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

Journal of Proteome Research

Volumn 9, Issue 1, 2010, Pages 528-544

  Calvete, Juan J ^a   Sanz, Libia ^a   Cid, Pedro ^a   De La Torre, Pilar ^a   Flores Díaz, Marietta ^b   Dos Santos, M Cristina ^c   Borges, Adolfo ^d   Bremo, Adolfo ^e   Angulo, Yamileth ^b   Lomonte, Bruno ^b   Alape Girón, Alberto ^b   Gutiérrez, José María ^b  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^c FEDERAL UNIVERSITY OF AMAZONAS   (Brazil)

^d UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^e Universidad Nacional Experimental Francisco de Miranda   (Venezuela)

Author keywords

Antibothropic and anticrotalic ABC antivenom; Antivenomics; Crotalus durissus; Crotalus simus; Crotoxin; Ontogenetic shift; Paedomorphism; Polyvalent (crotalinae) ICP antivenom; Snake venom protein families; Snake venomics

Indexed keywords

METALLOPROTEINASE; NEUROTOXIN; PHOSPHOLIPASE A2; PROTEOME; SERINE PROTEINASE; SNAKE VENOM;

ADOLESCENT; AGE; ARTICLE; CONTROLLED STUDY; EVOLUTION; GENOTYPE PHENOTYPE CORRELATION; GEOGRAPHIC DISTRIBUTION; NEUROTOXICITY; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOMICS; SPECIES DIFFERENCE; SPECIES DISTRIBUTION; SPECIES INVASION; TOXIN ANALYSIS; VENOMICS;

AGE FACTORS; AMINO ACID SEQUENCE; ANIMALS; ANTIVENINS; CROTALID VENOMS; CROTALUS; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROTOXINS; PROTEOME; REPTILIAN PROTEINS; SOUTH AMERICA; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

CROTALINAE; CROTALUS; CROTALUS DURISSUS; CROTALUS DURISSUS TERRIFICUS; MAMMALIA; MUS;

EID: 73649091449     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr9008749     Document Type: Article

References (110)

