A high-throughput venom-gland transcriptome for the Eastern Diamondback Rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes

Toxicon

Volumn 57, Issue 5, 2011, Pages 657-671

  Rokyta, Darin R ^a   Wray, Kenneth P ^a   Lemmon, Alan R ^a   Lemmon, Emily Moriarty ^a   Caudle, S Brian ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Crotalus adamanteus; Eastern Diamondback Rattlesnake; Positive selection; Transcriptome; Venom; Venom gland

Indexed keywords

AMINO ACID OXIDASE; CYSTEINE RICH SECRETORY PROTEIN; HYALURONIDASE; LECTIN; LYSOPHOSPHOLIPASE; METALLOPROTEINASE; MYOTOXIN; NUCLEOTIDASE; PHOSPHODIESTERASE; PHOSPHOLIPASE A2; SERINE PROTEINASE; SNAKE VENOM; TRANSCRIPTOME; UNCLASSIFIED DRUG; VENOM; VESPRYN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROTALUS ADAMANTEUS; GENE ACTIVITY; GENETIC CODE; GENETIC SELECTION; GENETIC VARIABILITY; HIGH THROUGHPUT SCREENING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POISONOUS SNAKE; PRIORITY JOURNAL; PROTEIN DATABASE; RNA SEQUENCE; SEQUENCE ANALYSIS; TOXIN ANALYSIS; TOXIN STRUCTURE; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CROTALID VENOMS; CROTALUS; GENE EXPRESSION PROFILING; GENE LIBRARY; GLYCOPROTEINS; HYALURONOGLUCOSAMINIDASE; L-AMINO ACID OXIDASE; LECTINS, C-TYPE; MOLECULAR SEQUENCE DATA; NUCLEOTIDASES; PEPTIDE HYDROLASES; PHOSPHOLIPASES A2; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

ANIMALIA; CROTALUS ADAMANTEUS; VERTEBRATA;

EID: 79953288892     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2011.01.008     Document Type: Article

References (81)

