Proteomic tools against the neglected pathology of snake bite envenoming

Expert Review of Proteomics

Volumn 8, Issue 6, 2011, Pages 739-758

  Calvete, Juan J ^a  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

antivenom; antivenomics; mass spectrometry; neglected pathology; snake bite; snake venomics; toxin; venom protein family

Indexed keywords

PROTEOME; SNAKE VENOM ANTISERUM;

CROSS REACTION; ENVENOMATION; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; PHYLOGENY; PROTEOMICS; REVIEW; SNAKEBITE;

ANIMALS; ANTIVENINS; HUMANS; PROTEOMICS; SNAKE BITES;

EID: 81555207448     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/epr.11.61     Document Type: Review

References (126)

1. Fry BG, Roelants K, Champagne DE et al. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics Hum. Genet. 10, 483-511 (2009).
2. Feldman CR, Brodie ED Jr, Brodie ED 3rd, Pfrender ME. The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc. Natl Acad. Sci. USA 106, 13415-13420 (2009).
3. Toxins and Hemostasis. From Bench to Bedside. Kini RM, Clemetson KJ, Markland FS, McLane MA, Morita T (Eds). Springer, Dordrecht, The Netherlands (2010).
4. Animal Toxins: State of the Art. Perspectives in Health and Biotechnology. De Lima ME, Pimenta AMC, Martin-Euclaire MF, Zingali RB, Rochat H (Eds). Editora UFMG, Belo Horizonte, Brazil (2009).
5. Vetter I, Davis JL, Rash LD et al. Venomics: a new paradigm for natural products-based drug discovery. Amino Acids 40, 15-28 (2011).
6. Escoubas P, King GF. Venomics as a drug discovery platform. Expert Rev. Proteomics 6, 221-224 (2009).
7. Stock RP, Massougbodji A, Alagón A, Chippaux J-P. Bringing antivenoms to Sub-Saharan Africa. Nature Biotechnol. 2, 173-177 (2007).
8. Kasturiratne A, Wickremasinghe AR, de Silva N et al. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med. 5, e218 (2008).
9. Chippaux J-P, Goyffon M. Epidemiology of scorpionism: a global appraisal. Acta Tropica 107, 71-79 (2008).
10. Williams D, Gutiérrez JM, Harrison R et al. The Global Snake Bite Initiative: an antidote for snake bite. Lancet 375, 89-91 (2010).
11. Gutiérrez JM, Williams D, Fan HW, Warrell DA. Confronting the neglected problem of snake bite envenoming: the need for a global partnership. Toxicon 56, 1223-1235 (2010).
12. Gutiérrez JM, Lomonte B, León G et al. Snake venomics and antivenomics: Proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J. Proteomics 72, 165-182 (2009).
13. Escoubas P. Mass spectrometry in toxinology: a 21st-century technology for the study of biopolymers from venoms. Toxicon 47, 609-726 (2006).
14. Calvete JJ, 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. 6, 2732-2745 (2007).
15. Tashima AK, Sanz L, Camargo ACM, Serrano SMT, Calvete JJ. Snake venomics of the Brazilian pitvipers Bothrops cotiara and Bothrops fonsecai. Identification of taxonomy markers. J. Proteomics 71, 473-485 (2008).
16. Calvete JJ, Borges A, Segura A 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 72, 227-240 (2009).
17. Guércio RA, Shevchenko A, Shevchenko A et al. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox. Proteome Sci. 4, 11 (2006).
18. Menezes MC, Furtado MF, Travaglia- Cardoso SR, Camargo AC, Serrano SM. Sex-based individual variation of snake venom proteome among eighteen Bothrops jararaca siblings. Toxicon 47, 304-312 (2006).
19. Alape-Girón A, Sanz L, Escolano J et al. Snake venomics of the lancehead pitviper Bothrops asper. Geographic, individual and ontogenetic variations. J. Proteome Res. 7, 3556-3571 (2008).
