Profiling the venom gland transcriptomes of costa rican snakes by 454 pyrosequencing

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Durban, Jordi ^a   Juárez, Paula ^a   Angulo, Yamileth ^b   Lomonte, Bruno ^b   Flores Diaz, Marietta ^b   Alape Girón, Alberto ^b   Sasa, Mahmood ^b   Sanz, Libia ^a   Gutiérrez, José M ^b   Dopazo, Joaquín ^c   Conesa, Ana ^c   Calvete, Juan J ^a  

^a CSIC   (Spain)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

454 pyrosequencing; Atropoides; Bioinformatic analysis; Bothriechis; Bothrops asper; Cerrophidion; Costa rican snakes; Crotalus; Next generation high throughput dna sequencing; Snake venom gland transcriptomics

Indexed keywords

APROTININ; SNAKE VENOM; MESSENGER RNA; PROTEOME;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COSTA RICA; DNA FINGERPRINTING; GENE DOSAGE; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; NONHUMAN; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PYROSEQUENCING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SNAKE; STRUCTURAL BIOINFORMATICS; TRANSCRIPTOMICS; ANIMAL; CLASSIFICATION; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; METHODOLOGY; SALIVARY GLAND;

ATROPOIDES; ATROPOIDES PICADOI; BOTHRIECHIS; BOTHRIECHIS LATERALIS; BOTHRIECHIS SCHLEGELII; BOTHROPS; BOTHROPS ASPER; CERROPHIDION; CROTALUS; SERPENTES;

ANIMALS; COSTA RICA; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PROTEOME; RNA, MESSENGER; SALIVARY GLANDS; SEQUENCE ANALYSIS, DNA; SNAKE VENOMS; SNAKES;

EID: 79956224874     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-259     Document Type: Article

References (120)

