Purification and characterization of a hemorrhagic metalloproteinase from Bothrops lanceolatus (Fer-de-lance) snake venom

Toxicon

Volumn 45, Issue 4, 2005, Pages 411-420

  Stroka, Alessandra ^a   Donato, José L ^a   Bon, Cassian ^b   Hyslop, Stephen ^a   De Araújo, Albetiza Lôbo ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b INSTITUT PASTEUR   (France)

Author keywords

Bothrops lanceolatus; Hemorrhage; Metalloproteinase; Proteolytic; Snake venom

Indexed keywords

APROTININ; BENZAMIDINE; BENZENE DERIVATIVE; BOTHROP VENOM ANTISERUM; EDETIC ACID; HEMORRHAGIN; MERCAPTOETHANOL; METAL CHELATE; METAL ION; METALLOPROTEINASE; PHOSPHOLIPASE A2; SNAKE VENOM; UNCLASSIFIED DRUG; VENOM ANTISERUM;

ALKALINITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; CHELATION; CHROMATOGRAPHY; COLLAGEN DEGRADATION; CONTROLLED STUDY; ELASTOLYSIS; ENZYME ACTIVITY; FIBRINOGENOLYSIS; GEL FILTRATION; HYDROPHOBICITY; IMMUNOBLOTTING; IMMUNOELECTROPHORESIS; MALE; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; SNAKE; TEMPERATURE;

BOTHROPS; SERPENTES;

EID: 13944263624     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2004.11.010     Document Type: Article

References (75)

