Snake venomics across genus Lachesis. Ontogenetic changes in the venom composition of Lachesis stenophrys and comparative proteomics of the venoms of adult Lachesis melanocephala and Lachesis acrochorda

Journal of Proteomics

Volumn 77, Issue , 2012, Pages 280-297

  Madrigal, Marvin ^a   Sanz, Libia ^b   Flores Díaz, Marietta ^a   Sasa, Mahmood ^a   Núñez, Vitelbina ^c   Alape Girón, Alberto ^a   Calvete, Juan J ^b,d  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^c UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^d UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

Central and South American bushmasters; Genus Lachesis; Mass spectrometry; Ontogenetic shift; Snake venomics

Indexed keywords

BRADYKININ POTENTIATING PEPTIDE; GAL LECTIN; LECTIN; METALLOPROTEINASE; NATRIURETIC PEPTIDE TYPE C; PEPTIDE; SNAKE VENOM; SNAKE VENOM METALLOPROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMICAL COMPOSITION; LACHESIS ACROCHORDA; LACHESIS MELANOCEPHALA; LACHESIS MUTA MUTA; LACHESIS STENOPHRYS; NONHUMAN; POISONOUS SNAKE; PRIORITY JOURNAL;

ANIMALS; METALLOPROTEASES; PROTEOMICS; SERINE PROTEASES; SPECIES SPECIFICITY; VIPER VENOMS; VIPERIDAE;

LACHESIS; LACHESIS MELANOCEPHALA; LACHESIS MUTA; LACHESIS MUTA MUTA; LACHESIS STENOPHRYS;

EID: 84870390635     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.09.003     Document Type: Article

References (73)