1. Aird S.D. Ophidian envenomation strategies and the role of purines. Toxicon 2002, 40:335-393.
2. 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.).
3. Anisimova M., Bielawski J.P., Yang Z. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Molecular Biology and Evolution 2001, 18:1585-1592.
4. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. Journal of Molelcular Biology 2004, 340:783-795.
5. Biardi J.E., Chien D.C., Coss R.G. California ground squirrel (Spermophilus beecheyi) defenses against rattlesnake venom digestive and hemostatic toxins. Journal of Chemical Ecology 2005, 31:2501-2518.
6. Bull J.J., Badgett M.R., Wichman H.A. Big-benefit mutations in a bacteriophage inhibited with heat. Molecular Biology and Evolution 2000, 17:942-950.
7. Calvete J.J., Juárez P., Sanz L. Snake venomics. Strategy and applications. Journal of Mass Spectrometry 2007, 42:1405-1414.
8. Casewell N.R., Harrison R.A., Wüster W., Wagstaff S.C. Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics 2009, 10:564.
9. Ching A.T.C., Rocha M.M.T., Paes Leme A.F., Pimenta D.C., Furtado M.F.D., Serrano S.M.T., Ho P.L., Junqueira-de Azevedo I.L.M. Some aspects of the venom proteome of the Colubridae snake Philodryas olfersii revealed from a Duvernoy's (venom) gland transcriptome. FEBS Letters 2006, 580:4417-4422.
10. Cidade D.A.P., Simao T.A., Dávila A.M.R., Wagner G., Junqueira-de Azevedo I.L.M., Ho P.L., Bon C., Zingali R.B., Albano R.M. Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern. Toxicon 2006, 48:437-461.
11. Conant R., Collins J.T. A Field Guide to Reptiles and Amphibians of Eastern and Central North America 1998, Houghton Mifflin Harcourt, New York, New York. third ed.
12. Crandall K.A., Kelsey C.R., Imamichi H., Lane H.C., Salzman N.P. Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Molecular Biology and Evolution 1999, 16:372-382.
13. de Azevedo I.L.M.J., Ching A.T.C., Carvalho E., Faria F., Nishiyama M.Y., Ho P.L., Diniz M.R.V. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of cobra (Elapidae) venoms: implications for snake toxin repertoire evolution. Genetics 2006, 173:877-889.
14. Deshimaru M., Ogawa T., ichi Nakashima K., Nobuhisa I., Chijiwa T., Shimohigashi Y., Fukumaki Y., Niwa M., Yamashina I., Hattori S., Ohno M. Accelerated evolution of crotalinae snake venom gland serine proteases. FEBS Letters 1996, 397:83-88.
15. 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.).
16. 2 enzymes. Handbook of Venoms and Toxins of Reptiles 2010, 173-205. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
17. Douglas M.E., Douglas M.R., Schuett G.W., Porras L.W. Evolution of rattlesnakes (Viperidae; Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and Quaternary climate change. Molecular Ecology 2006, 15:3353-3374.
18. Du X.-Y., Clemetson K.J. Reptile C-type lectins. Handbook of Venoms and Toxins of Reptiles 2010, 359-375. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
19. Dundee H.A., Rossman D.A. The Amphibians and Reptiles of Louisiana 1996, Louisiana University Press, Baton Rouge, Louisiana.
20. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2007, 2:953-971.
21. Emrich S.J., Barbazuk W.B., Li L., Schnabel P.S. Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Research 2007, 17:69-73.
22. Escoubas P., King G.F. Venomics as a drug discovery platform. Expert Review of Proteomics 2009, 6:221-224.
23. Fox J.W., Serrano S.M.T. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 2005, 45:969-985.
24. Fox J.W., Serrano S.M.T. Snake venom metalloproteinases. Handbook of Venoms and Toxins of Reptiles 2010, 95-113. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
25. Francischetti I.M.B., My-Pham V., Harrison J., Garfield M.K., Ribeiro J.M.C. Bitis gabonica (Gaboon viper) snake venom gland: toward a catalog for the full-length transcripts (cDNA) and proteins. Gene 2004, 337:55-69.
26. 2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. Journal of Molecular Evolution 2008, 66:151-166.
27. Gold B.S., Dart R.C., Barish R.A. Bites of venomous snakes. New England Journal of Medicine 2002, 347:347-356.
28. Gomis-Rüth F.-X., Kress L.F., Bode W. First structure of a snake venom metalloproteinase: a prototype for matrix metalloproteinases/collagenases. EMBO Journal 1993, 12:4151-4157.