1. Mackessy SP. Morphology and ultrastructure of the venom glands of the northern Pacific rattlesnake Crotalus viridis oreganus. J Morphol 1991, 208:109-128.
2. Fry BG, 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. 10.1093/molbev/msh091, 15014162.
3. Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SF, Vidal N, Poelmann RE, Norman JA. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics 2008, 7:215-246.
4. Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MAG, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, Mirtschin PJ, Kochva E, Witte F, Fry BG, Woods A, Richardson MK. Evolutionary origin and development of snake fangs. Nature 2008, 454:630-633. 10.1038/nature07178, 18668106.
5. Fry BG, Vidal N, Norman JA, Vonk FJ, Scheib H, Ramjan SF, Kuruppu S, Fung K, Hedges SB, Richardson MK, Hodgson WC, Ignjatovic V, Summerhayes R, Kochva E. Early evolution of the venom system in lizards and snakes. Nature 2006, 439:584-588. 10.1038/nature04328, 16292255.
6. Fry BG, Vidal N, van der Weerd L, Kochva E, Renjifo C. Evolution and diversification of the Toxicofera reptile venom system. J Proteomics 2009, 72:127-136. 10.1016/j.jprot.2009.01.009, 19457354.
7. Greene HW. Dietary correlates of the origin and radiation of snakes. Am Zool 1983, 23:431-441.
8. World Health Organization Rabies and envenomings. A neglected public health issue: Report of a consultative meeting. 2007, Geneva: WHO, World Health Organization., http://www.who.int/bloodproducts/animal_sera/Rabies.pdf
9. Kasturiratne A, Wickremasinghe AR, de Silva N, Gunawardena NK, Pathmeswaran A, Premaratna R, Savioli L, Lalloo DG, de Silva HJ. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med 2008, 5:e218. 10.1371/journal.pmed.0050218, 2577696, 18986210.
10. Chippaux JP, Goyffon M. Epidemiology of scorpionism: a global appraisal. Acta Trop 2008, 107:71-79. 10.1016/j.actatropica.2008.05.021, 18579104.
11. Koh DCI, Armugam A, Jeyaseelan K. Snake venom components and their applications in biomedicine. Cell Mol Life Sci 2006, 63:3030-3041. 10.1007/s00018-006-6315-0, 17103111.
12. Calvete JJ. Venomics: digging into the evolution of venomous systems and learning to twist nature to fight pathology. J Proteomics 2009, 72:121-126. 10.1016/j.jprot.2009.01.018, 19457346.
13. Harvey AL, Bradley KN, Cochran SA, Rowan EG, Pratt JA, Quillfeldt JA, Jerusalinsky DA. What can toxins tell us for drug discovery?. Toxicon 1998, 36:1635-1640. 10.1016/S0041-0101(98)00156-1, 9792180.
14. Ménez A. Functional architectures of animal toxins: a clue to drug design?. Toxicon 1998, 36:1557-1572. 10.1016/S0041-0101(98)00148-2, 9792172.
15. Ménez A, Stöcklin R, Mebs D. "Venomics" or: the venomous systems genome project. Toxicon 2006, 47:255-259. 10.1016/j.toxicon.2005.12.010, 16460774.
16. Escoubas P, King GF. Venomics as a drug discovery platform. Expert Rev Proteomics 2009, 6:221-224. 10.1586/epr.09.45, 19489692.
17. Vetter I, Davis JL, Rash LD, Anangi R, Mobli M, Alewood PF, Lewis RJ, King GF. Venomics: a new paradigm for natural products-based drug discovery. Amino Acids 2011, 17:15-28.
18. Gutiérrez JM, León G. Snake antivenoms: Technological, clinical and public health issues. Animal Toxins: State of the Art. Perspectives in Health and Biotechnology 2009, 393-421. Belo Horizonte: Editora UFMG, de Lima ME, Pimenta AMC, Martin-Euclaire MF, Zingali RB, Rochat H.
19. Espino-Solis GP, Riaño-Umbarila L, Becerril B, Possani LD. Antidotes against venomous animals: state of the art and prospectives. J Proteomics 2009, 72:183-199. 10.1016/j.jprot.2009.01.020, 19457345.
20. Calvete JJ, Juárez P, Sanz L. Snake venomics. Strategy and applications. J Mass Spectrom 2007, 42:1405-1414. 10.1002/jms.1242, 17621391.
21. Fox JW, Serrano SM. Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures. Proteomics 2008, 8:909-920. 10.1002/pmic.200700777, 18203266.
22. Escoubas P, Quinton L, Nicholson GM. Venomics: unravelling the complexity of animal venoms with mass spectrometry. J Mass Spectrom 2008, 43:279-295. 10.1002/jms.1389, 18302316.
23. Dos Santos LD, Santos KS, Pinto JR, Dias NB, de Souza BM, dos Santos MF, Perales J, Domont GB, Castro FM, Kalil JE, Palma MS. Profiling the proteome of the venom from the social wasp Polybia paulista: a clue to understand the envenoming mechanism. J Proteome Res 2010, 9:3867-3877. 10.1021/pr1000829, 20540563.
24. Rodríguez de la Vega RC, Schwartz EF, Possani LD. Mining on scorpion venom biodiversity. Toxicon 2009, 56:1155-1161.
25. Junqueira de Azevedo ILM, Diniz MRV, Ho PL. Venom gland transcriptomic analysis. Animal Toxins: State of the Art. Perspectives in Health and Biotechnology 2009, 693-713. Belo Horizonte: Editora UFMG, de Lima ME, Pimenta AMC, Martin-Euclaire MF, Zingali RB, Rochat H.
26. Sanz L, Escolano J, Ferretti M, Biscoglio MJ, Rivera E, Crescenti EJ, Angulo Y, Lomonte B, Gutiérrez JM, Calvete JJ. 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. 10.1016/j.jprot.2007.10.004, 18541473.
27. 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 2009, 71:609-623. 10.1016/j.jprot.2008.10.003, 19026773.
28. 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 2010, 73:932-942. 10.1016/j.jprot.2009.12.006, 20026262.
29. Ho PL, Soares MB, Yamane T, Raw I. Reverse biology applied to Micrurus corallinus, a south american coral snake. J Toxicol Toxin Reviews 1995, 14:327-337.
30. Adams MD, Kelley JM, Gocayne JD, Dubnick M, Polymeropoulos MH, Xiao H, Merril CR, Wu A, Olde B, Moreno RF, Kerlavage AR, McCombie WR, Venter JC. Complementary DNA sequencing: expressed sequence tags and human genome project. Science 1991, 252:1651-1656. 10.1126/science.2047873, 2047873.