1. Bullock, T. H.; Cowles, R. B. Physiology of an infrared receptor: the facial pit of pit vipers. Science 1952, 115, 541-543.
2. Bakken, G. S.; Krochmal, A. R. The imaging properties and sensitivity of the facial pit of pitvipers as determined by optical and heat-transfer analysis. J. Exp. Biol. 2007, 210, 2801-2810.
3. Castoe, T. A.; Daza, J. M.; Smith, E. N.; Sasa, M.; Kuch, U.; Campbell, J. A.; Chippindale, P. T.; Parkinson, C. L. Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. J. Biogeogr. 2009, 36, 88-103.
4. Castoe, T. A.; Parkinson, C. L. Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol. Phylogenet. Evol. 2006, 39, 91-110.
5. Knight, A.; Styler, D.; Pelikan, S.; Campbell, J. A.; Densmore, L. D.; Mindrell, D. P. Choosing among hypotheses of rattlesnake phylogeny: a best-fit rate test for DNA sequence data. Systematics Biol. 1993, 42, 356-367.
6. Parkinson, C. L. Molecular systematics and biogeographical history of pitvipers as determined by mitochondrial ribosomal DNA sequences. Copeia 1999, 1999, 576-586.
7. Murphy, R. W.; Fu, J.; Lathrop, A.; Feltham, J. V.; Kovac, V. Phylogeny of the rattlesnakes (Crotalus and Sistrurus) inferred from sequences of five mitochondrial DNA genes In Biology of the Vipers; Höggren, M., Schuett, G. W., Greene, H., Douglas, M. E., Eds.; Eagle Mountain Publishing: Eagle Mountain, UT, 2002; pp 69-92.
8. Gloyd, H. K. The Rattlesnakes, Genera Sistrurus and Crotalus: A Study in Zoogeography and Evolution; Special Publication No. 4; Chicago Academy of Sciences: Chicago, 1940; pp 1-270.
9. Brattstrom, B. H. Evolution of the pitvipers. Trans. San Diego Soc. Nat. History 1964, 13, 185-268.
10. Place, A. J.; Abramson, C. I. A quantitative analysis of the ancestral area of rattlesnakes. J. Herpetol. 2004, 38, 152-156.
11. Greene, H. Snakes: The Evolution of Mystery in Nature; Univ. of California Press: Berkeley, 1997.
12. Parkinson, C. L.; Campbell, J. A.; Chippindale, P. Multigene phylogenetic analysis of pitvipers, with comments on their biogeography. In Biology of the Vipers; Höggren, M., Schuett, G. W., Greene, H., Douglas, M. E. , Eds.; Eagle Mountain Publishing: Eagle Mountain, UT, 2002; pp 93-110.
13. Klauber, L. M. Classification, distribution and biology of the venomous snakes of northern Mexico, the United States and Canada. In Crotalus and Sistrurus; Bücherl, W., Buckley, E. E. , Eds; Venomous animals and their venoms, Vol. 2, Venomous vertebrates.Academic Press: New York, 1971; pp 115-156.
14. Klauber, L. M. Rattlesnakes: Their Habitats, Life Histories, and Influence on Mankind. 2nd ed.; University of California Press: Berkeley, 1997.
15. Campbell, J. A.; Lamar, W. W. The Venomous Reptiles of the Western Hemisphere; Comstock Publishing Associates: Ithaca, NY, 2004.
16. Wüster, W.; Ferguson, J. E.; Quijada-Mascareñas, J. A.; Pook, C. E.; Salomão, M. G.; Thorpe, R. S. Tracing an invasion: landbridges, refugia and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus. Mol. Ecol. 2005, 14, 1095-1108.
17. Quijada-Mascareñas, J. A.; Ferguson, J. E.; Pook, C. E.; Salomão, M. G.; Thorpe, R. S.; Wüster, W. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 2007, 34, 1296-1312.
18. Lewontin, R. C. The genetic basis of evolutionary change; Columbia University Press: New York, 1974.
19. Orr, H. A.; Coyne, J. A. The genetics of adaptation - A reassessment. Am. Nat. 1992, 140, 725-742.
20. Golding, G. B.; Dean, A. M. The structural basis of molecular adaptation. Mol. Biol. Evol. 1998, 15, 355-369.
21. Greene, H. W. Dietary correlates of the origin and radiation of snakes. Am. Zool. 1983, 23, 431-441.