1. I. Aguilar, M.E. Giron, and A. Rodriguez-Acosta Purification and characterization of a hemorrhagic fraction from the venom of the Uracoan rattlesnake Crotalus vegrandis Biochim. Biophys. Acta 1548 2001 57 65
2. V.A. Arruda, A.Q. Guimarães, S. Hyslop, P.M. Ferreira de Araújo, C. Bon, and A. Lôbo de Araújo Bothrops lanceolatus (Fer de lance) venom stimulates leukocyte migration into the peritoneal cavity of mice Toxicon 41 2003 99 107
3. M.T. Assakura, A.P. Reichl, C.A. Asperti, and F.R. Mandelbaum Isolation of the major proteolytic enzyme from the snake Bothrops moojeni Toxicon 23 1985 691 706
4. M.T. Assakura, A.P. Reichl, and F.R. Mandelbaum Comparison of immunological, biochemical and biophysical properties of three hemorrhagic factors isolated from the venom of Bothrops jararaca Toxicon 24 1986 943 946
5. M.T. Assakura, C.A. Silva, R. Mentele, A.C. Camargo, and S.M. Serrano Molecular cloning and expression of structural domains of bothropasin, a P-III metalloproteinase from the venom of Bothrops jararaca Toxicon 41 2003 217 227
6. E.N. Baramova, J.D. Shannon, J.B. Bjarnason, and J.W. Fox Degradation of extracellular matrix proteins by hemorrhagic metalloproteinases Arch. Biochem. Biophys. 275 1989 63 71
7. 2- macroglobulin Biochemistry 29 1990 1069 1074
8. 2 from Crotalus durissus cascavella rattlesnake (maracambóia) venom J. Protein Chem. 19 2000 603 607
9. J.B. Bjarnason, and J.W. Fox Hemorrhagic toxins from snake venoms J. Toxicol.-Toxin Rev. 7 1988-89 121 209
10. J.B. Bjarnason, and J.W. Fox Hemorrhagic metalloproteinases from snake venoms Pharmacol. Ther. 62 1994 325 372
11. J.B. Bjarnason, and A.T. Tu Hemorrhagic toxins from western diamondback rattlesnake (Crotalus atrox) venom: isolation and characterization of five toxins and the role of zinc in hemorrhagic toxin Biochemistry 17 1978 3395 3404
12. G. Bogarín, M. Romero, G. Rojas, C. Lutsch, M. Casadamont, J. Lang, R. Otero, and J.M. Gutiérrez Neutralization, by a monospecific Bothrops lanceolatus antivenom, of toxic activities induced by homologous and heterologous Bothrops snake venoms Toxicon 37 1999 551 557
13. T.C. Bog-Hansen Immunoelectrophoresis B.D. Hames D. Rickwood Gel Electrophoresis of Proteins - a Practical Approach 2nd ed. 1990 IRL Press Oxford 273 300
14. G. Borkow, J.M. Gutiérrez, and M. Ovadia Isolation and characterization of synergistic hemorrhagins from the venom of the snake Bothrops asper Toxicon 31 1993 1137 1150
15. B. Bucher, D. Canonge, L. Thomas, B. Tyburn, A. Robbe-Vicent, V. Choumet, C. Bon, J. Ketterlé, and J. Lang Clinical indicators of envenoming and serum levels of venom antigens in patients bitten by Bothrops lanceolatus in Martinique Trans. R. Soc. Trop. Med. Hyg. 9 1997 186 190
16. D.F. Cardoso, I.K. Yamaguchi, and A.M. Moura da Silva Produção de soros antitoxinas e perspectivas de modernização por técnicas de biologia molecular J.L.C. Cardoso F.O.S. França F.H. Wen C.M.S. Málaque V. Haddad Jr Animais Peçonhentos no Brasil: Biologia, Clínica e Terapêutica dos Acidentes 2003 Sarvier São Paulo 367 379
17. S.M. Carneiro, M.T. Assakura, F.A. Barrence, S.R. Cardoso, A.C. de Martins Camargo, and A. Sesso Immunolocalization of venom metalloproteinases in venom glands of adult and of newborn snakes of Bothrops jararaca Tissue Cell 34 2002 381 389
18. P.B. Clissa, G.D. Laing, R.D.G. Theakston, I. Mota, M.J. Taylor, and A.M. Moura-da-Silva The effect of jararhagin, a metalloproteinase from Bothrops jararaca venom, on pro-inflammatory cytokines released by murine peritoneal adherent cells Toxicon 39 2001 1567 1573
19. E.P. Costa, P.B. Clissa, C.F.P. Teixeira, and A.M. Moura-da-Silva Importance of metalloproteinases and macrophages in viper snake envenomation-induced local inflammation Inflammation 26 2002 13 17
