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BioMed Research International
Volume 2014 (2014), Article ID 595186, 13 pages
http://dx.doi.org/10.1155/2014/595186
Research Article

Isolation and Biochemical Characterization of a New Thrombin-Like Serine Protease from Bothrops pirajai Snake Venom

1Centro de Estudos de Biomoléculas Aplicadas à Saúde, CEBio, Fundação Oswaldo Cruz, Fiocruz Rondônia e Departamento de Medicina, Universidade Federal de Rondônia, UNIR, Rua da Beira 7176, Bairro Lagoa, 76812-245 Porto Velho, RO, Brazil
2Departmento de Biologia Celular e Molecular, Instituto de Biologia, Universidade Federal Fluminense, 24210-130 Niteroi, RJ, Brazil
3Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, 09210-170 Santo André, SP, Brazil
4Escola de Artes, Ciências e Humanidades, USP, 03828-000 São Paulo, SP, Brazil
5Universidade Federal de São João Del Rei, UFSJ, Campus Alto Paraopeba, 36420-000 Ouro Branco, MG, Brazil
6Institute for Research in Biomedicine (IRB Barcelona), 08028 Barcelona, Spain
7CIBER-BBN, Barcelona Science Park, 08028 Barcelona, Spain
8Proteomic Platform, Barcelona Science Park, 08028 Barcelona, Spain
9Department of Organic Chemistry, University of Barcelona, 08028 Barcelona, Spain
10School of Chemistry, University of KwaZulu Natal, Durban 4001, South Africa

Received 9 July 2013; Revised 20 September 2013; Accepted 1 December 2013; Published 26 February 2014

Academic Editor: Edward G. Rowan

Copyright © 2014 Kayena D. Zaqueo 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. 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
  2. T. Matsui, Y. Fujimura, and K. Titani, “Snake venom proteases affecting hemostasis and thrombosis,” Biochimica et Biophysica Acta, vol. 1477, no. 1-2, pp. 146–156, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. S. M. T. Serrano and R. C. Maroun, “Snake venom serine proteinases: sequence homology versus 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
  4. J. A. F. P. Villar, F. T. D. Lima, C. L. Veber et al., “Synthesis and evaluation of nitrostyrene derivative compounds, new snake venom phospholipase A2 inhibitors,” Toxicon, vol. 51, no. 8, pp. 1467–1478, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. D. O. Costa, K. C. Fonseca, M. S. Garrote-Filho et al., “Structural and functional comparison of proteolytic enzymes from plant latex and snake venoms,” Biochimie, vol. 92, no. 12, pp. 1760–1765, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. J. D. O. Costa, K. C. Fonseca, C. C. Neves Mamede et al., “Bhalternin: functional and structural characterization of a new thrombin-like enzyme from Bothrops alternatus snake venom,” Toxicon, vol. 55, no. 7, pp. 1365–1377, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Longo, F. M. L. G. Stamato, R. Ferreira, and O. Tapia, “The catalytic mechanism of serine proteases II: the effect of the protein environment in the α-chymotrypsin proton relay system,” Journal of Theoretical Biology, vol. 112, no. 4, pp. 783–798, 1985. View at Google Scholar · View at Scopus
  8. S. Braud, C. Bon, and A. Wisner, “Snake venom proteins acting on hemostasis,” Biochimie, vol. 82, no. 9-10, pp. 851–859, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. 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
  10. D. E. Vivas-Ruiz, G. A. Sandoval, J. Mendoza et al., “Coagulant thrombin-like enzyme (barnettobin) from Bothrops barnetti venom: molecular sequence analysis of its cDNA and biochemical properties,” Biochimie, vol. 95, no. 494, pp. 1476–1486, 2013. View at Google Scholar