22. Calvete, J. J.; Juárez, P.; Sanz, L. Snake venomics. Strategy and applications. J. Mass Spectrom. 2007, 42, 1405-1414.
23. Calvete, J. J.; Sanz, L.; Angulo, Y.; Lomonte, B.; Gutiérrez, J. M. Venoms, venomics, antivenomics. FEBS Lett. 2009, 583, 1736-1743.
24. Gutiérrez, J. M.; Lomonte, B.; León, G.; Alape-Girón, A.; Flores-Díaz, M.; Sanz, L.; Angulo, Y.; Calvete, J. J. 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.
25. Warrell, D. A. Snakebites in Central and South America: Epidemiology, Clinical Features, and Clinical Management. In The Venomous Reptiles of the Western Hemisphere; Campbell, J. A.; Lamar, W. W., Eds.; Comstock Publishing Associates: Ithaca, NY, 2004; pp 709-761.
26. Gutiérrez, J. M.; Dos Santos, M. C.; Furtado, M. F.; Rojas, G. Biochemical and pharmacological similarities between the venoms of newborn Crotalus durissus durissus and adult Crotalus durissus terrificus rattlesnakes. Toxicon 1991, 29, 1273-1277.
27. Saravia, P.; Rojas, E.; Arce, V.; Guevara, C.; López, J. C.; Chaves, E.; Velásquez, R.; Rojas, G.; Gutiérrez, J. M. Geographic and ontogenic variability in the venom of the neotropical rattlesnake Crotalus durissus: Pathophysiological and therapeutic implications. Rev. Biol. Trop. 2002, 50, 337-346.
28. Bolaños, R.; Marín, O.; Mora-Medina, E.; Alfaro, E. A. El accidente ofídico por cascabela (Crotalus durissus durissus) en Costa Rica. Acta Méd. Costarric. 1981, 24, 211-214.
29. Gutiérrez, J. M. Snakebite envenomation in Central America In Handbook of venoms and toxins of reptiles; Mackessy, S. P., Ed.; CRC Press: Boca Raton, 2009; pp 491-507.
30. 2 In Venom phospholipase A2 enzymes: structure, function and mechanism (Kini, R. M. , ed.), Wiley: Chichester, 1997; pp 269-28.
31. Lomonte, B.; Gené, J. A.; Gutiérrez, J. M.; Cerdas, L. Estudio comparativo de los venenos de serpiente cascabel (Crotalus durissus durissus) de ejemplares adultos y recién nacidos. Toxicon 1983, 21, 379-384.
32. Azevedo-Marques, M. M.; Cupo, P.; Coimbra, T. M.; Hering, S. E.; Rossi, M. E.; Laure, C. J. Myonecrosis, myoglobinuria and acute renal failure induced by South American rattlesnake (Crotalus durissus terrificus) envenomation in Brazil. Toxicon 1985, 23, 631-636.
33. Otero, R. Manual de Diagnóstico y Tratamiento del Accidente Ofídico; Editorial Universidad de Antioquia: Medellín, 1994.
34. Fan, H. W.; Cardoso, J. L. Clinical toxicology of snake bites South America. In Handbook of Clinical Toxicology of Animal Venoms and Poisons; Meier, J., White, J., Eds.; CRC Press: Boca Raton, FL, 1995; pp 667-688.
35. Sánchez, E. F.; Freitas, T. V.; Ferreira-Alves, D. L.; Velarde, D. T.; Diniz, M. R.; Cordeiro, M. N.; Agostini-Cotta, G.; Diniz, C. R. Biological activities of venoms from South American snakes. Toxicon 1992, 30, 95-103.
36. Santoro, M. L.; Sousa-e-Silva, M. C. C.; Gonçalves, L. R. C.; Almeida-Santos, S. M.; Cardoso, D. F.; Laporta-Ferreira, I. L.; Saiki, M.; Peres, C. A.; Sano-Martins, I. S. Comparison of the biological activities in venoms from three subspecies of the South American rattlesnake (Crotalus durissus terrificus, C. durissus casca6ella and C. durissus collilineatus) . Comp. Biochem. Physiol. C 1999, 122, 61-73.
37. Rosenfeld, G. Symptomatology, pathology, and treatment of snake bites in South America In Crotalus and Sistrurus; Bücherl, W., Buckley, E. E., eds; Venomous animals and their venoms. Vol. 2, Venomous vertebrates. Academic Press: New York, 1971; pp 345-384.
