Linking the transcriptome and proteome to characterize the venom of the eastern diamondback rattlesnake (Crotalus adamanteus)

Journal of Proteomics

Volumn 96, Issue , 2014, Pages 145-158

  Margres, Mark J ^a   McGivern, James J ^a   Wray, Kenneth P ^a   Seavy, Margaret ^a   Calvin, Kate ^b   Rokyta, Darin R ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Crotalus adamanteus; Genotype phenotype map; Liquid chromatography; Mass spectrometry; Snake venomics; Transcriptomics

Indexed keywords

MESSENGER RNA; PROTEOME; SNAKE VENOM; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CROTALUS; CROTALUS ADAMANTEUS; ELECTROSPRAY MASS SPECTROMETRY; GENE LOCUS; GENOTYPE PHENOTYPE CORRELATION; LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN DATABASE; PROTEIN SECRETION; PROTEOMICS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

CROTALUS ADAMANTEUS; GENOTYPE-PHENOTYPE MAP; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; SNAKE VENOMICS; TRANSCRIPTOMICS;

ANIMALS; CROTALID VENOMS; CROTALUS; PROTEOME; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84896956884     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.11.001     Document Type: Article

References (57)

1. Landry C., Rifkin S. The genotype-phenotype maps of systems biology and quantitative genetics: distinct but complementary. Advances in Experimental Medicine and Biology 2012, 371-398. Springer, New York, New York. O.S. Soyer (Ed.).
2. Alberch P. From genes to phenotype: dynamical systems and evolvability. Genetics 1991, 84:5-11.
3. Waddington C. Canalization of development and the inheritance of acquired characters. Nature 1942, 150:563-565.
4. Gause G. Problems of evolution. Trans Conn Acad Sci 1947, 37:17-68.
5. Bradshaw A. Evolutionary significance of phenotypic plasticity in plants. Adv Genet 1965, 13:115-155.
6. Ghazalpour A., Bennett B., Petyuk V., Orozco L., Hagopian R., Mungrue I., et al. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet 2011, 7(6):e1001393.
7. Gygi S., Rochon Y., Franza R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19(3):1720-1730.
8. Haider S., Pal R. Integrated analysis of transcriptomic and proteomic data. Curr Genomics 2013, 14:91-110.
9. Travisano M., Shaw R. Lost in the map. Evolution 2012, 67(2):305-314.
10. 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(5):870-883.
11. 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.
12. Fry B.G., Vidal N., Norman J.A., Vonk F.J., Scheib H., Ramjan S.F.R., et al. Early evolution of the venom system in lizards and snakes. Nature 2006, 439:584-588.
13. Doley R., Kini R.M. Protein complexes in snake venom. Cell Mol Life Sci 2009, 66:2851-2871.
14. Mackessy S.P. Venom composition in rattlesnakes: trends and biological significance. The Biology of Rattlesnakes 2008, 495-510. Loma Linda University Press, Loma Linda, California. W.K. Hayes, K.R. Beaman, M.D. Cardwell, S.P. Bush (Eds.).
15. Jansa S.A., Voss R.S. Adaptive evolution of the venom-targeted vWF protein in Opossums that eat pitvipers. PLoS One 2011, 6(6):e20997.
16. Rokyta D.R., Lemmon A.R., Margres M.J., Aronow K. The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics 2012, 13:312.
17. Rokyta D.R., Wray K.P., Margres M.J. The genesis of an exceptionally deadly venom in the timber rattlesnake (Crotalus horridus) revealed through comparative venom-gland transcriptomics. BMC Genomics 2013, 14:394.
18. Margres M.J., Aronow K., Loyacano J., Rokyta D.R. The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms. BMC Genomics 2013, 14:531.
19. Madrigal M., Sanz L., Flores-Diaz M., Sasa M., Nunez V., Alape-Girón A. 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. J Proteomics 2012, 77:280-297.
20. 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.
21. Fernandez J., Alape-Girón A., Angulo Y., Sanz L., Gutierrez J., Calvete J.J., et al. Venomic and antivenomic analyses of the Central American coral snake, Micrurus nigrocinctus (Elapidae). J Proteome Res 2011, 10:1816-1827.
22. Boldrini-França J., Corrêa-Netto C., Silva M.M.S., Rodrigues R.S., Torre P.D.L., Pérez A., et al. Snake venomics and antivenomics of Crotalus durissus subspecies from Brazil: assessment of geographic variation and its implication on snakebite management. J Proteomics 2010, 73:1758-1776.
23. Calvete J.J., Borges A., Segura Á., Flores-Díaz M., Alape-Girón A., Gutiérrez 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.
24. Rodrigues R.S., Boldrini-França J., Fonseca F.P.P., de la Torre P., Henrique-Silva F., Sanz L., et al. Combined snake venomics and venom gland transcriptome analysis of Bothropoides pauloensis. J Proteomics 2012, 75:2707-2720.
25. Corrêa-Netto C., Junqueira-de-Azevedo IdLM, Silva D., Ho P., Leitão-de Araújo M., Alves M., et al. Snake venomics and venom gland transcriptomic analysis of Brazilian coral snakes, Micrurus altirostris and M. corallinus. J Proteomics 2011, 74:1795-1809.