  11. A. K. Mukherjee and S. P. Mackessy, “Biochemical and pharmacological properties of a new thrombin-like serine protease (Russelobin) from the venom of Russell's Viper (Daboia russelii russelii) and assessment of its therapeutic potential,” Biochimica et Biophysica Acta, vol. 1830, no. 495, pp. 3476–3488, 2013. View at Google Scholar
  12. S. S. Tang, X. H. Wang, J. H. Zhang et al., “Biochemical properties and comparative pharmacology of a coagulant from Deinagkistrodon acutus snake venom,” European Journal of Pharmaceutical Sciences, vol. 49, no. 496, pp. 90–98, 2013. View at Google Scholar
  13. Y. Zheng, F. P. Ye, J. Wang et al., “Purification, characterization and gene cloning of Da-36, a novel serine protease from Deinagkistrodon acutus venom,” Toxicon, vol. 67, no. 497, pp. 1–11, 2013. View at Google Scholar
  14. L. C. Mancuso, M. M. Correa, C. A. Vieira et al., “Fractionation of Bothrops pirajai snake venom: isolation and characterization of piratoxin-I, a new myotoxic protein,” Toxicon, vol. 33, no. 5, pp. 615–626, 1995. View at Publisher · View at Google Scholar · View at Scopus
  15. M. H. Toyama, L. C. Mancuso, J. R. Giglio, J. C. Novello, B. Oliveira, and S. Marangoni, “A quick procedure for the isolation of dimeric piratoxins-I and II, two myotoxins from Bothrops pirajai snake venom. N-terminal sequencing,” Biochemistry and Molecular Biology International, vol. 37, no. 6, pp. 1047–1055, 1995. View at Google Scholar · View at Scopus
  16. M. H. Toyama, P. D. Costa, J. C. Novello et al., “Purification and amino acid sequence of MP-III 4R D49 phospholipase A2 from Bothrops pirajai snake venom, a toxin with moderate PLA2 and anticoagulant activities and high myotoxic activity,” Protein Journal, vol. 18, no. 3, pp. 371–378, 1999. View at Google Scholar · View at Scopus
  17. S. S. Teixeira, L. B. Silveira, F. M. N. da Silva et al., “Molecular characterization of an acidic phospholipase A2 from Bothrops pirajai snake venom: synthetic C-terminal peptide identifies its antiplatelet region,” Archives of Toxicology, vol. 85, no. 10, pp. 1219–1233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Havt, M. H. Toyama, N. R. F. Do Nascimento et al., “A new C-type animal lectin isolated from Bothrops pirajai is responsible for the snake venom major effects in the isolated kidney,” International Journal of Biochemistry and Cell Biology, vol. 37, no. 1, pp. 130–141, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. L. F. M. Izidoro, M. C. Ribeiro, G. R. L. Souza et al., “Biochemical and functional characterization of an l-amino acid oxidase isolated from Bothrops pirajai snake venom,” Bioorganic and Medicinal Chemistry, vol. 14, no. 20, pp. 7034–7043, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. D. L. Menaldo, C. P. Bernardes, N. A. Santos-Filho et al., “Biochemical characterization and comparative analysis of two distinct serine proteases from Bothrops pirajai snake venom,” Biochimie, vol. 94, no. 613, pp. 2545–2558, 2012. View at Google Scholar
  21. U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, pp. 680–685, 1970. View at Publisher · View at Google Scholar · View at Scopus
  22. R. D. G. 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 Google Scholar · View at Scopus
  23. A. M. Chudzinski-Tavassi and J. C. A. Modesto, “Venenos de serpentes e suas ações nos mecanismos de coagulação e fibrinólise,” in Métodos em Toxinologia: Toxinas de Serpentes, H. S. Selistre-de-Araújo and D. H. F. Souza, Eds., pp. 11–23, EDUFSCar, São Carlos, Brazil, 2007. View at Google Scholar