38. Azevedo-Marques, M. M.; Hering, S. E.; Cupo, P. Acidente crotálico. In Animais Peçonhentos no Brasil. Biología, Clínica e Terapeutica dos Acidentes, 2nd ed.; Cardoso, J. L. C., Franca, F. O. S., Wen, F. H., Málaque, C. M. S., Haddad, V., Eds.; Sarvier: Sao Paulo, 2009; pp 108-115.
39. Yoshida-Kanashiro, E.; Navarrete, L. F.; Rodriguez-Acosta, A. On the unusual hemorrhagic and necrotic activities caused by the rattlesnake (Crotalus durissus cumanensis) in a Venezuelan patient. Rev. Cubana Med. Tropical 2003, 55, 38-40.
40. Vital Brazil, O. Pharmacology of crystalline crotoxin. II. Neuromuscular blocking action. Mem. Inst. Butantan 1966, 33, 981-992.
41. Chang, C. C.; Tseng, H. Effect of crotamine, a toxin of South American rattlesnake venom, on the sodium channel of murine skeletal muscle. Br. J. Pharmacol. 1978, 63, 551-559.
42. Oguiura, N.; Boni-Mitak, M.; Rádis-Baptista, G. New view on crotamine, a small basic polypeptide myotoxin from South American rattlesnake venom. Toxicon 2005, 46, 363-370.
43. Dos-Santos, M. C.; Ferreira, L. C. L.; Dias da Silva, W.; Furtado, M. F. D. Caracterizacion de las actividades biologicas de los venenos 'amarillo' y 'blanco' de Crotalus durissus ruruima comparados con el veneno de Crotalus durissus terrificus. Toxicon 1993, 31, 1459-1469.
44. Lomonte, B.; Escolano, J.; Fernández, J.; Sanz, L.; Angulo, Y.; Gutiérrez, J. M.; Calvete, J. J. Snake venomics and antivenomics of the arboreal neotopical pitvipers Bothriechis lateralis and Bothriehis schlegelii. J. Proteome Res. 2008, 7, 2445-2457.
45. Gutiérrez, J. M.; Sanz, L.; Escolano, J.; Fernández, J.; Lomonte, B.; Angulo, Y.; Rucavado, A.; Warrell, D. A.; Calvete, J. J. Snake venomic of the Lesser Antillean pit vipers Bothrops caribbaeus and Bothrops lanceolatus: correlation with toxicological activities and immunoreactivity of a heterologous antivenom. J. Proteome Res. 2008, 7, 4396-3408.
46. Calvete, J. J.; Borges, A.; Segura, A.; Flores-Díaz, M.; Alape-Girón, A.; Gutiérrez, J. M.; Diez, N.; De Sousa, L.; Kiriakos, D.; Sánchez, E.; Faks, J. G.; Escolano, J.; Sanz, L. Snake venomics and antivenomics of Bothrops colombiensis, a medically important pitviper of the Bothrops atrox-asper complex endemic to Venezuela: Contributing to its taxonomy and snakebite management. J. Proteomics 2009, 72, 227-240.
47. Núñez, V.; Cid, P.; Sanz, L.; De La Torre, P.; Angulo, Y.; Lomonte, B.; Gutiérrez, J. M.; Calvete, J. J. Snake venomics and antivenomics of Bothrops atrox venoms from Colombia and the Amazon regions of Brazil, Perú and Ecuador suggest the occurrence of geographic variation of venom phenotype by a trend towards paedomorphism. J. Proteomics 2009, 73, 57-78.
48. Savage, J. M.; Campbell, J. A.; Lamar, W. W. On names for Neotropical rattlesnakes. Herpetol. Rev. 2005, 36, 369-371.
49. Dos-Santos, M. C.; Borges de Assis, E.; Moreira, T. D.; Pinheiro, J.; Fortes-Dias, C. L. Individual venom variability in Crotalus durissus ruruima snakes, a subspecies of Crotalus durissus from the Amazonian region. Toxicon 2005, 46, 958-961.
50. Angulo, Y.; Estrada, R.; Gutiérrez, J. M. Clinical and laboratory alterations in horses during immunization with snake venoms for the production of polyvalent (Crotalinae) antivenom. Toxicon 1997, 35, 81-90.
51. Rojas, G.; Jiménez, J. M.; Gutiérrez, J. M. Caprylic acid fractionation of hyperimmune horse plasma: description of a simple procedure for antivenom production. Toxicon 1994, 32, 59-67.
52. Fasman, D. G. Practical Handbook of Biochemistry and Molecular Biology; CRC Press: Boston, 1992.
53. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389-3402.