20. G.R. Delpierre Studies on African snake venoms - I. The proteolytic activities of some African viperidae venoms Toxicon 5 1968 233 238
21. T. Escalante, J. Núñez, A.M. Moura-da-Silva, A. Rucavado, R.D. Theakston, and J.M. Gutiérrez Pulmonary hemorrhage induced by jararhagin, a metalloproteinase from Bothrops jararaca snake venom Toxicol. Appl. Pharmacol. 193 2003 17 28
22. 2-macroglobulin and mouse serum and does not induce systemic hemorrhage or coagulopathy Toxicon 43 2004 213 217
23. H.W. Fan, and J.L.C. Cardoso Clinical toxicology of snake bites in South America J. Meier J. White Handbook of Clinical Toxicology of Animal Venoms and Poisons 1995 CRC Press Boca Raton 667 688
24. L. Faria, E. Antunes, C. Bon, and A. Lôbo de Araújo Pharmacological characterization of the paw edema induced by Bothrops lanceolatus (Fer de lance) venom Toxicon 39 2001 825 830
25. F.O.S. França, and C.M.S. Málaque Acidente botrópico J.L.C. Cardoso F.O.S. França F.H. Wen C.M.S. Málaque V. Haddad Jr Animais Peçonhentos no Brasil: Biologia, Clínica e Terapêutica dos Acidentes 2003 Sarvier São Paulo 72 86
26. A. Franceschi, A. Rucavado, N. Mora, and J.M. Gutiérrez Purification and characterization of BaH4, a hemorrhagic metalloproteinase from the venom of the snake Bothrops asper Toxicon 38 2000 63 77
27. A.Q. Guimarães, M.A. Cruz-Höfling, P.M. Ferreira de Araújo, C. Bon, and A. Lôbo de Araújo Pharmacological and histopathological characterization of Bothrops lanceolatus (Fer de lance) venom-induced edema Inflamm. Res. 53 2004 284 291
28. J.M. Gutiérrez, and B. Lomonte Local tissue damage induced by Bothrops snake venoms Mem. Inst. Butantan 51 1989 211 223
29. 2 myotoxins from Bothrops snake venoms Toxicon 33 1995 1405 1424
30. J.M. Gutiérrez, and B. Lomonte Efectos locales en el envenenamiento ofídico en América Latina J.L.C. Cardoso F.O.S. França F.H. Wen C.M.S. Málaque V. Haddad Jr Animais Peçonhentos no Brasil: Biologia, Clínica e Terapêutica dos Acidentes 2003 Sarvier São Paulo 310 323
31. J.M. Gutiérrez, and A. Rucavado Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage Biochimie 82 2000 841 845
32. J.M. Gutiérrez, M. Romero, C. Diaz, G. Borkow, and M. Ovadia Isolation and characterization of a metalloproteinase with weak hemorrhagic activity from the venom of the snake Bothrops asper (terciopelo) Toxicon 33 1995 19 29
33. J.M. Gutiérrez, M. Romero, J. Núñez, F. Chavez, G. Borkow, and M. Ovadia Skeletal muscle necrosis and regeneration after injection of BaH1, a hemorrhagic metalloproteinase isolated from the venom of the snake Bothrops asper (terciopelo) Exp. Mol. Pathol. 62 1995 28 41
34. R.A. Harrison, W. Wuster, and R.D. Theakston The conserved structure of snake venom toxins confers extensive immunological cross-reactivity to toxin-specific antibody Toxicon 41 2003 441 449
35. L.G. Jia, K. Shimokawa, J.B. Bjarnason, and J.W. Fox Snake venom metalloproteinases: structure, function and relationship to the ADAMs family of proteins Toxicon 34 1996 1269 1276
36. A.S. Kamiguti, R.D. Theakston, H. Desmond, and R.A. Hutton Systemic haemorrhage in rats induced by a haemorrhagic fraction from Bothrops jararaca venom Toxicon 29 1991 1097 1105
37. A.S. Kamiguti, F.P. Rugman, R.D. Theakston, F.O. França, H. Ishii, and C.R. Hay The role of venom haemorrhagin in spontaneous bleeding in Bothrops jararaca envenoming. Butantan Institute Antivenom Study Group Thromb. Haemost. 67 1992 484 488
38. A.S. Kamiguti, C.R. Hay, R.D.G. Theakston, and M. Zuzel Insights into the mechanism of haemorrhage caused by snake venom metalloproteinases Toxicon 34 1996 627 642
