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BioMed Research International
Volume 2013 (2013), Article ID 903292, 12 pages
http://dx.doi.org/10.1155/2013/903292
Research Article

Rapid Purification and Procoagulant and Platelet Aggregating Activities of Rhombeobin: A Thrombin-Like/Gyroxin-Like Enzyme from Lachesis muta rhombeata Snake Venom

1Department of Biochemistry, Institute of Biology, University of Campinas (UNICAMP), P.O. Box 6109, 13083-970 Campinas, SP, Brazil
2Department of Structural and Functional Biology, Institute of Biology, State University of Campinas (UNICAMP), P.O. Box 6109, 13083-865 Campinas, SP, Brazil
3Department of Pharmacology, State University of Campinas (UNICAMP), P.O. Box 6109, 13083-887 Campinas, SP, Brazil

Received 4 June 2013; Accepted 29 June 2013

Academic Editor: Saulo Luís da Silva

Copyright © 2013 Frank Denis Torres-Huaco et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. R. Zamudio and H. W. Greene, “Phylogeography of the bushmaster (Lachesis muta: Viperidae): implications for neotropical biogeography, systematics, and conservation,” Biological Journal of the Linnean Society, vol. 62, no. 3, pp. 421–442, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. M. T. Jorge, I. S. Sano-Martins, S. C. Tomy et al., “Snakebite by the bushmaster (Lachesis muta) in Brazil: case report and review of the literature,” Toxicon, vol. 35, no. 4, pp. 545–554, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Rucavado, E. Flores-Sanchéz, A. Franceschi, A. Magalhaes, and J. M. Gutiérrez, “Characterization of the local tissue damage induced by LHF-II, a metalloproteinase with weak hemorrhagic activity isolated from Lachesis muta muta snake venom,” Toxicon, vol. 37, no. 9, pp. 1297–1312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. Ministerio da Saúde do Brasil—Fundação Nacional de Saúde, Manual de Diagnóstico e Tratamento de Acidentes por Animais Peçonhentos, Federal District, Brazil, 2001.
  5. D. C. Damico, L. G. Bueno, L. Rodrigues-Simioni, S. Marangoni, M. A. da Cruz-Höfling, and J. C. Novello, “Neurotoxic and myotoxic actions from Lachesis muta muta (surucucu) whole venom on the mouse and chick nerve-muscle preparations,” Toxicon, vol. 46, no. 2, pp. 222–229, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Otero, M. F. Furtado, C. Gonçalves et al., “Comparative study of the venoms of three subspecies of Lachesis muta (bushmaster) from Brazil, Colombia and Costa Rica,” Toxicon, vol. 36, no. 12, pp. 2021–2027, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Barrett and N. D. Rawlings, “Families and clans of serine peptidases,” Archives of Biochemistry and Biophysics, vol. 318, no. 2, pp. 247–250, 1995. View at Publisher · View at Google Scholar · View at Scopus
  8. S. M. Serrano and R. C. Maroun, “Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved,” Toxicon, vol. 45, no. 8, pp. 1115–1132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Aguiar, C. R. Alves, A. Melgarejo, and S. Giovanni-de-Simone, “Purification and partial characterization of a thrombin-like/gyroxin enzyme from bushmaster (Lachesis muta rhombeata) venom,” Toxicon, vol. 34, no. 5, pp. 555–565, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Giovanni-de-Simone, A. S. Aguiar, A. R. Gimenez, K. Novellino, and R. S. de Moura, “Purification, properties, and N-terminal amino acid sequence of a kallikrein-like enzyme from the venom of Lachesis muta rhombeata (bushmaster),” Journal of Protein Chemistry, vol. 16, no. 8, pp. 809–818, 1997. View at Scopus
  11. H. Pirkle and N. Marsh, “Nomenclature of exogenous hemostatic factors,” Toxicon, vol. 30, no. 12, pp. 1513–1514, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Magalhães, B. C. da Fonseca, C. R. Diniz, J. Gilroy, and M. Richardson, “The complete amino acid sequence of a thrombin-like enzyme/gyroxin analogue from venom of the bushmaster snake (Lachesis muta muta),” FEBS Letters, vol. 29, no. 1-2, pp. 116–120, 1993. View at Publisher · View at Google Scholar · View at Scopus
