195.PubMedGoogle Scholar
  72. Yamada, D., Morita, T., 1997. Purification and characterization of a Ca2+-dependent prothrombin activator, multactivase, from the venom of Echis multisquamatus. J. Biochem. (Tokyo) 122, 991–997.CrossRefGoogle Scholar
  73. Yamada, D., Sekiya, F., Morita, T., 1996. Isolation and characterization of carinactivase, a novel prothrombin activator in Echis carinatus venom with a unique catalytic mechanism. J. Biol. Chem. 271, 5200–5207.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Genetic Engineering and BiotechnologyUniversity of RajshahiRajshahiBangladesh
  2. 2.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  3. 3.Protein Science Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  4. 4.Department of Biochemistry and Molecular BiophysicsMedical College of Virginia, Virginia Commonwealth UniversityRichmondUSA

Personalised recommendations