54. Le Blanc, J. C.; Hager, J. W.; Ilisiu, A. M.; Hunter, C.; Zhong, F.; Chu, I. Unique scanning capabilities of a new hybrid linear ion trap mass spectrometer (QTRAP) used for high sensitivity proteomics applications. Proteomics 2003, 3, 859-869.
55. Alape-Girón, A.; Sanz, L.; Escolano, J.; Flores-Díaz, M.; Madrigal, M.; Sasa, M.; Calvete, J.J. Snake venomics of the lancehead pitviper Bothrops asper: Geographic, individual, and ontogenetic variations. J. Proteome Res. 2008, 7, 3556-3571.
56. Angulo, Y.; Escolano, J.; Lomonte, B.; Gutiérrez, J. M.; Sanz, L.; Calvete, J. J. Snake venomics of Central American pitvipers. Clues for rationalizing the distinct envenomation profiles of Atropoides nummifer and Atropoides picadoi. J. Proteome Res. 2008, 7, 708-719.
57. Sanz, L.; Escolano, J.; Ferretti, M.; Biscoglio, M. J.; Rivera, E.; Crescenti, E. J.; Angulo, Y.; Lomonte, B.; Gutiérrez, J. M.; Calvete, J. J. Snake venomics of the South and Central American Bushmasters. Comparison of the toxin composition ofLachesis muta gathered from proteomic versus transcriptomic analysis. J. Proteomics 2008, 71, 46-60.
58. Sanz, L.; Ayvazyan, N.; Calvete, J. J. Snake venomics of the Armenian mountain vipers Macrovipera lebetina obtusa and Vipera raddei. J. Proteomics 2008, 71, 198-209.
59. Wagstaff, S. C.; Sanz, L.; Juárez, P.; Harrison, R. A.; Calvete, J. J. Combined snake venomics and venom gland transcriptomic analysis of the ocellated carpet viper, Echis ocellatus. J. Proteomics 2009, 71, 609-623.
60. Chippaux, J. P.; Williams, V.; White, J. Snake venom variability: methods of study, results and interpretation. Toxicon 1991, 29, 1279-1303.
61. Aguilar, I.; Guerrero, B.; Salazar, A. M.; Girón, M. E.; Pérez, J. C.; Sánchez, E. E.; Rodríguez-Acosta, A. Individual venom variability in the South American rattlesnake Crotalus durissus cumanensis. Toxicon 2007, 50, 214-224.
62. Salazar, A, M.; Aguilar, I.; Guerrero, B.; Girón, M. E.; Lucena, S.; Sánchez, E. E.; Rodríguez-Acosta, A. Intraspecies differences in hemostatic venom activities of the South American rattlesnakes, Crotalus durissus cumanensis, as revealed by a range of protease inhibitors. Blood Coagulation Fibrinolysis 2008, 19, 525-530.
63. Vanzolini, P. E.; Calleffo, M. E. V. A taxonomic bibliography of the South American snakes of the Crotalus durissus complex (Serpentes, Viperidae). An. Acad. Bras. Ciênc. 2002, 74, 37-83.
64. 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.
65. 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.
66. Fox, J. W.; Serrano, S. M. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 2005, 45, 969-985.
67. Gutiérrez, J. M.; Rucavado, A.; Escalante, T.; Díaz, C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon 2005, 45, 997-1011.
68. Raw, I.; Rocha, M. C.; Esteves, M. I.; Kamiguti, A. S. Isolation and characterization of a thrombin-like enzyme from the venom of Crotalus durissus terrificus. Braz. J. Med. Biol. Res. 1986, 19, 333-338.
69. Guércio, R. A. P.; Shevchenko, A.; Shevchenko, A.; López-Lozano, J. L.; Paba, J.; Sousa, M. V.; Ricart, C. A. O. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox. Proteome Sci. 2006, 4, 11.
70. Mackessy, S. P.; Williams, K.; Ashton, K. G. Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: a case of venom paedomorphosis? Copeia 2003, 2003, 769-782.
71. Mackessy, S. P. Venom Composition in Rattlesnakes: Trends and Biological Significance In The Biology of Rattlesnakes; Hayes, W. K., Beaman, K. R., Cardwell, M. D., Bush, S. P., Eds.; Loma Linda University Press: Loma Linda, CA, 2008; pp 495-510.
72. 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.