1. Fry B.G., Wüster W. Assembling an arsenal: origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences. Mol Biol Evol 2004, 21:870-883.
2. Fry B.G. From genome to "venome": molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res 2005, 15:403-420.
3. Fry B.G., Vidal N., Norman J.A., Vonk F.J., Scheib H., Ramjan S.F., et al. Early evolution of the venom system in lizards and snakes. Nature 2006, 439:584-588.
4. Fry B.G., Scheib H., van der Weerd L., Young B., McNaughtan J., Ramjan S.F., et al. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics 2008, 7:215-246.
5. Fry B.G., Vidal N., van der Weerd L., Kochva E., Renjifo C. Evolution and diversification of the Toxicofera reptile venom system. J Proteomics 2009, 72:127-136.
6. Vidal N., Rage J.-C., Couloux A., Hedges S.B. Snakes (Serpentes). The timetree of life 2009, 390-397. Oxford Univ. Press. S.B. Hedges, S. Kumar (Eds.).
7. Greene H.W. Dietary correlates of the origin and radiation of snakes. Am Zool 1983, 23:431-441.
8. Ohno M., Ménez R., Ogawa T., Danse J.M., Shimohigashi Y., Fromen C., et al. Molecular evolution of snake toxins: is the functional diversity of snake toxins associated with a mechanism of accelerated evolution?. Prog Nucleic Acid Res Mol Biol 1998, 59:307-364.
9. Daltry J.C., Wüster W., Thorpe R.S. Diet and snake venom evolution. Nature 1996, 379:537-540.
10. Gibbs H.L., Sanz L., Calvete J.J. Snake population venomics: proteomics-based analyses of individual variation reveals significant gene regulation effects on venom protein expression in Sistrurus rattlesnakes. J Mol Evol 2009, 68:113-125.
11. Mackessy S.P. Venom ontogeny in the Pacific rattlesnakes, Crotalus viridis helleri and C. viridis oreganus. Copeia 1988, 1988:92-101.
12. Gutiérrez J.M., Avila C., Camancho Z., Lomonte B. Ontogenic changes in venom of the snake Lachesis muta stenophrys (Bushmaster) from Costa Rica. Toxicon 1990, 28:419-426.
13. Andrade D.V., Abe A.S. Relationship of venom ontogeny and diet in Bothrops. Herpetologica 1999, 55:200-204.
14. Guércio R.A.P., Shevchenko A., Shevchenko A., López-Lozano J.L., Paba J., Sousa M.V., et al. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox. Proteome Sci 2006, 4:11.
15. Mackessy S.P., Sixberry N.M., Heyborne W.H., Fritts T. Venom of the brown treesnake, Boiga irregularis: ontogenetic shifts and taxa-specific toxicity. Toxicon 2006, 47:537-548.
16. Alape-Girón A., Sanz L., Escolano J., Flores-Díaz M., Madrigal M., Sasa M., et al. Snake venomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J Proteome Res 2008, 7:3556-3571.
17. Calvete J.J., Sanz L., Cid P., De La Torre P., Flores-Diaz M., Dos Santos M.C., et al. Snake venomics of the Central American rattlesnake Crotalus simus and the South American Crotalus durissus complex points to neurotoxicity as an adaptive paedomorphic trend along Crotalus dispersal in South America. J Proteome Res 2010, 9:528-544.
18. Calvete J.J., Sanz L., Pérez A., Borges A., Vargas A.M., Lomonte B., et al. Snake population venomics and antivenomics of Bothrops atrox: paedomorphism along its transamazonian dispersal and implications of geographic venom variability on snakebite management. J Proteomics 2011, 74:510-527.
19. Saldarriaga M.M., Otero R., Núñez V., Toro M.F., Díaz A., Gutiérrez J.M. Ontogenetic variability of Bothrops atrox and Bothrops asper snake venoms from Colombia. Toxicon 2003, 42:405-411.
20. Gutiérrez J.M., Chaves F., Bolaños R. Estudio comparativo de venenos de ejemplares recién nacidos y adultos de Bothrops asper. Rev Biol Trop 1980, 28:341-351.
21. Gibbs H.L., Sanz L., Chiucchi J.E., Farrell T.M., Calvete J.J. Proteomic analysis of ontogenetic and diet-related changes in venom composition of juvenile and adult dusky pigmy rattlesnakes (Sistrurus miliarius barbouri). J Proteomics 2011, 74:2169-2179.
22. Zelanis A., Travaglia-Cardoso S.R., Furtado M.F.D. Ontogenetic changes in Bothrops insularis (Serpentes:Viperidae) snake venom and its biological implications. South Am J Herpetol 2008, 3:45-50.
23. Zelanis A., Tashima A.K., Rocha M.M., Furtado M.F., Camargo A.C., Ho P.L., et al. Analysis of the ontogenetic variation in the venom proteome/peptidome of Bothrops jararaca reveals different strategies to deal with prey. J Proteome Res 2010, 9:2278-2291.
24. Zelanis A., Tashima A.K., Pinto A.F., Leme A.F., Stuginski D.R., Furtado M.F., et al. Bothrops jararaca venom proteome rearrangement upon neonate to adult transition. Proteomics 2011, 11:4218-4228.