29. Gong W., Zhu X., Liu S., Teng M., Niu L. Crystal structures of Acutolysin A, a three-disulfide hemorrhagic zinc metalloproteinase from the snake venom of Agkistrodon acutus. Journal of Molelcular Biology 1998, 283:657-668.
30. Gutiérrez J.M., Rucavado A., Escalante T. Snake venom metalloproteinases: biological roles and participation in the pathophysiology of envenomation. Handbook of Venoms and Toxins of Reptiles 2010, 115-138. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
31. Harrison R.A., Ibison F., Wilbraham D., Wagstaff S.C. Identification of cDNAs encoding viper venom hyaluronidases: cross-generic sequence conservation of full-length and unusually short variant transcripts. Gene 2007, 392:22-33.
32. Harvey A.L., Bradley K.N., Cochran S.A., Rowan E.G., Pratt J.A., Quillfeldt J.A., Jerusalinsky D.A. What can toxins tell us for drug discovery?. Toxicon 1998, 36:1635-1640.
33. Hayes M.B., Wellner D. Microheterogeneity of L-amino acid oxidase. Journal of Biological Chemistry 1969, 244:6636-6644.
34. 2 from the venom of the cottonmouth snake at 2.0-Å resolution. Journal of Biological Chemistry 1990, 265:17649-17656.
35. Jia Y., Cantu B.A., Sánchez E.E., Pérez J.C. Complementary DNA sequencing and identification of mRNAs from the venomous gland of Agkistrodon piscivorus leucostoma. Toxicon 2008, 51:1457-1466.
36. Juárez P., Comas I., González-Candelas F., Calvete J.J. Evolution of snake venom disintegrins by positive Darwinian selection. Molecular Biology and Evolution 2008, 25:2391-2407.
37. Junqueira-de Azevedo I.L.M., Ho P.L. 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 2002, 299:279-291.
38. Kemparaju K., Girish K.S., Nagaraju S. Hyaluronidases, a neglected class of glycosidases from snake venom: beyond a spreading factor. Handbook of Venoms and Toxins of Reptiles 2010, 237-258. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
39. 2 enzymes. Toxicon 2003, 42:827-840.
40. Klauber L.M. Rattlesnakes: Their Habits, Life Histories, and Influence on Mankind 1997, University of California Press, Berkeley, California. second ed.
41. Kordiš D., Gubenšek F. Adaptive evolution of animal toxin multigene families. Gene 2000, 261:43-52.
42. 2-proteinase from the venom of Trimeresurus flavoviridis. Journal of Biochemistry 1996, 119:49-57.
43. Leão L.I., Ho P.L., Junqueira-de Azevedo I.L.M. Transcriptomic basis for an antiserum against Micrurus corallinus (coral snake) venom. BMC Genomics 2009, 10:112.
44. Lou Z., Hou J., Liang X., Chen J., Qiu P., Liu Y., Li M., Rao Z., Yan G. Crystal structure of a non-hemorrhagic fibrin(ogen)olytic metalloproteinase complexed with a novel natural tri-peptide inhibitor from venom of Agkistrodon acutus. Journal of Structural Biology 2005, 152:195-203.
45. 2 genes. BMC Evolutionary Biology 2007, 7:2.
46. Mackessy S.P., Baxter L.M. Bioweapons synthesis and storage: the venom gland of front-fanged snakes. Zoologischer Anzeiger 2006, 245:147-159.
47. 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.
48. Ménez A. Functional architectures of animal toxins: a clue to drug design?. Toxicon 1998, 36:1557-1572.
49. Minin V., Abdo Z., Joyce P., Sullivan J. Performance-based selection of likelihood models for phylogeny. Systematic Biology 2003, 52:647-683.
50. Oguiura N., Boni-Mitake M., Rádis-Baptista G. New view on crotamine, a small basic polypeptide myotoxin from South American rattlesnake venom. Toxicon 2005, 46:363-370.
51. 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 Molecular Biology 2007, 8:115.
52. Palmer W.M., Braswell A.L. Reptiles of North Carolina 1995, University of North Carolina Press, Chapel Hill, North Carolina.
53. Pawelek P.D., Cheah J., Coulombe R., Macheroux P., Ghisla S., Vrielink A. The structure of L-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. EMBO Journal 2000, 19:4204-4215.
54. Phillips D.J., Swenson S.D., Francis S., Markland J. Thrombin-like snake venom serine proteinases. Handbook of Venoms and Toxins of Reptiles 2010, 139-154. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
55. Pung Y.F., Wong P.T.H., Kumar P.P., Hodgson W.C., Kini R.M. Ohanin, a novel protein from king cobra venom, induces hypolocomotion and hyperalgesia in mice. Journal of Biological Chemistry 2005, 280:13137-13147.