73. Marques, O. A. V.; Martins, M.; Sazima, I. A new insular species of pitviper from Brazil, with comments on evolutionary biology and conservation of the Bothrops jararaca group (Serpentes, Viperidae). Herpetologica 2002, 58, 303-312.
74. Solórzano, A. Serpientes de Costa Rica/Snakes of Costa Rica; INBio: Santo Domingo de Heredia, Costa Rica, 2004; pp 677-682.
75. McCue, M. D. Cost of producing venom in three North American pitviper species. Copeia 2006, 2006, 818-825.
76. Baslow, A.; Pook, C. E.; Harrison, R. A.; Wüster, W. Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc. R. Soc. B 2009, 276, 2443-2449.
77. Mackessy, S. P. Venom ontogeny in the Pacific rattlesnakes Crotalus viridis helleri and C.v. oreganus. Copeia 1988, 1988, 92-101.
78. Gibbs, H. L.; Mackessy, S. P. Functional basis of a molecular adaptation: prey-specific toxic effects of venom from Sistrurus rattlesnakes. Toxicon 2009, 53, 672-679.
79. Daltry, J. C.; Wüster, W.; Thorpe, R. S. Diet and snake venom evolution. Nature 1996, 379, 537-540.
80. 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.
81. Sasa, M. Diet and snake venom evolution: Can local selection alone explain intraspecific venom variation? Toxicon 1999, 37, 249-252.
82. Wüster, W.; Daltry, J. C.; Thorpe, R. S. Can diet explain intraspecific venom variation? Reply to Sasa. Toxicon 1999, 37, 253-258.
83. Mebs, D. Toxicity in animals. Trends in evolution? Toxicon 2001, 39, 87-96.
84. Mancin, A. C.; Soares, A. M.; Andrião-Escarso, S. H.; Faça, V. M.; Greene, L. J.; Zuccolotto, S.; Pelá, I. R.; Giglio, J. R. The analgesic activity of crotamine, a neurotoxin from Crotalus durissus terrificus (South American rattlesnake) venom: a biochemical and pharmacological study. Toxicon 1998, 36, 1927-1937.
85. Mouhat, S.; Jouirou, B.; Mosbah, A.; De Waard, M.; Sabatier, J. M. Diversity of folds in animal toxins acting on ion channels. Biochem. J. 2004, 378, 717-726.
86. Bober, M. A.; Glenn, J. L.; Straight, R. C.; Ownby, C. L. Detection of myotoxin alpha-like proteins in various snake venoms. Toxicon 1988, 26, 665-673.
87. Schenberg, S. Geographical pattern of crotamine distribution in the same rattlesnake subspecies. Science 1959, 129, 1361-1363.
88. Garstang, W. The Theory of Recapitulation: a critical Re-statement of the Biogenetic Law. Linn. Soc. Jour. Zool. 1922, XXXV, 81-101.
89. Marques, O. A. V.; Martins, M.; Sazima, I. A new insular species of pitviper from Brazil, with comments on evolutionary biology and conservation of the Bothrops jararaca group (Serpentes, Viperidae). Herpetologica 2002, 58, 303-312.
90. Grazziotin, F. G.; Monzel, M.; Echeverrigaray, S.; Bonatto, S. L. Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic forest. Mol. Ecol. 2006, 15, 3969-3682.
91. Powell, R. L.; Lieb, C. S. Perspectives on venom evolution in Crotalus. In The Biology of Rattlesnakes; Hayes, W. K., Beaman, K. R., Cardwell, M. D., Bush, S. P., Eds.; Loma Linda University Press: Loma Linda, CA, 2008; pp 551-556.
92. Rangel-Santos, A.; Dos-Santos, E. C.; Lopes-Ferreira, M.; Lima, C.; Cardoso, D. F.; Mota, I. A comparative study of biological activities of crotoxin and CB fraction of venoms from Crotalus durissus terrificus, Crotalus durissus cascavella and Crotalus durissus collilineatus. Toxicon 2004, 43, 801-810.
93. Salomão, M. G.; Samtos, S. M. A.; Puorto, G. Activity pattern ofCrotalus durissus (Viperidae, Crotalinae): Feeding, reproduction and snakebite. Stud. Neotrop. Fauna Environ. 1995, 30, 101-106, 1995.
94. Furtado, M. F. D.; Santos, M. C.; Kamiguti, A. S. Age-related biological activity of South American rattlesnake (Crotalus durissus terrificus) venom. J. Venom. Anim. Toxins incl. Trop. Dis. 2009, 9, 186-201.
