Exploring the proteomes of the venoms of the Peruvian pit vipers Bothrops atrox, B. barnetti and B. pictus

Journal of Proteomics

Volumn 75, Issue 7, 2012, Pages 2181-2195

  Kohlhoff, Markus ^a   Borges, Marcia H ^a   Yarleque, Armando ^b   Cabezas, Cesar ^c   Richardson, Michael ^a   Sanchez, Eladio F ^a  

^a Ezequiel Dias Foundation   (Brazil)

^b UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS   (Peru)

^c INSTITUTO NACIONAL DE SALUD   (Peru)

Author keywords

Bothrops atrox; Bothrops barnetti; Bothrops pictus; Proteomics; Snake venomics

Indexed keywords

AMINO ACID OXIDASE; CYSTEINE; CYSTEINE RICH SECRETORY PROTEIN; DISINTEGRIN; LECTIN; LECTIN C; METALLOPROTEINASE; PHOSPHOLIPASE A2; PROTEOME; SECRETORY PROTEIN; SERINE PROTEINASE; SNAKE VENOM; TRYPSIN; UNCLASSIFIED DRUG;

ARTICLE; BOTHROPS ATROX; BOTHROPS BARNETTI; BOTHROPS PICTUS; CONTROLLED STUDY; NONHUMAN; PEPTIDE ANALYSIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEOMICS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SNAKE;

ANIMALS; BOTHROPS; CROTALID VENOMS; PERU; PROTEOME; PROTEOMICS; SPECIES SPECIFICITY;

BOTHROPS; BOTHROPS ATROX; BOTHROPS PICTUS; CROTALINAE;

EID: 84858749669     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.01.020     Document Type: Article

References (49)