  24. L. Romero, S. Marcussi, D. P. Marchi-Salvador et al., “Enzymatic and structural characterization of a basic phospholipase A2 from the sea anemone Condylactis gigantea,” Biochimie, vol. 92, no. 8, pp. 1063–1071, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. S. L. Da Silva, C. A. Dias-Junior, P. A. Baldasso et al., “Vascular effects and electrolyte homeostasis of the natriuretic peptide isolated from Crotalus oreganus abyssus (North American Grand Canyon rattlesnake) venom,” Peptides, vol. 36, no. 501, pp. 206–212, 2012. View at Google Scholar
  26. A. L. Fuly, O. L. T. Machado, E. W. Alves, and C. R. Carlini, “Mechanism of inhibitory action on platelet activation of a phospholipase A2 isolated from Lachesis muta (Bushmaster) snake venom,” Thrombosis and Haemostasis, vol. 78, no. 5, pp. 1372–1380, 1997. View at Google Scholar · View at Scopus
  27. M. R. Cominetti, C. L. S. Pontes, and D. H. F. Souza, “Métodos cromatográficos e critério de pureza,” in Métodos em Toxinologia: Toxinas de Serpentes, H. S. Selistre-de-Araújo and D. H. F. Souza, Eds., pp. 11–23, EDUFSCar, São Carlos, Brazil, 2007. View at Google Scholar
  28. C. Chothia and A. M. Lesk, “The relation between the divergence of sequence and structure in proteins,” The EMBO Journal, vol. 5, no. 4, pp. 823–826, 1986. View at Google Scholar · View at Scopus
  29. L. Holm and C. Sander, “Protein structure comparison by alignment of distance matrices,” Journal of Molecular Biology, vol. 233, no. 1, pp. 123–138, 1993. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Holm and C. Sander, “Dali: a network tool for protein structure comparison,” Trends in Biochemical Sciences, vol. 20, no. 11, pp. 478–480, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Söding, A. Biegert, and A. N. Lupas, “The HHpred interactive server for protein homology detection and structure prediction,” Nucleic Acids Research, vol. 33, no. 2, pp. W244–W248, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Zeng, B. Shen, Z. Zhu et al., “Crystal structure and activating effect on RyRs of AhV_TL-I, a glycosylated thrombin-like enzyme from Agkistrodon halys snake venom,” Archives of Toxicology, vol. 87, no. 647, pp. 535–545, 2013. View at Google Scholar
  33. N. Blom, T. Sicheritz-Pontén, R. Gupta, S. Gammeltoft, and S. Brunak, “Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence,” Proteomics, vol. 4, no. 6, pp. 1633–1649, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. H. J. C. Berendsen, D. van der Spoel, and R. van Drunen, “GROMACS: a message-passing parallel molecular dynamics implementation,” Computer Physics Communications, vol. 91, no. 1–3, pp. 43–56, 1995. View at Google Scholar · View at Scopus
  35. E. Lindahl, B. Hess, and D. van der Spoel, “GROMACS 3.0: a package for molecular simulation and trajectory analysis,” Journal of Molecular Modeling, vol. 7, no. 8, pp. 306–317, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. W. F. Van Gunsteren, S. R. Billeter, A. A. Eising et al., “Biomolecular simulations: the GROMOS96 manual and user guide,” VdF Hochschulverlag ETHZ, vol. 648, 1996. View at Google Scholar
  37. S. C. Lovell, I. W. Davis, W. B. Arendall III et al., “Structure validation by Calpha geometry: phi, psi and Cbeta deviation,” Proteins, vol. 50, pp. 437–450, 2003. View at Google Scholar
  38. J. U. Bowie, R. Luthy, and D. Eisenberg, “A method to identify protein sequences that fold into a known three-dimensional structure,” Science, vol. 253, pp. 164–170, 1991. View at Google Scholar · View at Scopus
  39. R. Luthy, J. U. Bowie, and D. Eisenberg, “Assesment of protein models with three-dimensional profiles,” Nature, vol. 356, pp. 83–85, 1992. View at Publisher · View at Google Scholar · View at Scopus