95. Pawlak, J.; Mackessy, S. P.; Fry, B. G.; Bhatia, M.; Mourier, G.; Fruchart-Gaillard, C.; Servent, D.; Ménez, R.; Stura, E.; Ménez, A.; Kini, R. M. Denmotoxin, a three-finger toxin from the colubrid snake Boiga dendrophila (mangrove catsnake) with bird-specific activity. J. Biol. Chem. 2006, 281, 29030-29041.
96. Pawlak, J.; Mackessy, S. P.; Sixberry, N. M.; Stura, E. A.; Le Du, M. H.; Ménez, R.; Foo, C. A.; Ménez, A.; Nirthanan, S.; Kini, R. M. Iriditoxin, a novel covalently-linked heterodimeric three-finger toxin with high taxon-specific neurotoxicity. FASEB J. 2009, 23, 534-545.
97. Starkov, V. G.; Osipov, A. V.; Utkin, Y. N. Toxicity of venoms from vipers of Pelias group to crickets Gryllus assimilis and its relation to snake entomophagy. Toxicon 2007, 49, 995-1001.
98. Gutiérrez, J. M.; Theakston, R. D. G.; Warrell, D. A. Confronting the neglected problem of snake bite envenoming: The need for a global partnership. PLoS Med. 2006, 3, e150.
99. Gutiérrez, J. M.; Higashi, H. G.; Wen, F. H.; Burnouf, T. Strengthening antivenom production in Central and South American public laboratories: Report of a workshop. Toxicon 2007, 49, 30-35.
100. Stock, R. P.; Massougbodji, A.; Alagón, A.; Chippaux, J.-P. Bringing antivenoms to Sub-Saharan Africa. Nat. Biotechnol. 2007, 2, 173-177.
101. Bolaños, R. Las serpientes venenosas de Centroamérica y el problema del ofidismo. Primera parte. Aspectos zoológicos, epidemiológicos y biomédicos. Rev. Costarric. Cien. Méd. 1982, 3, 165-184.
102. De Oliveira, R. C. ; Wen, F. H.; Sifuentes, D. N. Epidemiologia dos accidentes poe animais peçonhentos. In Animais Peçonhentos no Brasil. Biologia, Clínica e Terapêutica dos Acidentes, 2nd ed.; Cardoso, J. L. C., França, F. O. S., Wen, F. H., Málaque, C. M. S., Haddad, V., Eds.; Sarvier: Sao Paulo, 2009; pp 6-21.
103. Jorge, M. T.; Ribeiro, L. A. Epidemiology and clinical picture of accidental bites by the South American rattlesnake (Crotalus durissus. Rev. Inst. Med. Trop. Sao Paulo 1992, 34, 347-354.
104. Chippaux, J. P. Les envenimations ophidiennes en Guyane Francaise. Méd. Trop. 2002, 62, 177-184.
105. Zavaleta, A.; Salas, M. C. Ofidismo: envenenamiento por mordedura de serpientes. In Emergencias en Medicina Interna; Villaverde, J. R., León-Barúa, R., Vidal-Neira, L., Losno-García, R., Eds.; Lima, 1996; pp 241-260.
106. World Health Organization Rabies and envenomings. A neglected public health issue: Report of a consultative meeting; WHO: Geneva, 2007; Available: http://www.who.int/bloodproducts/animal-sera/Rabies.pdf.
107. Azofeifa-Cordero, A; Arce-Estrada, V.; Flores-Díaz, M.; Alape-Girón, A. Immunization with cDNA of a novel P-III type metalloproteinase from the rattlesnake Crotalus durissus durissus elicits antibodies which neutralize 69% of the hemorrhage induced by the whole venom. Toxicon 2008, 52, 302-308.
108. Rodriguez, J. P.; De Marzi, M.; Maruñak, S.; Malchiodi, E. L.; Leiva, L. C.; Acosta, O. Rabbit IgG antibodies against phospholipase A2 from Crotalus durissus terrificus neutralize the lethal activity of the venom. Med. (B. Aires) 2006, 66, 512-516.
109. 2 from Crotalus durissus cascavella venom neutralize the neurotoxicity of the venom and crotoxin. Toxicon 2004, 44, 141-148.
110. Calvete, J. J.; Fasoli, E.; Sanz, L.; Boschetti, E.; Righetti, P. G. Exploring the venom proteome of the western diamondback rattlesnake, Crotalus atrox, via snake venomics and combinatorial peptide ligand library approaches. J. Proteome Res. 2009, 8, 3055-3067.