39. A.S. Kamiguti, M. Zuzel, and R.D. Theakston Snake venom metalloproteinases and disintegrins: interactions with cells Braz. J. Med. Biol. Res. 31 1998 853 862
40. J. Kawano, K. Anai, M. Sugiki, E. Yoshida, and M. Maruyama Vascular endothelial cell injury induced by Bothrops jararaca venom; non-significance of hemorrhagic metalloproteinase Toxicon 40 2002 1553 1563
41. O. Khow, L. Chanhome, T. Omori-Satoh, S. Puempunpanich, and V. Sitprija A hemorrhagin as a metalloprotease in the venom of Trimeresurus purpureomaculatus: purification and characterization Toxicon 40 2002 455 461
42. 4 Nature 227 1970 680 685
43. G.D. Laing, P.B. Clissa, R.D. Theakston, A.M. Moura-da-Silva, and M.J. Taylor Inflammatory pathogenesis of snake venom metalloproteinase-induced skin necrosis Eur. J. Immunol. 33 2003 3458 3463
44. A. Leonardi, F. Gubensek, and I. Krizaj Purification and characterization of two hemorrhagic metalloproteinases from the venom of the long-nosed viper, Vipera ammodytes ammodytes Toxicon 40 2001 55 92
45. 2, blood-clotting, caseinolytic and hemorrhagic activities of some Bothrops snake venoms Toxicon 28 1990 601 (abstract)
46. 2 from Bothrops lanceolatus (Fer de lance) venom: molecular and enzymatic properties Toxicon 32 1994 1069 1081
47. A. Lôbo de Araújo, J.L. Donato, and C. Bon Purification from Bothrops lanceolatus (Fer de lance) venom of a fibrino(geno)lytic enzyme with esterolytic activity Toxicon 36 1998 745 758
48. A. Lôbo de Araújo, A.O. Souza, M.A. Cruz-Höfling, C.A. Flores, and C. Bon Bothrops lanceolatus (Fer de lance) venom induces oedema formation and increases vascular permeability in the mouse hind paw Toxicon 38 2000 209 221
49. A. Lôbo de Araújo, A Kamiguti, and C. Bon Coagulant and anticoagulant activities of Bothrops lanceolatus (Fer de lance) venom Toxicon 39 2001 371 375
50. J.L. Lopez-Lozano, M.V. de Sousa, C.A. Ricart, C. Chávez- Olórtegui, E.F. Sanchez, E.G. Muniz, P.F. Buhrnheim, and L. Morhy Ontogenetic variation of metalloproteinases and plasma coagulant activity in venoms of wild Bothrops atrox specimens from Amazonian rain forest Toxicon 40 2002 997 1006
51. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
52. F.R. Mandelbaum, A.P. Reichl, and M.T. Assakura Isolation and characterization of a proteolytic enzyme from the venom the snake Bothrops jararaca (jararaca) Toxicon 20 1982 955 972
53. F.R. Mandelbaum, M.T. Assakura, and A.P. Reichl Characterization of two hemorrhagic factors isolated from the venom of Bothrops neuwiedi (jararaca pintada) Toxicon 22 1983 193 206
54. M. Martinez, E.D. Rael, and N.L. Maddux Isolation of a hemorrhagic toxin from Mojave rattlesnake (Crotalus scutulatus) venom Toxicon 28 1990 685 694
55. M. Maruyama, M. Sugiki, E. Yoshida, K. Shimaya, and H. Mihara Broad substrate specificity of snake venom fibrinolytic enzymes: possible role in haemorrhage Toxicon 30 1992 1387 1397
56. M. Maruyama, M. Tanigawa, M. Sugiki, E. Yoshida, and H. Mihara Purification and characterization of low molecular weight fibrinolytic/ hemorrhagic enzymes from snake (Bothrops jararaca) venom Enzyme Protein 47 1993 24 35
57. M. Maruyama, M. Sugiki, K. Anai, and E. Yoshida N-terminal amino acid sequences and some characteristics of fibrinolytic/hemorrhagic metalloproteinases purified from Bothrops jararaca venom Toxicon 40 2002 1223 1226
58. M.V. Mazzi, S. Marcussi, G.B. Carlos, R.G. Stabeli, J.J. Franco, F.K. Ticli, A.C. Cintra, S.C. Franca, A.M. Soares, and S.V. Sampaio A new hemorrhagic metalloprotease from Bothrops jararacussu snake venom: isolation and biochemical characterization Toxicon 44 2004 215 223