  40. M. J. Sippl, “Recognition of errors in three-dimensional structures of proteins,” Proteins: Structure, Function and Genetics, vol. 17, no. 4, pp. 355–362, 1993. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Wiederstein and M. J. Sippl, “ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins,” Nucleic Acids Research, vol. 35, pp. W407–W410, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Pirkle, “Thrombin-like enzymes from snake venoms: an updated inventory,” Thrombosis and Haemostasis, vol. 79, no. 3, pp. 675–683, 1998. View at Google Scholar · View at Scopus
  43. S. Swenson and F. S. Markland Jr., “Snake venom fibrin(ogen)olytic enzymes,” Toxicon, vol. 45, no. 8, pp. 1021–1039, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. J. O. Costa, C. B. Petri, A. Hamaguchi et al., “Purification and functional characterization of two fibrinogenolytic enzymes from Bothrops alternatus venom,” Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 13, no. 3, pp. 640–654, 2007. View at Google Scholar · View at Scopus
  45. Y.-S. Koh, K.-H. Chung, and D.-S. Kim, “Biochemical characterization of a thrombin-like enzyme and a fibrinolytic serine protease from snake (Agkistrodon saxatilis) venom,” Toxicon, vol. 39, no. 4, pp. 555–560, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. 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, vol. 146, no. 4, pp. 565–575, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. L. A. Ponce-Soto, V. L. Bonfim, J. C. Novello, R. Navarro Oviedo, A. Yarlequé Chocas, and S. Marangoni, “Isolation and characterization of a serine protease, Ba III-4, from Peruvian Bothrops atrox venom,” Protein Journal, vol. 26, no. 6, pp. 387–394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. C. D. Sant' Ana, F. K. Ticli, L. L. Oliveira et al., “BjussuSP-I: a new thrombin-like enzyme isolated from Bothrops jararacussu snake venom,” Comparative Biochemistry and Physiology, vol. 151, no. 3, pp. 443–454, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. 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
  50. A. Vilca-Quispe, L. A. Ponce-Soto, F. V. Winck, and S. Marangoni, “Isolation and characterization of a new serine protease with thrombin-like activity (TLBm) from the venom of the snake Bothrops marajoensis,” Toxicon, vol. 55, no. 4, pp. 745–753, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Magalhaes, G. J. De Oliveira, and C. R. Diniz, “Purification and partial characterization of a thrombin-like enzyme from the venom of the bushmaster snake, Lachesis muta noctivaga,” Toxicon, vol. 19, no. 2, pp. 279–294, 1981. View at Google Scholar · View at Scopus
  52. F. S. Markland and P. S. Damus, “Purification and properties of a thrombin-like enzyme from the venom of Crotalus adamanteus (Eastern diamondback rattlesnake),” Journal of Biological Chemistry, vol. 246, no. 21, pp. 6460–6473, 1971. View at Google Scholar · View at Scopus
  53. H. S. Selistre and J. R. Giglio, “Isolation and characterization of a thrombin-like enzyme from the venom of the snake Bothrops insularis (jararaca ilhoa),” Toxicon, vol. 25, no. 11, pp. 1135–1144, 1987. View at Google Scholar · View at Scopus
  54. K. Stocker and G. H. Barlow, “The coagulant enzyme from Bothrops atrox venom (batroxobin),” Methods in Enzymology, vol. 45, pp. 214–223, 1976. View at Publisher · View at Google Scholar · View at Scopus
  55. S. M. T. Serrano, R. Mentele, C. A. M. Sampaio, and E. Fink, “Purification, characterization, and amino acid sequence of a serine proteinase PA-BJ, with platelet-aggregating activity from the venom of Bothrops jararaca,” Biochemistry, vol. 34, no. 21, pp. 7186–7193, 1995. View at Google Scholar · View at Scopus