25. Chippaux J.P., Williams V., White J. Snake venom variability: methods of study, results and interpretation. Toxicon 1991, 29:1279-1303.
26. Warrell D.A. Geographical and intraspecies variation in the clinical manifestations of envenoming by snakes. Venomous snakes. Ecology, evolution and snakebite 1997, 189-203. Clarendon Press, Oxford, United Kingdom. R.S. Thorpe, W. Wüster, A. Malhotra (Eds.).
27. Gutiérrez J.M., Lomonte B., León G., Alape-Girón A., Flores-Díaz M., Sanz L., et al. Snake venomics and antivenomics: proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J Proteomics 2009, 72:165-182.
28. Solórzano A., Cerdas L. A new subspecies of the bushmaster, Lachesis muta, from Southeastern Costa Rica. J Herpetol 1986, 20:463-466.
29. Garcia E. Los ofidios venenosos del Cauca. Métodos empíricos y racionales empleados contra los accidentes producidos por la mordedura de esos reptiles 1896, Librería Colombiana XV, Cali.
30. Campbell J.A., Lamar W.W. The venomous reptiles of the western hemisphere 2004, Comstock Publishing Associates, Ithaca and London, 870 pp.
31. Málaque C.M.S., Franca F.O.S. Acidente laquético. Animais Peçonhentos no Brasil. Biología, Clínica e Terapéutica dos Accidentes 2003, 87-90. Sarvier, Sao Paulo. J.L.C. Cardoso, F.O.S. Franca, F.H. Wen, C.M.S. Málaque, V. Hadad (Eds.).
32. Brown J.H. Toxicology and pharmacology of venoms from poisonous snakes 1973, Charles C. Thomas, Springfield: Illinois.
33. Fernandes D.S., Franco F.L., Fernandes R. Systematic revision of the genus Lachesis Daudin, 1803 (Serpentes, Viperidae). Herpetol 2004, 60:245-260.
34. Zamudio K.R., Greene H.W. Phylogeograpy of the bushmaster (Lachesis muta: Viperidae): implications for neotropical biogeography, systematic and conservation. Biol J Linn Soc 1997, 62:421-422.
35. Sanz L., Escolano J., Ferretti M., Biscoglio M.J., Rivera E., Crescenti E.J., et al. Snake venomics of the South and Central American Bushmasters. Comparison of the toxin composition of Lachesis muta gathered from proteomic versus transcriptomic analysis. J Proteomics 2008, 71:46-60.
36. Calvete J.J., Juárez P., Sanz L. Snake venomics. Strategy and applications. J Mass Spectrom 2007, 42:1405-1414.
37. Calvete J.J. Proteomic tools against the neglected pathology of snake bite envenoming. Expert Rev Proteomics 2011, 8:739-758.
38. Sanz L., Gibbs H.L., Mackessy S.P., Calvete J.J. Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J Proteome Res 2006, 5:2098-2112.
39. Wetton J.H., Carter R.E., Parkin D.T., Walters D. Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 1987, 327:147-149.
40. Bolaños O.R. Toxicity of Costa Rica snake venoms for white mouse. Am J Trop Med Hyg 1972, 21:360-363.
41. Ripa D. Six new cases of bushmaster envenoming. The Bushmasters (genus Lachesis Daudin, 1803): morphology in evolution and behavior 2003, Electronic book. Cape Fear Serpentarium, Wilmington, NC. 3rd edition.
42. De Souza R.C.G., Nogueira A.P.B., Lima T., Cardoso J.L.C. The enigma of the north margin of the Amazon River: proven Lachesis bites in Brazil, report of two cases, general considerations about the genus and bibliographic review. Bull Chic Herpetol Soc 2007, 42:105-115.
43. Jorge M.T., Sano-Martins I.S., Tomy S.C., Castro S.C., Ferrari R.A., Ribeiro L.A., et al. Snakebite by the bushmaster (Lachesis muta) in Brazil: case report and review of the literature. Toxicon 1997, 35:545-554.
44. Warrell D.A. Snkebites in Central and South America: epidemiology, clinical features, and clinical management. The venomous reptiles of the western hemisphere 2004, 709-761. Comstock Publishing Associates, Ithaca and London. J.A. Campbell, W.W. Lamar (Eds.).
45. Otero-Patiño R., Jaramillo G.S.T., Gómez L.F. Bites from the bushmaster (Lachesis muta) in Antioquia and Chocó, report of five accidents. Toxicon 1993, 31:158-159. (abstract).
46. The venomous reptiles of Latin America 1989, Cornell Univ. Press, Ithaca. NY, 425 pp. J.A. Campbell, W.W. Lamar (Eds.).
47. Silva-Haad J. Accidentes humanos por las serpientes de los géneros Bothrops y Lachesis. Mem Inst Butantan 1982, 44-45:403-423.
48. Hulin A., Och Q.A., Desbordes J.-M. Envenimations par des crotalidés en Guyane Française. Med Afr Noire 1982, 29:249-255.