20. Gibbs HL, Sanz L, Calvete JJ. Snake population venomics: proteomics-based analyses of individual variation reveals gene regulation effects on venom protein expression in Sistrurus rattlesnakes. J. Mol. Evol. 68, 113-125 (2009).
21. Zelanis A, Tashima AK, Rocha MMT, 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. 9, 2278-2291 (2010).
22. Juárez P, Sanz L, Calvete JJ. Snake venomics: characterization of protein families in Sistrurus barbouri venom by cysteine mapping, N-terminal sequencing, and tandem mass spectrometry analysis. Proteomics 4, 327-338 (2004).
23. Calvete JJ, Juárez P, Sanz L. Snake venomics. Strategy and applications. J. Mass Spectrom. 42, 1405-1414 (2007).
24. Quinton L, Demeure K, Dobson R, Gilles N, Gabelica V, De Pauw E. New method for characterizing highly disulfide-bridged peptides in complex mixtures: application to toxin identification from crude venoms. J. Proteome Res. 6, 3216-3223 (2007).
25. Buczek O, Bulaj G, Olivera BM. Conotoxins and the posttranslational modification of secreted gene products. Cell. Mol. Life Sci. 62, 3067-3079 (2005).
26. Jakubowski JA, Kelley WP, Sweedler JV. Screening for post-translational modifications in conotoxins using liquid chromatography/mass spectrometry: an important component of conotoxin discovery. Toxicon 47, 688-699 (2006).
27. Escoubas P, Quinton L, Nicholson GM. Venomics: unravelling the complexity of animal venoms with mass spectrometry. J. Mass Spectrom. 43, 279-295 (2008).
28. Menin L, Perchuc A, Favreau P et al. High throughput screening of bradykinin-potentiating peptides in Bothrops moojeni snake venom using precursor ion mass spectrometry. Toxicon 51, 1288-1302 (2008).
29. Schmid DG, Grosche P, Bandel H, Jung G. FTICR-mass spectrometry for high-resolution analysis in combinatorial chemistry. Biotechnol. Bioeng. 71, 149-161 (2000).
30. Scigelova M, Makarov A. Orbitrap mass analyzer - overview and applications in proteomics. Proteomics 1(Suppl. 2), 16-21 (2006).
31. De Hoffmann E, Stroobant V. Mass Spectrometry. Principles and Applications (3rd Edition). John Wiley & Sons Ltd, Chichester, UK (2007).
32. Jagannadham MV. Identifying the sequence and distinguishing the oxidizedmethionine from phenylalanine peptides by MALDI TOF/TOFmass spectrometry in an antarctic bacterium Pseudomonassyringae. Proteomics Insights 2 27-31 (2009).
33. Armirotti A, Scapolla C, Benatti U, Damonte G. Electrospray ionization ion trap multiple-stage mass spectrometric fragmentation pathways of leucine and isoleucine: an ab initio computational study. Rapid Commun. Mass Spectrom. 21, 3180-3184 (2007).
34. Soltwish J, Dreisewerd K. Discrimination of isobaric leucine and isoleucine residues and analysis of post-translational modifications in peptides by MALDI in-source decay mass spectrometry combined with collisional cooling. Anal. Chem. 82, 5628-5635 (2010).
35. Kapp E, Schütz F. Overview of tandem mass spectrometry (MS/MS) database search algorithms. Curr. Protoc. Protein Sci. 25, Unit 25.2 (2007).
36. Kandasamy K, Pandey A, Molina H. Evaluation of several MS/MS search algorithms for analysis of spectra derived from electron transfer dissociation experiments. Anal. Chem. 81, 7170-7180 (2009).