  13. C. M. Yonamine, A. R. Prieto-da-Silva, G. S. Magalhaes et al., “Cloning of serine protease cDNAs from Crotalus durissus terrificus venom gland and expression of a functional gyroxin homologue in COS-7 cells,” Toxicon, vol. 54, no. 2, pp. 110–120, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. S. G. de-Simone, C. Correa-Netto, O. A. Antunes, R. B. de-Alencastro, and F. P. Silva Jr., “Biochemical and molecular modeling analysis of the ability of two p-aminobenzamidine-based sorbents to selectively purify serine proteases (fibrinogenases) from snake venoms,” Journal of Chromatography B, vol. 822, no. 1-2, pp. 1–9, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Nikai, A. Ohara, Y. Komori, J. W. Fox, and H. Sugihara, “Primary structure of a coagulant enzyme, bilineobin, from Agkistrodon bilineatus venom,” Archives of Biochemistry and Biophysics, vol. 318, no. 1, pp. 89–96, 1995. View at Publisher · View at Google Scholar · View at Scopus
  16. C. D. Sant'Ana, C. P. Bernardes, L. F. M. Izidoro et al., “Molecular characterization of BjussuSP-I, a new thrombin-like enzyme with procoagulant and kallikrein-like activity isolated from Bothrops jararacussu snake venom,” Biochimie, vol. 90, no. 3, pp. 500–507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Itoh, N. Tanaka, I. Funakoshi, T. Kawasaki, S. Mihashi, and I. Yamashina, “Organization of the gene for batroxobin, a thrombin-like snake venom enzyme. Homology with the trypsin/kallikrein gene family,” The Journal of Biological Chemistry, vol. 263, no. 16, pp. 7628–7631, 1988. View at Scopus
  18. Y. M. Wang, S. R. Wang, and I. H. Tsai, “Serine protease isoforms of Deinagkistrodon acutus venom: cloning, sequencing and phylogenetic analysis,” Biochemical Journal, vol. 354, no. 1, pp. 161–168, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. H. C. Castro, D. M. Silva, C. Craik, and R. B. Zingali, “Structural features of a snake venom thrombin-like enzyme: thrombin and trypsin on a single catalytic platform?” Biochimica et Biophysica Acta, vol. 1547, no. 2, pp. 183–195, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970. View at Publisher · View at Google Scholar · View at Scopus
  21. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Scopus
  22. B. F. Erlanger, N. Kokowsky, and W. Cohen, “The preparation and properties of two new chromogenic substrates of trypsin,” Archives of Biochemistry and Biophysics, vol. 95, no. 2, pp. 271–278, 1961. View at Scopus
  23. R. D. Theakston and H. A. Reid, “Development of simple standard assay procedures for the characterization of snake venoms,” Bulletin of the World Health Organization, vol. 61, no. 6, pp. 949–956, 1983. View at Scopus
  24. D. C. Damico, T. Vassequi-Silva, F. D. Torres-Huaco et al., “LmrTX, a basic PLA2 (D49) purified from Lachesis muta rhombeata snake venom with enzymatic-related antithrombotic and anticoagulant activity,” Toxicon, vol. 60, pp. 773–781, 2012.
  25. C. Seki, J. C. Vidal, and A. Barrio, “Purification of gyroxin from a South American rattlesnake (Crotalus durissus terrificus) venom,” Toxicon, vol. 18, no. 3, pp. 235–247, 1980. View at Scopus
  26. H. Barrabin, J. L. Martiarena, J. C. Vidal, and A. Barrio, “Isolation and characterization of gyroxin from Crotalus durissus terriftcus venom,” in Toxins: Animal, Plant and Microbial, P. Rosenberg, Ed., p. 133, Pergamon, New York, NY, USA, 1978.
  27. S. L. Maruñak, O. C. Acosta, L. C. Leiva, R. M. Ruiz, M. V. Aguirre, and P. Teibler, “Mice plasma fibrinogen consumption by thrombin-like enzyme present in rattlesnake venom from the North-East region of Argentina,” Medicina B, vol. 64, no. 6, pp. 509–517, 2004. View at Scopus
  28. S. Nishida, Y. Fujimura, S. Miura et al., “Purification and characterization of bothrombin, a fibrinogen-clotting serine protease from the venom of Bothrops jararaca,” Biochemistry, vol. 33, no. 7, pp. 1843–1849, 1994. View at Scopus
  29. A. Magalhães, H. P. B. Magalhães, M. Richardson et al., “Purification and properties of a coagulant thrombin-like enzyme from the venom of Bothrops leucurus,” Comparative Biochemistry and Physiology A, vol. 146, no. 4, pp. 565–575, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. S. M. Serrano, C. A. Sampaio, R. Mentele, A. C. Camargo, and E. Fink, “A novel fibrinogen-clotting enzyme, TL-BJ, from the venom of the snake Bothrops jararaca: purification and characterization,” Thrombosis and Haemostasis, vol. 83, no. 3, pp. 438–444, 2008. View at Scopus