59. O. Molina, R.K. Seriel, M. Martinez, M.I. Sierra, A. Varela-Ramirez, and E.D. Rael Isolation of two hemorrhagic toxins from Crotalus basiliscus basiliscus (Mexican west coast rattlesnake) venom and their effect on blood clotting and complement Int. J. Biochem. 22 1990 253 261
60. A.M. Moura-da-Silva, M.S. Della-Casa, A.S. David, M.T. Assakura, D. Butera, I. Lebrun, J.D. Shannon, S.M. Serrano, and J.W. Fox Evidence for heterogenous forms of the snake venom metalloproteinase jararhagin: a factor contributing to snake venom variability Arch. Biochem. Biophys. 409 2003 395 401
61. C.L. Ownby, and T.R. Colberg Presence of heat-stable hemorrhagic toxins in snake venoms Toxicon 32 1994 945 954
62. J.H. Petretski, M.M. Kanashiro, F.R. Rodrigues, E.W. Alves, O.L.T. Machado, and T.L. Kipnis Edema induction by the disintegrin-like/cysteine-rich domains from a Bothrops atrox hemorrhagin Biochem. Biophys. Res. Commun. 276 2000 29 34
63. G. Rosenfeld Symptomatology, pathology and treatment of snake bites in South America W. Bücherl E.E. Buckley Venomous Animals and Their Venoms vol. 2 1971 Academic Press New York 345 384
64. A. Rucavado, J. Núñez, and J.M. Gutiérrez Blister formation and skin damage induced by BaP1, a hemorrhagic metalloproteinase from the venom of the snake Bothrops asper Int. J. Exp. Pathol. 79 1998 245 254
65. A. Rucavado, T. Escalante, C.F. Teixeira, C.M. Fernandes, C. Diaz, and J.M. Gutiérrez Increments in cytokines and matrix metalloproteinases in skeletal muscle after injection of tissue-damaging toxins from the venom of the snake Bothrops asper Mediators Inflamm. 11 2002 121 128
66. E.F. Sanchez, A. Magalhães, F.R. Mandelbaum, and C.R. Diniz Purification and characterization of the hemorrhagic factor II from the venom of the bushmaster snake (Lachesis muta muta) Biochim. Biophys. Acta 1074 1991 347 356
67. D.M. Shotton Elastase Methods Enzymol. 19 1970 113 117
68. I. Tanjoni, D. Butera, P.J. Spencer, H.A. Takehara, I. Fernandes, and A.M. Moura-da-Silva Phylogenetic conservation of a snake venom metalloproteinase epitope recognized by a monoclonal antibody that neutralizes hemorrhagic activity Toxicon 42 2003 809 816
69. R.D.G. Theakston, and H.A. Reid Development of simple standard assay procedures for the characterization of snake venoms Bull. WHO 61 1983 949 956
70. L. Thomas, B. Tyburn, B. Bucher, F. Pecout, J. Ketterle, D. Rieux, D. Smadja, D. Garnier, and Y. Plumelle Prevention of thromboses in human patients with Bothrops lanceolatus envenoming in Martinique: failure of anticoagulants and efficacy of a monospecific antivenom Am. J. Trop. Med. Hyg. 52 1995 419 426
71. L. Thomas, B. Tyburn, J. Ketterle, T. Biao, H. Mehdaoui, V. Moravie, C. Rouvel, Y. Plumelle, B. Bucher, D. Canonee, C.A. Marie-Nelly, and J. Lang Prognostic significance of clinical grading of patients envenomed by Bothrops lanceolatus in Martinique Trans. R. Soc. Trop. Med. Hyg. 92 1998 542 545
72. H. Towbin, T. Staehelin, and J. Gordon Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications Proc. Natl Acad. Sci. USA 76 1979 4350 4354
73. C.C. Viljoen, C.M. Meehan, and D.P. Botes Separation of Bitis gabonica (gaboon adder) venom arginine esterases into kinin-releasing, clotting and fibrinolytic factors Toxicon 17 1979 145 154
74. L. Watanabe, J.D. Shannon, R.H. Valente, A. Rucavado, A. Alapé-Girón, A.S. Kamiguti, R.D. Theakston, J.W. Fox, J.M. Gutiérrez, and R.K. Arni Amino acid sequence and crystal structure of BaP1, a metalloproteinase from Bothrops asper snake venom that exerts multiple tissue-damaging activities Protein Sci. 12 2003 2273 2281
75. G. Watt Snakebite treatment and first aid J.A. Campbell W.W. Lamar The Venomous Reptiles of Latin America 1989 Comstock Publishing Associates/Cornell University Press Ithaca 6 13