37. Perspectives in Molecular Toxinology. Ménez A (Ed.). John Wiley & Sons Ltd, Chichester, UK (2002).
38. Wilm M, Neubauer G, Mann M. Parent ion scans of unseparated peptide mixtures. Anal. Chem. 68, 527-533 (1996).
39. Huddleston HJ, Bean MF, Carr SA. Collisional fragmentation of glycopeptides by electrospray ionization LC/MS and LC/ MS/MS: methods for selective detection of glycopeptides in protein digests. Anal. Chem. 65, 877-884 (1993).
40. Lehmann WD, Krüger R, Salek M, Hung CW, Wolschin F, Weckwerth W. Neutral loss-based phosphopeptide recognition: a collection of caveat. J. Proteome Res. 6, 2866-2873 (2007).
41. Cox DM, Zhong F, Du M, Duchoslav E, Sakuma T, McDermott JC. Multiple reaction monitoring as a method for identifying protein posttranslational modifications. J. Biomol. Tech. 16, 83-90 (2005).
42. Serrano SMT, Shannon JD, Wang D, Camargo ACM, Fox JW. A multifaceted analysis of viperid snake venoms by two-dimensional gel electrophoresis: an approach to understanding venom proteomics. Proteomics 5, 501-510 (2005).
43. Rabilloud T, Chevallet M, Luche S, Lelong C. Two-dimensional gel electrophoresis in proteomics: past, present and future. J. Proteomics 73, 2064-2077 (2010).
44. Nawarak J, Sinchaikul S, Wu C-Y, Liau M-Y, Phutrakui S, Chen S-T. Proteomics of snake venoms from Elapidae and Viperidae families by multidimensional chromatographic methods. Electrophoresis 24, 2838-2854 (2003).
45. Li S, Wang J, Zhang X et al. Proteomic characterization of two snake venoms: Naja naja atra and Agkistrodon halys. Biochem. J. 384, 119-127 (2004).
46. Georgieva D, Risch M, Kardas A, Buck F, von Bergen M, Betzel C. Comparative analysis of the venom proteomes of Vipera ammodytes ammodytes and Vipera ammodytes meridionalis. J. Proteome Res. 7, 866-886 (2008).
47. Risch M, Georgieva D, von Bergen M. et al. Snake venomics of the Siamese Russell's viper (Daboia russelli siamensis) - relation to pharmacological activities. J. Proteomics 72, 256-269 (2009).
48. Georgieva D, Öhler M, Seifert J et al. Snake venomics of Crotalus durissus terrificus - correlation with pharmacological activities. J. Proteome Res. 9, 2302-2316 (2010).
49. Öhler M, Georgieva D, Seifert J et al. The venomics of Bothrops alternatus is a pool of acidic proteins with perdominant hemorrhagic and coagulopathic activities. J. Proteome Res. 9, 2422-2437 (2010).
50. Georgieva D, Seifert J, Ohler M et al. Pseudechis australis venomic: adaptation for a defense against microbial pathogens and recruitment of body transferrin. J. Proteome Res. 10, 2440-2464 (2011).
51. Antunes TC, Yamashita KM, Barbaro KC, Saiki M, Santoro ML. Comparative analysis of newborn and adult Bothrops jararacasnake venoms. Toxicon 56, 1443-1458 (2010).
52. Paes LAF, Kitano ES, Furtado MF et al. Analysis of the subproteomes of proteinases and heparin-binding toxins of eight Bothrops venom. Proteomics 9, 733-745 (2009).
53. Birrell GW, Earl STH, Masci PP et al. Molecular diversity in venom from the Australian Brown snake, Pseudonaja textilis. Mol. Cell. Proteomics 5, 379-389 (2006).
54. Birrell GW, Earl STH, Wallis TP et al. The diversity of bioactive proteins in Australian snake venoms. Mol. Cell. Proteomics 6, 973-986 (2007).
55. St. Pierre L, Birrell GW, Earl ST et al. Diversity of toxin components from the venom of the evolutionary distinct Black Whip snake, Demansia vestigiata. J. Proteome Res. 6, 2093-3107 (2007).