56. Pung Y.F., Kumar S.V., Rajagopalan N., Fry B.G., Kumar P.P., Kini R.M. Ohanin, a novel protein from king cobra venom: its cDNA and genomic organization. Gene 2006, 371:246-256.
57. Qinghua L., Xiaowei Z., Wei Y., Chenji L., Yijun H., Pengxin Q., Xingwen S., Songnian H., Guangmei Y. A catalog for transcripts in the venom gland of the Agkistrodon acutus: identification of the toxins potentially involved in coagulopathy. Biochemical and Biophysical Research Communications 2006, 341:522-531.
58. Rádis-Baptista G., Oguiura N., Hayashi M.A.F., Camargo M.E., Grego K.F., Oliveira E.B., Yamane T. Nucleotide sequence of crotamine isoform precursors from a single South American rattlesnake (Crotalus durissus terrificus). Toxicon 1999, 37:973-984.
59. Raibekas A.A., Massey V. Primary structure of the snake venom L-amino acid oxidase shows high homology with the mouse B cell interleukin 4-induced Fig1 protein. Biochemical and Biophysical Research Communications 1998, 248:476-478.
60. Rokyta D.R., Wichman H.A. Genic incompatibilities in two hybrid bacteriophages. Molecular Biology and Evolution 2009, 26:2831-2839.
61. Rokyta D.R., Burch C.L., Caudle S.B., Wichman H.A. Horizontal gene transfer and the evolution of microvirid coliphage genomes. Journal of Bacteriology 2006, 188:1134-1142.
62. Rotenberg D., Bamberger E.S., Kochva E. Studies on ribonucleic acid synthesis in the venom glands of Vipera palaestinae (Ophidia, Reptilia). Biochemical Journal 1971, 121:609-612.
63. Samejima Y., Aoki Y., Mebs D. Amino acid sequence of a myotoxin from venom of the Eastern Diamondback Rattlesnake (Crotalus adamanteus). Toxicon 1991, 29:461-468.
64. Serrano S.M.T., Maroun R.C. Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved. Toxicon 2005, 45:1115-1132.
65. Soto J.G., Powell R.L., Reyes S.R., Wolana L., Swanson L.J., Sanchez E.E., Perez J.C. Genetic variation of a disintegrin gene found in the American copperhead snake (Agkistrodon contortrix). Gene 2006, 373:1-7.
66. Swofford D.L. Phylogenetic Analysis Using Parsimony* (PAUP*), Version 4.0 1998, Sinauer Associates, Sunderland, MA.
67. Tan N.-H., Fung S.-Y. Snake venom L-amino acid oxidases. Handbook of Venoms and Toxins of Reptiles 2010, 221-235. CRC Press, Boca Raton, Florida. S.P. Mackessy (Ed.).
68. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22:4673-4680.
69. 1 integrin-binding motifs in venom metalloproteinases and a new group of putative toxins, renin-like aspartic proteases. Gene 2006, 377:21-32.
70. 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.
71. Watanabe L., Shannon J.D., Valente R.H., Rucavado A., Alape-Girón A., Kamiguti A.S., Theakston R.D.G., Fox J.W., Gutiérrez J.M., Arni R.K. Amino acid sequence and crystal structure of BaP1, a metalloproteinase from Bothrops asper snake venom that exerts multiple tissue-damaging activities. Protein Science 2003, 12:2273-2281.
72. Yamazaki Y., Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon 2004, 44:227-231.
73. Yamazaki Y., Hyodo F., Morita T. Wide distribution of cysteine-rich secretory proteins in snake venoms: isolation and cloning of novel snake venom cysteine-rich secretory proteins. Archives of Biochemistry and Biophysics 2003, 412:133-141.
74. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences 1997, 13:555-556.
75. Yang Z. PAML 4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 2007, 24:1586-1591.
76. Yang Z., Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Evolution 2000, 17:32-43.
77. Yang Z., Swanson W.J. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Molecular Biology and Evolution 2002, 19:49-57.
78. Yang Z., Nielsen R., Goldman N., Pedersen A.-M.K. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
79. Zhang D., Botos I., Gomis-Rüth F.-X., Doll R., Blood C., Njoroge F.G., Fox J.W., Bode W., Meyer E.F. Structural interaction of natural and synthetic inhibitors with the venom metalloproteinase, atrolysin C (form d). Proceedings of the National Academy of Sciences of the USA 1994, 91:8447-8451.
80. Zhang Z., Schwartz S., Wagner L., Miller W. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 2000, 7:203-214.
81. Zhang B., Liu Q., Yin W., Zhang X., Huang Y., Luo Y., Qiu P., Su X., Yu J., Hu S., Yan G. Transcriptome analysis of Deinagkistrodon acutus venomous gland focusing on cellular structure and functional aspects using expressed sequence tags. BMC Genomics 2006, 7:152.