49. Hardy D.L., Haad J.S. A review of venom toxinology and epidemiology of envenoming of the bushmaster (Lachesis) with report of a fatal bite. Bull Chic Herpetol Soc 1998, 33:113-123.
50. Escalante T., Rucavado A., Fox J.W., Gutiérrez J.M. Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J Proteomics 2011, 74:1781-1794.
51. Baldo C., Tanjoni I., León I.R., Batista I.F., Della-Casa M.S., Clissa P.B., et al. BnP1, a novel P-I metalloproteinase from Bothrops neuwiedi venom: biological effects benchmarking relatively to jararhagin, a P-III SVMP. Toxicon 2008, 51:54-65.
52. Rodrigues V.M., Soares A.M., Guerra-Sá R., Rodrigues V., Fontes M.R., Giglio J.R. Structural and functional characterization of neuwiedase, a nonhemorrhagic fibrin(ogen)olytic metalloprotease from Bothrops neuwiedi snake venom. Arch Biochem Biophys 2000, 381:213-224.
53. de Souza DL Naves, Gomes M.S.R., Ferreira F.B., Rodrigues R.S., Achê D.C., Richardson M., et al. Biochemical and enzymatic characterization of BpMP-I, a fibrinogenolytic metalloproteinase isolated from Bothropoides pauloensis snake venom. Comp Biochem Physiol B 2012, 161:102-109.
54. 2 from Bothrops leucurus snake venom. Comp Biochem Physiol C Toxicol Pharmacol 2011, 154:226-233.
55. Cintra-Francischinelli M., Caccin P., Chiavegato A., Pizzo P., Carmignoto G., Angulo Y., et al. Bothrops snake myotoxins induce a large efflux of ATP and potassiium with spreading of cell damage and pain. Proc Natl Acad Sci U S A 2010, 107:14140-14145.
56. 2 (D49) purified from Lachesis muta rhombeata snake venom with enzymatic-related antithrombotic and anticoagulant activity. Toxicon 2012, 60:773-781.
57. 2 from the venom of the bushmaster snake (Lachesis muta). Braz J Med Biol Res 1993, 26:459-463.
58. Kini R.M. Toxins in thrombosis and haemostasis: potential beyond imagination. J Thromb Haemost 2011, 9(Suppl. 1):195-208.
59. 2 from Lachesis stenophrys (the Central American Bushmaster) snake venom. Protein J 2008, 27:327-333.
60. Ferreira L.A.F., Galle A., Raida M., Schrader M., Lebrun I., Habermehl G. Isolation: analysis and properties of three bradykinin-potentiating peptides (BPP-II, BPP-III, and BPP-V) from Bothrops neuwiedi venom. J Protein Chem 1998, 17:285-289.
61. Ferreira S.H., Bartelt D.C., Greene L.J. Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 1970, 9:2583-2593.
62. Greene L.-J., Camargo A.C., Krieger E.M., Stewart J.M., Ferreira S.H. Inhibition of the conversion of angiotensin I to II and potentiation of bradykinin by small peptides present in Bothrops jararaca venom. Circ Res 1972, 31(Suppl. 2):62-71.
63. Luft F.C. The Bothrops legacy: vasoactive peptides from Brazil. Renin Rep 2008, 10:57-64.
64. Koh C.Y., Kini R.M. From snake venom toxins to therapeutics. Cardiovascular examples. Toxicon 2012, 59:497-506.
65. Du X.Y., Clemetson K.J. Snake venom l-amino acid oxidases. Toxicon 2002, 40:659-665.
66. Guo C., Liu S., Yao Y., Zhang Q., Sun M.Z. Past decade study of snake venom l-amino acid oxidase. Toxicon 2012, 60:302-311.
67. 2, l-amino acid oxidase, and proteinase enzymatic activities of the Lachesis muta rhombeata venom. J Biochem Mol Toxicol 2012, 26:308-314.
68. Ozeki Y., Matsui T., Hamako J., Suzuki M., Fujimura Y., Yoshida E., et al. C-type galactoside-binding lectin from Bothrops jararaca venom: comparison of its structure and function with those of botrocetin. Arch Biochem Biophys 1994, 308:306-310.
69. Hamako J., Suzuki Y., Hayashi N., Kimura M., Ozeki Y., Hashimoto K., et al. Amino acid sequence and characterization of C-type lectin purified from the snake venom of Crotalus ruber. Comp Biochem Physiol B Biochem Mol Biol 2007, 146:299-306.
70. Otero R., Furtado M.F.D., Gonçalves R.C., Núñez V., García M.E., Osorio R.G., et al. Comparative study of the venoms of three subspecies of Lachesis muta (bushmaster) from Brazil, Colombia and Costa Rica. Toxicon 1998, 36:2021-2027.
71. Bigarella J.J., Andrade-Lima D. Paleoenvironmental changes in Brazil. Biological differentiation in the tropics 1982, 27-40. Columbia Univ. Press, New York, USA. G.T. Prance (Ed.).
72. Aguiar A.S., Alves C.R., Melgarejo A., Giovanni-de-Simone S. Purification and partial characterization of a thrombin-like/gyroxin enzyme from bushmaster (Lachesis muta rhombeata) venom. Toxicon 1996, 34:555-565.
73. Gutiérrez J.M., Rojas G., Cerdas L. Ability of a polyvalent antivenom to neutralize the venom of Lachesis muta melanocephala, a Costa Rica subspecies of the bushmaster. Toxicon 1987, 25:713-720.