1. 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.
2. Clemetson K.J., Navdaev A., Dormann D., Du X.Y., Clemetson J.M. Multifuntional snake C-type lectins affecting platelets. Haemostasis 2001, 31:148-154.
3. Núñez V., Cid P., Sanz L., De La Torre P., Angulo Y., Lomonte B., et al. 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.
4. Fenwick A.M., Gutberlet JR R.L., Evans J.A., Parkinson C.L. Morphological and molecular evidence for phylogeny and classification of South American pitvipers, genera Bothrops, Bothriopsis, and Bothrocophias (Serpentes:Viperidae). Zool J Linn Soc 2009, 156:617-640.
5. Peterson M.E. Snakebite:pit vipers. Clin Tech Small Anim Pract 2006, 21:174-182.
6. Wüster W., Thorpe R.S., Puorto G. Systematics of the Bothrops atrox complex (Reptilia: serpents: viperidae) in Brazil: a multivariate analysis. Herpetologica 1996, 52:263-271.
7. Warrell D.A. Snakebites in Central and South America: epidemiology, clinical features, and clinical management. The venomous reptiles of the Western Hemisphere 2004, 709-761. Cornell University Press, Ithaca, NY. J.A. Campbell, W.W. Lamar (Eds.).
8. Campbell J.A., Lamar W.W. The venomous reptiles of the Western Hemisphere 2004, Comstock Publishing Associates, Ithaca, NY.
9. Castoe T.A., Daza J.M., Smith E.N., Sasa M., Duch U., Campbell J.A., et al. Comparative phylogeography highland biogeography. J Biogeogr 2009, 36:88-103.
10. White J. Snake venom and coagulopathy. Toxicon 2005, 45:951-967.
11. Markland F.S. Snake venoms and the hemostatic system. Toxicon 1998, 36:1749-1800.
12. Manrique H.C., Chunga D., Cáceres M., Espinoza E., Castañeda M.N. Ofidismo en Ucayali. Rev Peruana de Enfermedades Infecciosas y Tropicales 2001, 1:1-12.
13. Sanchez E.F., Schneider F.S., Yarleque A., Borges M.H., Richardson M., Figueiredo S.G., et al. The novel metalloproteinase atroxlysin-I from Peruvian Bothrops atrox (Jergón) snake venom acts both on blood vessel ECM and platelets. Arch Biochem Biophys 2010, 496:9-20.
14. Oropeza D.L., Gonzaga R.A., Villafuerte Y.N., Vásquez M.V., Tapia J.C. Ofidismo por Bothrops atrox: Estudio clínico-epidemiológico. Diagnostico 2000, 38:1-6.
15. Calvete J.J., Sanz L., Pérez A., Borges A., Vargas A.M., Lomonte B., et al. Snake population venomics and antivenomics of Bothrops atrox: Paedomorfism along its transamazonian dispersal and implications of geographic venom variability on snakebite management. J Proteomics 2011, 74:510-527.
16. Maguiña C., Enrique C., Ilquimiche L., Mostorino R., Gotuzzo E., Legua P., et al. Ofidismo por Bothrops pictus en el Hospital Nacional Cayetano Heredia: Estudio prospectivo de 23 casos. Folia Dermatol Perú 1998, 9:41-48.
17. Gutierrez L.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-e159.
18. Lewis R.J., Garcia M.L. Therapeutic potential of venom peptides. Nat Rev Drug Discov 2003, 2:790-802.
19. Martins M., Oliveira M.E. Natural history of snakes in forest of the Manaus region. Central Amazonia, Brazil. Herpetol Nat History 1998, 6:78-150.
20. 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, 71:6-60.
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
22. Souza G.H.M.F., Catharino R.R., Ifa D.R., Eberlin M.N., Hyslop S. Peptide fingerprinting of snake venoms by direct infusion nano-electrospray ionization mass spectrometry: potential use in venom identification and taxonomy. J Mass Spectrom 2008, 43:594-599.
23. Kumarathasan P., Mohottalage S., Goegan P., Vincent R. An optimized protein in-gel digest method for reliable proteome characterization by MALDI-TOF-MS analysis. Anal Biochem 2005, 346:85-89.
24. Calvete J.J., Júarez P., Sanz L. Snake venomics. Strategy and applications. J Mass Spectrom 2007, 42:1405-1414.
25. Towbin H., Stahelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 1979, 76:4350-4356.
26. Sanchez E.F., Freitas T.V., Ferreira-Alves D.L., Velarde D.T., Diniz M.R., Cordeiro M.N., et al. Biological activities of venoms from South American snakes. Toxicon 1992, 30:95-103.
27. Finney D.J. Probit Analysis 1971, Cambridge University Press, London. Third Edn.
28. Sanchez E.F., Santos C.I., Magalhaes A., Diniz C.R., Figueiredo S., Gilroy J., et al. Isolation of a proteinase with plasminogen-activating activity from Lachesis muta muta (Bushmaster). Arch Biochem Biophys 2000, 378:131-141.
29. Camey K.U., Velarde D.T., Sanchez E.F. Pharmacological characterization and neutralization of the venoms used in the production of Bothropic antivenom in Brazil. Toxicon 2002, 40:501-509.
30. Guércio R.A.P., Shevchenko A., Shevchenko A., López-Lozano J.L., Paba J., Souza M.V., et al. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox. Proteome Sci 2006, 4:11.
31. Calvete J.J., Borges A., Segura A., Flores-Dias M., Alape-Giron A., Gutierrez J.M., et al. 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.
32. Saldarriaga M.M., Otero R., Nuñez V., Toro M.F., Diaz A., Gutierrez J.M. Ontogenetic variability of Bothrops atrox and Bothrops asper snake venoms from Colombia. Toxicon 2003, 42:405-411.
33. López-Lozano J.L., de Souza M.V.S., Ricart C.A.T., Chavez-Olortegui C., Sanchez E.F., Muniz E.G., et al. Ontogenetic variation of metalloproteinases and plasma coagulant activity in venoms of wild Bothrops atrox specimens from Amazonian rain forest. Toxicon 2002, 40:997-1006.
34. De Roodt A.R., Litwin S., Vidal J.C. Hemorrhagic activity of Bothrops venoms determined by two different methods and relationship with proteolytic activity on gelatin and lethality. Toxicon 2003, 41:949-958.
35. Masuda S., Hayashi H., Araki S. Two vascular apoptosis-inducing proteins from snake venom are members of the metalloprotease/disintegrin family. Eur J Biochem 1998, 253:36-41.
36. Chippaux J.P., Williams V., White J. Snake venom variability: Methods of study, results and interpretation. Toxicon 1991, 29:1279-1303.
37. Daltry J.C., Wüster W., Thorpe R.S. Diet and snake venom evolution. Nature 1996, 379:537-540.
38. Sasa M. Diet and snake venom evolution: Can local selection alone explain intraspecific venom variation?. Toxicon 1999, 37:249-252.
39. Alape-Giron A., Sanz L., Escolano J., Flores-Diaz 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.
40. Tashima A.K., Sanz L., Camargo A.C.M., Serrano S.M.T., Calvete J.J. Snake venomics of the Brazilian pitvipers Bothrops cotiara and Bothrops fonsecai. Identification of taxonomy markers. J Proteomics 2008, 71:437-485.
41. Ferreira R.N., Rates B., Richardson M., Guimaraes B.G., Sanchez E.F., Pimenta A.M.C., et al. Complete amino acid sequence, crystallization and preliminary X-ray diffraction studies of leucurolysin-a, a nonhemorrhagic metalloproteinase from Bothrops leucurus snake venom. Acta Cryst 2009, F65:798-801.
42. Sanchez E.F., Gabriel L.M., Gontijo S., Gremski H.L., Veiga S.S., Evangelista K.S., et al. Structural and functional characterization of a P-III metalloproteinase, leucurolysin-B from Bothrops leucurus venom. Arch Biochem Biophys 2007, 468:193-204.
43. Naumann G.B., Silva L.F., Silva L., Faria G., Richardson M., Evangelista K., et al. Cytotoxicity and inhibition of platelet aggregation caused by an l-amino acid oxidase from Bothrops leucurus venom. Biochim Biophys Acta 2011, 1810:683-694.
44. Fraveau P., Cheneval O., Menin L., Michalet S., Gaertner H., Principaud F., et al. The venom of the snake genus Atheris contains a new class of peptides with clusters of histidine and glycine residues. Rapid Commun Mass Spectrom 2007, 21:406-412.
45. Wagstaff S.C., Favreau P., Cheneval O., Laing G.D., Wilkinson M.C., Miller R.L., et al. Molecular characterization of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun 2008, 365:650-656.
46. Lomonte B., Carmona E. Individual expression patterns of myotoxin isoforms in the venom of the snake Bothrops asper. Comp Biochem Physiol B 1992, 102:325-329.
47. Calvete J.J., Escolano J., Sanz L. Snake venomics of Bitis species reveals large intragenus venom toxin composition variation: application to taxonomy of congeneric taxa. J Proteome Res 2007, 6:2732-2745.
48. Furtado M.F.D., Cardoso S.T., Soares O.E., Pereira A.P., Fernandes D.S., Tambourgi D.V., et al. Antigenic cross-reactivity and immunogenicity of Bothrops venoms from snakes of the Amazon region. Toxicon 2010, 55:881-887.
49. Neiva M., Arraes F.B., de Souza J.V., Radis-Baptista G., Prieto da Silva A.R., Astofi-Filho S. Transcriptome analysis of the Amazonian viper Bothrops atrox venom gland using expressed sequence tags (ESTs). Toxicon 2009, 53:427-436.