  56. D. F. Vieira, L. Watanabe, C. D. Sant'Ana et al., “Purification and characterization of jararassin-I, a thrombin-like enzyme from Bothrops jararaca snake venom,” Acta Biochimica et Biophysica Sinica, vol. 36, no. 12, pp. 798–802, 2004. View at Google Scholar · View at Scopus
  57. L. Muszbek, V. C. Yee, and Z. Hevessy, “Blood coagulation factor XIII: structure and function,” Thrombosis Research, vol. 94, no. 5, pp. 271–305, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Adany, “Intracellular factor XIII: cellular distribution of factor XIII subunit a in humans,” Seminars in Thrombosis and Hemostasis, vol. 22, no. 5, pp. 399–408, 1996. View at Google Scholar · View at Scopus
  59. S. I. Rapaport, “The initiation of the tissue factor dependent pathway of blood coagulation,” Advances in Experimental Medicine and Biology, vol. 281, pp. 97–103, 1991. View at Google Scholar · View at Scopus
  60. R. Bezerra and L. B. Carvalho, “Proteases no trato digestivo de Peixes,” Biotecnologia Ciência & Desenvolvimento, vol. 622, pp. 46–49, 2001. View at Google Scholar
  61. S. Niewiarowski, E. P. Kirby, T. M. Brudzynski, and K. Stocker, “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 Google Scholar
  62. F. S. Markland, “Snake venoms and the hemostatic system,” Toxicon, vol. 36, no. 12, pp. 1749–1800, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Ouyang, C.-M. Teng, and T.-F. Huang, “Characterization of snake venom components acting on blood coagulation and platelet function,” Toxicon, vol. 30, no. 9, pp. 945–966, 1992. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Martins-Silva, J. Carvalho de Sousa, C. Saldanha, and J. Martins-Silva, in Fibrinogen: From Physiopathology to Clinics, C. Perdigão, Ed., pp. 13–26, 1996.
  65. N. Marsh and V. Williams, “Practical applications of snake venom toxins in haemostasis,” Toxicon, vol. 45, no. 8, pp. 1171–1181, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. W. R. Bell, “Clinical trials with ancrod,” in Hemostasis and Animal Venoms, H. Pirkle and F. S. Markland Jr., Eds., pp. 541–551, Marcel Dekker, New York, 1988. View at Google Scholar
  67. K. Stocker and J. Meier, “Thrombin-like snake-venom enzymes,” Thrombosis and Haemostasis, vol. 54, pp. 313–313, 1985. View at Google Scholar
  68. C. Demers, J. S. Ginsberg, P. Brill-Edwards et al., “Rapid anticoagulation using ancrod for heparin-induced thrombocytopenia,” Blood, vol. 78, no. 9, pp. 2194–2197, 1991. View at Google Scholar · View at Scopus
  69. J. G. Kelton, J. W. Smith, D. Moffatt, A. Santos, and P. Horsewood, “The interaction of ancrod with human platelets,” Platelets, vol. 10, no. 1, pp. 24–29, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Bacila, “Gyroxin, a new neurotoxin of Crotalus durissus terrificus venom,” Acta Physiologica Latinoamericana, vol. 11, p. 224, 1961. View at Google Scholar
  71. G. Alexander, J. Grothusen, H. Zepeda, and R. J. Schwartzman, “Gyroxin, a toxin from the venom of Crotalus durissus terrificus, is a thrombin-like enzyme,” Toxicon, vol. 26, no. 10, pp. 953–960, 1988. View at Google Scholar · View at Scopus
  72. W. H. Dascombe, G. Dumanian, C. Hong et al., “Application of thrombin based fibrin glue and non-thrombin based batroxobin glue on intact human blood vessels: evidence for transmural thrombin activity,” Thrombosis and Haemostasis, vol. 78, no. 2, pp. 947–951, 1997. View at Google Scholar · View at Scopus
  73. L. C. Barros, R. S. Ferreira Jr., S. R. C. S. Barraviera et al., “A new fibrin sealant from Crotalus durissus terrificus venom: applications in medicine,” Journal of Toxicology and Environmental Health B, vol. 12, no. 8, pp. 553–571, 2009. View at Publisher · View at Google Scholar · View at Scopus