56. Olamendi-Portugal T, Batista CVF, Restano-Cassulini R et al. Proteomic analysis of the venom from the fish eating coral snake Micrurus surinamensis: novel toxins, their function and phylogeny. Proteomics 8, 1919-1932 (2008).
57. Kulkeaw K, Chaicumpa W, Sakolvaree Y, Tongtawe P, Tapchaisri P. Proteome and immunome of the venom of the Thai cobra, Naja kaouthia. Toxicon 49, 1026-1041 (2007).
58. Corrêa-Netto C, Teixeira-Araujo R, Aguiar AS et al. Immunome and venome of Bothrops jararacussu: a proteomic approach to study the molecular immunology of snake venoms. Toxicon 55, 1222-1235 (2010).
59. Fry BG, Wickramaratna JC, Hodgson WC et al. Electrospray liquid chromatography/ mass spectrometry fingerprinting of Acanthophis (death adder) venoms: taxonomic and toxinological implications. Rapid Commun. Mass Spectrom. 16, 600-608 (2002).
60. Fox JW, Shannon JD, Stefansson B et al. Role of discovery science in toxinology: examples in venom proteomics. In:Perspectives in Molecular Toxinology . Ménez A (Ed.). John Wiley & Sons Ltd, Chichester, UK, 97-108 (2002).
61. Fry BG, Wüster W, Ramjan SFR et al. Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications. Rapid Commun. Mass Spectrom. 17, 2047-2062 (2003).
62. Quinton L, Le Caer J-P, Phan G et al. Characterization of toxins within crude venoms by combineduse of Fourier transform mass spectrometry and cloning. Anal. Chem. 77, 6630-6639 (2005).
63. Fox JW, Ma L, Nelson K, Sherman NE, Serrano SMT. Comparison of indirect and direct approaches using ion-trap and Fourier transform ion cyclotron resonance mass spectrometry for exploring viperid venom proteomes. Toxicon 47, 700-714 (2006).
64. Bandeira N, Clauser KR, Pevzner PA. Shotgun protein sequencing. Assembly of peptide tandem mass spectra from mixtures of modified proteins. Mol. Cell. Proteomics 6, 1123-1134 (2007).
65. Wermelinger LS, Dutra DL, Oliveira- Carvalho AL et al. Fast analysis of low molecular mass compounds present in snake venom: identification of ten new pyroglutamate-containing peptides. Rapid Commun. Mass Spectrom. 19, 1703-1708 (2005).
66. Favreau P, Cheneval O, Menin L 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. 21, 406-412 (2007).
67. Pimenta DC Prezoto BC Konno K et al. Mass spectrometric analysis of the individual variability of Bothrops jararaca venom peptide fraction. Evidence for sex based variation among the bradykinin-potentiating peptides. Rapid Commun. Mass Spectrom. 21, 1034-1042 (2007).
68. Doley R, Kini RM. Protein complexes in snake venom. Cell. Mol. Life Sci. 66, 2851-2871 (2009).
69. Marschall C, Inglis AS. Protein oligomer composition, preparation of monomers and constituent chains. In:Practical Protein Chemistry . Darbre A (Ed.). John Wiley & Sons Ltd, Chichester, UK, 1-66 (1986).
70. Benesch JL, Ruotolo BT, Simmons DA, Robinson CV. Protein complexes in the gas phase: technology for structural genomics and proteomics. Chem Rev. 107, 3544-3567 (2007).
71. Bich C, Zenobi R. Mass spectrometry of large complexes. Curr. Opin. Struct. Biol. 19, 632-639 (2009)
72. Zhou M, Robinson CV. When proteomics meets structural biology. Trends Biochem. Sci. 35, 522-529 (2010).
73. Edman P. Method for determination of the amino acid sequence in peptides. Acta Chem. Scand. 4, 283-293 (1950).
74. Ohno M, Ménez R, Ogawa T 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. 59, 307-364 (1998).
75. Calvete JJ, Sanz L, Angulo Y, Lomonte B, Gutiérrez JM. Venoms, venomics, antivenomics. FEBS Lett. 583, 1736-1743 (2009).
