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BioMed Research International
Volume 2013 (2013), Article ID 903292, 12 pages
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.
- 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.
- 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.
- 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.
- Ministerio da Saúde do Brasil—Fundação Nacional de Saúde, Manual de Diagnóstico e Tratamento de Acidentes por Animais Peçonhentos, Federal District, Brazil, 2001.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- H. Pirkle and N. Marsh, “Nomenclature of exogenous hemostatic factors,” Toxicon, vol. 30, no. 12, pp. 1513–1514, 1992.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- J. White, “Snake venoms and coagulopathy,” Toxicon, vol. 45, no. 8, pp. 951–967, 2005.
- 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.
- 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.
- 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.