26. Sanz L., Escolano J., Ferritti 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.
27. Calvete J.J., Marcinkiewicz C., Sanz L. Snake Venomics of Bitis gabonica gabonica. Protein family composition, subunit organization of venom toxins, and characterization of dimeric disintegrins Bitisgabonin-1 and Bitisgabonin-2. J Proteome Res 2007, 6:326-336.
28. 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.
29. Vaiyapuri S., Wagstaff S., Harrison R., Gibbins J., Hutchinson E. Evolutionary analysis of novel serine proteases in the venom gland transcriptome of Bitis gabonica rhinoceros. PLoS One 2011, 6(6):e21532.
30. Klauber L.M. Rattlesnakes: their habits, life histories, and influence on mankind 1997, University of California Press, Berkeley, California.
31. Rokyta D.R., Wray K.P., Lemmon A.R., Lemmon E.M., Caudle S.B. A high-throughput venom-gland transcriptome for the eastern diamondback rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon 2011, 57:657-671.
32. McCleary R.J.R., Heard D.J. Venom extraction from anesthetized Florida cottonmouths, Agkistrodon piscivorus conanti, using a portable nerve stimulator. Toxicon 2010, 55:250-255.
33. Choo K., Tan T., Ranganathan S. A comprehensive assessment of N-terminal signal peptides prediction methods. Nucleic Acids Res 2009, vol. 10. BMC Bioinformatics, Singapore.
34. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795.
35. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2(4):953-971.
36. McNaught A., Wilkinson A. Compendium of chemical terminology: IUPAC recommendations 1997, vol. 1669. Oxford Blackwell Science, Oxford, United Kingdom.
37. 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.
38. Bernheimer A., Linder R., Weinstein S., Kim K.S. Isolation and characterization of a phospholipase B from venom of Collett's Snake, Pseudechis colletti. Toxicon 1987, 25(5):547-554.
39. Fry B.G., Casewell N.R., Wüster W., Vidal N., Young B., Jackson T.N.W. The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 2012, 60:434-448.
40. Chatrath S., Chapeaurouge A., Lin Q., Lim T., Dunstan N., Mirtschin P., et al. Identification of a novel protein from the venom of a cryptic snake Drysdalia coronoides by a combined transcriptomics and proteomics approach. J Proteome Res 2011, 10:739-750.
41. Aird S.D. Ophidian envenomation strategies and the role of purines. Toxicon 2002, 40:335-393.
42. Aird S.D. The role of purine and pyrimidine nucleosides in snake venoms. Handbook of Venoms and Toxins of Reptiles 2010, 393-419. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
43. Dhananjaya B.L., Vishwanath B.S., D'Souza C.J.M. Snake venom nucleases, nucleotidases, and phosphomonoesterases. Handbook of Venoms and Toxins of Reptiles 2010, 155-171. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
44. Pigliucci M. Genotype-phenotype mapping and the end of the 'genes as a blueprint' metaphor. Phil Trans R Soc B 2010, 365:557-566.
45. Walker J.R., Nagar B., Young N.M., Hirama T., Rini J.M. X-ray crystal structure of a galactose-specific C-type lectin possessing a novel decameric quaternary structure. Biochemistry 2004, 43:3783-3792.
46. Pahari S., Mackessy S.P., Kini R.M. 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 2007, 8:115.
47. 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.
48. Aitchison J. The statistical analysis of compositional data 1986, Chapman and Hall, London, United Kingdom.
49. Aitchison J., Barceló-Vidal C., Martín-Fernández J.A., Pawlowsky-Glahn V. Logratio analysis and compositional distance. Math Geol 2000, 32(3):271-275.
50. Aitchison J., Egozcue J.J. Compositional data analysis: where are we and where should we be heading?. Math Geol 2005, 37(7):829-850.
51. Compositional Data Analysis. Theory and Applications 2011, John Wiley & Sons, Chichester, United Kingdom. V. Pawlowsky-Glahn, A. Buccianti (Eds.).
52. Templ M., Hron K., Filzmoser P. robCompositions: an R-package for robust statistical analysis of compositional data. Theory and Applications 2011, 341-355. John Wiley & Sons, Chichester, United Kingdom. V. Pawlowsky-Glahn, A. Buccianti (Eds.).
53. Mackessy S.P. Venom ontogeny in the pacific rattlesnakes Crotalus viridis helleri and C. v. oreganus. Copeia 1988, 1988:92-101.
54. Guércio R.A.P., Shevchenko A., Schevchenko 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.
55. 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.
56. Durban J., Perez A., Sanz L., Gomez A., Bonilla F., Rodriguez S., et al. Integrated "omics" profiling indicates that miRNAs are modulators of the ontogenetic venom composition shift in the Central American rattlesnake, Crotalus simus simus. BMC Genomics 2012, 14:234.
57. Calvete J.J., Sanz L., Cid P., de la Torre P., Flores-Díaz M., Santos M.C.D., 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.