76. Calvete JJ. Antivenomics and venom phenotyping: a marriage of convenience to address the performance and range of clinical use of antivenoms. Toxicon 56, 1284-1291 (2010).
77. Calvete JJ. Snake venomics, antivenomics, and venom phenotyping: ménage àtrois of proteomic tools aimed at understanding the biodiversity of venoms. In:Toxins and Hemostasis: From Bench to Bedside. Kini RM, Clemetson K, Markland F, McLane MA, Morita T (Eds). Springer, Dordrecht, The Netherlands, 45-72 (2010).
78. Fox JW, Serrano SMT. Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures. Proteomics 8, 909-920 (2008).
79. Georgieva D, Arni RK, Betzel C. Proteome analysis of snake venom toxins: pharmacological insights. Expert Rev. Proteomics 5, 787-797 (2008).
80. Righetti PG, Boschetti E, Kravchuk AV, Fasoli E. The proteome buccaneers: how to unearth your treasure chest via combinatorial peptide ligand libraries. Expert Rev. Proteomics 7, 373-378 (2010).
81. Calvete JJ, Fasoli E, Sanz L, Boschetti E, Righetti PG. Exploring the venom proteome of the western diamondback rattlesnake, Crotalus atrox, via snake venomics and combinatorial peptide ligand library approaches. J. Proteome Res. 8, 3055-3067 (2009).
82. Fasoli E, Sanz L, Wagstaff S, Harrison RA, Righetti PG, Calvete JJ. Exploring the venom proteome of the African puff adder, Bitis arietans, using a combinatorial peptide ligand library approach at different pHs. J. Proteomics 73, 932-934 (2010).
83. Angulo Y, Escolano J, Lomonte B, Gutiérrez JM, Sanz L, Calvete JJ. Snake venomics of central american pitvipers: clues for rationalizing the distinct envenomation profiles of Atropoides nummifer and Atropoides picadoi. J. Proteome Res. 7, 708-719 (2008).
84. Junqueira de Azevedo ILM, Diniz MRV, Ho PL. Venom gland transcriptomic analysis. In:Animal Toxins: State of the Art. Perspectives in Health and Biotechnology . De Lima ME, Pimenta AMC, Martin-Euclaire MF, Zingali RB, Rochat H (Eds.). Editora UFMG, Belo Horizonte, Brazil, 693-713 (2009).
85. Durban J, Juárez P, Angulo Y et al. Profiling the venom gland transcriptomes of Costa Rican snakes by 454 pyrosequencing. BMC Genomics 12, 259 (2011).
86. Sanz L, Escolano J, Ferretti M 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 71, 46-60 (2008).
87. Wagstaff SC, Sanz L, Juárez P, Harrison RA, Calvete JJ. Combined snake venomics and venom gland transcriptomic analysis of the ocellated carpet viper, Echis ocellatus. J. Proteomics 71, 609-623 (2009).
88. Calvete JJ, Marcinkiewicz C, Sanz L. Snake venomics of Bitis gabonica gabonica. Protein family, composition, subunit organization of venom toxins, andcharacterization of dimeric disintegrins Bitisgabonin-1 and Bitisgabonin-2. J. Proteome Res. 6, 326-336 (2007).
89. Valente RH, Guimarães PR, Junqueira M et al. Bothrops insularis venomics: a proteomic analysis supported by transcriptomic-generated sequence data. J. Proteomics 72, 241-255 (2009).
90. WHO. Guidelines for the production, control and regulation of snake antivenom immunoglobulins. World Health Organization, Geneva, Switzerland (2009).
91. Lomonte B, Escolano J, Fernández J et al. Snake venomics and antivenomics of the arboreal neotopical pitvipers Bothriechis lateralis and Bothriehis schlegelii. J. Proteome Res. 7, 2445-2457 (2008).