  31. J. W. Lee, J. H. Seu, I. K. Rhee, I. Jin, Y. Kawamura, and W. Park, “Purification and characterization of brevinase, a heterogeneous two-chain fibrinolytic enzyme from the venom of Korean snake, Agkistrodon blomhoffii brevicaudus,” Biochemical and Biophysical Research Communications, vol. 260, no. 3, pp. 665–670, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. R. K. Bortoleto, M. T. Murakami, L. Watanabe, A. M. Soares, and R. K. Arni, “Purification, characterization and crystallization of Jararacussin-I, a fibrinogen-clotting enzyme isolated from the venom of Bothrops jararacussu,” Toxicon, vol. 40, no. 9, pp. 1307–1312, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. F. P. Silva-Junior, H. L. Guedes, L. C. Garvey et al., “BJ-48, a novel thrombin-like enzyme from the Bothrops jararacussu venom with high selectivity for Arg over Lys in P1: role of N-glycosylation in thermostability and active site accessibility,” Toxicon, vol. 50, no. 1, pp. 18–31, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Murayama, K. Saguchi, R. Mentele et al., “The unusual high molecular mass of bothrops protease A, a trypsin-like serine peptidase from the venom of Bothrops jararaca, is due to its high carbohydrate content,” Biochimica et Biophysica Acta, vol. 1652, no. 1, pp. 1–6, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Burkhart, G. F. Smith, J. L. Su, I. Parikh, and H. LeVine III, “Amino acid sequence determination of ancrod, the thrombin-like α-fibrinogenase from the venom of Akistrodon rhodostoma,” FEBS Letters, vol. 297, no. 3, pp. 297–301, 1992. View at Publisher · View at Google Scholar · View at Scopus
  36. H. C. Castro, R. B. Zingali, M. G. Albuquerque, M. Pujol-Luz, and C. R. Rodrigues, “Snake venom thrombin-like enzymes: from reptilase to now,” Cellular and Molecular Life Sciences, vol. 61, no. 7-8, pp. 843–856, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. W. Kisiel, “Molecular properties of the factor V-activating enzyme from Russell's viper venom,” The Journal of Biological Chemistry, vol. 254, no. 23, pp. 12230–12234, 1979. View at Scopus
  38. F. Tokunaga, K. Nagasawa, S. Tamura, T. Miyata, S. Iwanaga, and W. Kisiel, “The factor V-activating enzyme (RVV-V) from Russell's viper venom. Identification of isoproteins RVV-V alpha, -V beta, and -V gamma and their complete amino acid sequences,” The Journal of Biological Chemistry, vol. 263, no. 33, pp. 17471–17481, 1988. View at Scopus
  39. E. Siigur, M. Samel, K. Tonismagi, J. Subbi, T. Reintamm, and J. Siigur, “Isolation, properties and N-terminal amino acid sequence of a factor V activator from Vipera lebetina (Levantine viper) snake venom,” Biochimica et Biophysica Acta, vol. 1429, no. 1, pp. 239–248, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Niewiarowski, E. P. Kirby, T. Brudzynski, et al., “Thrombocytin, a serine protease from Bothrops atrox venom. 2. Interaction with platelets and plasma-clotting factors,” Biochemistry, vol. 18, no. 16, pp. 3570–3577, 1979. View at Scopus
  41. N. Marrakchi, R. Barbouche, S. Guermazi, H. Karoui, C. Bon, and M. El Ayeb, “Cerastotin, a serine protease from Cerastes cerastes venom, with platelet-aggregating and agglutinating properties,” European Journal of Biochemistry, vol. 247, no. 1, pp. 121–128, 1997. View at Scopus
  42. G. K. Isbister, “Procoagulant snake toxins: laboratory studies, diagnosis, and understanding snakebite coagulopathy,” Seminars in Thrombosis and Hemostasis, vol. 35, no. 1, pp. 93–103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. J. White, “Snake venoms and coagulopathy,” Toxicon, vol. 45, no. 8, pp. 951–967, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. G. K. Isbister, “Snakebite doesn't cause disseminated intravascular coagulation: coagulopathy and thrombotic microangiopathy in snake envenoming,” Seminars in Thrombosis and Hemostasis, vol. 36, no. 4, pp. 444–451, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. B. F. Santos, S. M. Serrano, A. Kuliopulos, and S. Niewiarowski, “Interaction of viper venom serine peptidases with thrombin receptors on human platelets,” FEBS Letters, vol. 477, no. 3, pp. 199–202, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. M. C. Chang and T. F. Huang, “Characterization of a thrombin-like enzyme, grambin, from the venom of Trimeresurus gramineus and its in vivo antithrombotic effect,” Toxicon, vol. 33, no. 8, pp. 1087–1098, 1995. View at Publisher · View at Google Scholar · View at Scopus