92. Gutiérrez JM, León G. Snake antivenoms. Technological, clinical and public health issues. In:Animal Toxins: State of the Art. Perspectives in Health and Biotechnology . De Lima ME, Pimenta AMC, Martin-Euclaire MF, Zingali RB, Rochat H (Eds). Editora UFMG, Belo Horizonte, Brazil, 393-421 (2009).
93. Williams DJ, Gutiérrez JM, Calvete JJ et al. Ending the drought: new strategies for improving the flow of affordable, effective antivenoms in Asia and Africa. J. Proteomics 74(9), 1735-1767 (2011).
94. Campbell JA, Lamar WW. The Venomous Reptiles of the Western Hemisphere. Comstock Publishing Associates, NY, USA (2004).
95. Warrell DA. Snakebites in central and south america: epidemiology, clinical features and clinical management. In:The Venomous Reptiles of the Western Hemisphere. Campbell JA, Lamar WW (Eds.). Comstock Publishing Associates, NY, USA, 709-761 (2004).
96. Núñez V, Cid P, Sanz L 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 73, 57-78 (2009).
97. Calvete JJ, Sanz L, Pérez A 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 74, 510-527 (2011).
98. Gutiérrez JM, Sanz L, Flores-Diaz M et al. Impact of regional variation in Bothrops asper snake venom on the design of antivenoms: integrating antivenomics and neutralization approaches. J. Proteome Res. 9, 564-577 (2010).
99. Calvete JJ, Sanz L, Cid P 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. 9, 528-544 (2010).
100. Boldrini-França J, Corrêa-Netto C, Soares MM et al. Snake venomics and antivenomics of Crotalus durissus subspecies from Brazil: assessment of geographic variation and its implication on snakebite management. J. Proteomics 73, 1758-1776 (2010).
101. Saravia P, Rojas E, Arce V et al. Geographic and ontogenic variability in the venomof the neotropical rattlesnake Crotalus durissus: pathophysiological and therapeutic implications. Rev. Biol. Trop. 50, 337-346 (2002).
102. Mackessy SP. Venom composition in rattlesnakes: trends and biological significance. In:The Biology of Rattlesnakes. Hayes WK, Beaman KR, Cardwell MD, Bush SP (Eds). Loma Linda University Press, CA, USA, 495-510 (2008).
103. Fernández J, Lomonte B, Sanz L, Angulo Y, Gutiérrez JM, Calvete JJ. Snake venomics of Bothriechis nigroviridis reveals extreme variability among palm pitviper venoms: different evolutionary solutions for the same trophic purpose. J. Proteome Res. 9, 4234-4241 (2010).
104. Francischetti IM, My-Pham V, Harrison J, Garfield MK, Ribeiro JM. Bitis gabonica (Gaboon viper) snake venom gland: toward a catalog for the full-length transcripts (cDNA) and proteins. Gene 337, 55-69 (2004).
105. Cardoso KC, Da Silva MJ, Costa GG et al. A transcriptomic analysis of gene expression in the venom gland of the snake Bothrops alternatus (urutu). BMC Genomics 11, 605 (2010).
106. Junqueira-de-Azevedo IL, Ho PL. A survey of gene expression and diversity in the venom glands of the pitviper snake Bothrops insularis through the generation of expressed sequence tags (ESTs). Gene 299, 279-291 (2002).
107. Cidade DA, Simão TA, Dávila AM et al. Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern. Toxicon 48, 437-461 (2006).
108. Kashima S, Roberto PG, Soares AM et al. Analysis of Bothrops jararacussu venomous gland transcriptome focusing on structural and functional aspects: I - gene expression profile of highly expressed phospholipases A2. Biochimie 86, 211-219 (2004).
109. Neiva M, Arraes FB, de Souza JV et al. Transcriptome analysis of the Amazonian viper Bothrops atrox venom gland using expressed sequence tags (ESTs). Toxicon 53, 427-436 (2009).
110. OmPraba G, Chapeaurouge A, Doley R et al. Identification of a novel family of snake venom proteins veficolins from Cerberus rynchops using a venom gland transcriptomics and proteomics approach. J. Proteome Res. 9, 1882-1893 (2010).
111. Boldrini-França J, Rodrigues RS, Fonseca FP et al. Crotalus durissus collilineatus venom gland transcriptome: analysis of gene expression profile. Biochimie 91, 586-595 (2009).
112. Wagstaff SC, Harrison RA. Venom gland EST analysis of the saw-scaled viper, Echis ocellatus, reveals novel a9b1 integrin-binding motifs in venom metalloproteinases and a new group of putative toxins, renin-like aspartic proteases. Gene 377, 21-32 (2006).
113. Casewell NR, Harrison RA, Wüster W, Wagstaff SC. Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics 10, 564 (2009).
114. Junqueira-de-Azevedo IL, Ching AT, Carvalho E et al. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of cobra (Elapidae) venoms: implications for snake toxin repertoire evolution. Genetics 173, 877-878 (2006).
115. Pahari S, Mackessy SP, Kini RM. The venom gland transcriptome of the Desert Massasauga rattlesnake (Sistrurus catenatus edwardsii): towards an understanding of venom composition among advanced snakes (superfamily Colubroidea). BMC Mol. Biol. 8, 115 (2007).
116. Leão LI, Ho PL, Junqueira-de-Azevedo IL. Transcriptomic basis for an antiserum against Micrurus corallinus (coral snake) venom. BMC Genomics 10, 112 (2009).
117. Corrêa-Netto C, Junqueira-de-Azevedo ID, Silva D et al. Snake venomics and venom gland transcriptomic analysis of Brazilian coral snakes, Micrurus altirostris and M. corallinus. J. Proteomics 74(9), 1795-1809 (2011).
118. Warrell DA. Snake bite. Lancet 375, 77-88 (2010).
119. Gutiérrez JM, Williams D, Fan HW, Warrell DA. Snakebite envenoming from a global perspective: towards an integrated approach. Toxicon 56, 1223-1235 (2010).
120. Rokyta DR, Wray KP, Lemmon AR, Lemmon EM, Caudle SB. A high-throughput venom-gland transcriptome for the Eastern Diamondback rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon 57, 657-671 (2011).
121. Rucavado A, Escalante T, Shannon JD, Gutiérrez JM, Fox JW. Proteomics of wound exudate in snake venom-induced pathology: biomarkers to assess tissue damage and therapeutic success. J. Proteome Res. 10, 1987-2005 (2011).
122. Escalante T, Rucavado A, Pinto AF, Terra RM, Gutiérrez JM, Fox JW. Wound exudate as a proteomic window to reveal different mechanisms of tissue damage by snake venom toxins. J. Proteome Res. 8, 5120-5131 (2009).
123. Gutiérrez JM, Rucavado A, Escalante T, Lomonte B, Angulo Y, Fox JW. Tissue pathology induced by snake venoms: how to understand a complex pattern of alterations from a systems biology perspective? Toxicon 55, 166-170 (2010).
124. Burnum KE, Frappier SL, Caprioli RM. Matrix-assisted laser desorption/ ionization imaging mass spectrometry for the investigation of proteins and peptides. Annu. Rev. Anal. Chem. 1, 689-705 (2008).
125. Wagstaff SC, Favreau P, Cheneval O et al. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem. Biophys. Res. Commun. 365, 650-656 (2008).
126. Calvete JJ, Sanz L, Cid P, et al. Antivenomic assessment of the immunological reactivity of EchiTAb-Plus- ICP®, an antivenom for the treatment of snakebite envenoming in sub-Saharan Africa. Am. J. Trop. Med. Hyg. 82, 1194-1201 (2010).