31. Calvete JJ, 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. 10.1021/pr060494k, 17203976.
32. Valente RH, Guimarães PR, Junqueira M, Neves-Ferreira AG, Soares MR, Chapeaurouge A, Trugilho MR, León IR, Rocha SL, Oliveira-Carvalho AL, Wermelinger LS, Dutra DL, Leão LI, Junqueira-de-Azevedo IL, Ho PL, Zingali RB, Perales J, Domont GB. Bothrops insularis venomics: a proteomic analysis supported by transcriptomic-generated sequence data. J Proteomics 2009, 72:241-255. 10.1016/j.jprot.2009.01.001, 19211044.
33. Chippaux JP, Williams V, White J. Snake venom variability: methods of study, results and interpretation. Toxicon 1991, 29:1279-1303. 10.1016/0041-0101(91)90116-9, 1814005.
34. Wagstaff SC, Harrison RA. Venom gland EST analysis of the saw-scaled viper, Echis ocellatus, reveals novel α9β1 integrin-binding motifs in venom metalloproteinases and a new group of putative toxins, renin-like aspartic proteases. Gene 2006, 377:21-32.
35. Wheat CW. Rapidly developing functional genomics in ecological model systems via 454 transcriptome sequencing. Genetica 2010, 138:433-451. 10.1007/s10709-008-9326-y, 18931921.
36. Linnarsson S. Recent advances in DNA sequencing methods. General principles of sample preparation. Exp Cell Res 2010, 316:1339-1343. 10.1016/j.yexcr.2010.02.036, 20211618.
37. Morozova O, Hirst M, Marra MA. Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 2009, 10:135-151. 10.1146/annurev-genom-082908-145957, 19715439.
38. Mardis ER. The impact of next-generation sequencing technology on genetics. Trends Genet 2008, 24:133-141. 10.1016/j.tig.2007.12.007, 18262675.
39. 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. 10.1186/1471-2164-7-152, 1525187, 16776837.
40. Rokyta DR, Wray KP, Lemmon AR, Lemmon EM, Caudle SB. A high-throughput venom-gland transcriptome for the Eastern Diamond Rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon 2011, 57:657-671.
41. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10:57-63. 10.1038/nrg2484, 2949280, 19015660.
42. Gutiérrez JM. Snakebite envenomation in Central America. Handbook of Venoms and Toxins of Reptiles 2009, 491-507. CRC Press: Boca Raton, Florida, Mackessy SP.
43. Campbell JA, Lamar WW. The Venomous Reptiles of the Western Hemisphere 2004, Cornell University Press: Ithaca.
44. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Edgar R, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Khovayko O, Landsman D, Lipman DJ, Madden TL, Maglott DR, Miller V, Ostell J, Pruitt KD, Schuler GD, Shumway M, Sequeira E, Sherry ST, Sirotkin K, Souvorov A, Starchenko G, Tatusov RL, Tatusova TA, Wagner L, Yaschenko E. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2008, (36 Database):D13-21.
45. Wang W, Wang Y, Zhang Q, Qi Y, Guo D. Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. BMC Genomics 2009, 10:465. 10.1186/1471-2164-10-465, 2763888, 19818120.
46. McClintock B. Controlling elements and the gene. Cold Spring Harb Symp Quant Biol 1956, 21:197-216.
47. Bannert N, Kurth R. Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004, 101:14572-14579. 10.1073/pnas.0404838101, 521986, 15310846.
48. Deininger PL, Batzer MA. Mammalian retroelements. Genome Res 2002, 12:1455-1465. 10.1101/gr.282402, 12368238.
49. Hughes JF, Coffin JM. Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat Genet 2001, 29:487-489. 10.1038/ng775, 11704760.
50. Jern P, Coffin JM. Effects of retroviruses on host genome function. Annu Rev Genet 2008, 42:709-732. 10.1146/annurev.genet.42.110807.091501, 18694346.
51. Pi W, Zhu X, Wu M, Wang Y, Fulzele S, Eroglu A, Ling J, Tuan D. Long-range function of an intergenic retrotransposon. Proc Natl Acad Sci USA 2010, 107:12992-12997. 10.1073/pnas.1004139107, 2919959, 20615953.
52. Junqueira-de-Azevedo ILM, Ho PL. A survey of gene expression and diversity in the venom glands of the pit viper snake Bothrops insularis through the generation of expressed sequence tags (ESTs). Gene 2002, 299:279-291. 10.1016/S0378-1119(02)01080-6, 12459276.
53. Junqueira-de-Azevedo ILM, Ching ATC, Carvalho E, Faria F, Nishiyama MY, Ho PL, Diniz MRV. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of cobra (Elapidae) venoms: implications for snake toxin repertoire evolution. Genetics 2006, 172:877-889.
54. Ching AT, Rocha MM, Leme AFP, Pimenta DC, Furtado MFD, Serrano SM, Ho PL, Junqueira de Azevedo IL. Some aspects of the venom proteome of the Colubridae snake Philodryas olfersii revealed from a Duvernoy's (venom) gland transcriptome. FEBS Lett 2006, 580:4417-4422. 10.1016/j.febslet.2006.07.010, 16857193.
55. Kordis D, Gubenšek F. Bov-B long interspersed repeated DNA (LINE) sequences are present in Vipera ammodytes phospholipase A2 genes and in genomes of Viperidae snakes. Eur J Biochem 1997, 246:772-779. 10.1111/j.1432-1033.1997.00772.x, 9219538.
56. Kordis D, Gubenšek F. The Bov-B lines found in Vipera ammodytes toxic PLA2 genes are widespread in snake genomes. Toxicon 1998, 36:1585-1590. 10.1016/S0041-0101(98)00150-0, 9792174.
57. Ikeda N, Chijiwa T, Matsubara K, Oda-Ueda N, Hattori S, Matsuda Y, Ohno M. Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake. Gene 2010, 461:15-25. 10.1016/j.gene.2010.04.001, 20406671.
58. Ohno M. Evolution by gene duplication. 1970, Springer Verlag: Berlin.
59. Lynch VJ. Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol 2007, 7:2. 10.1186/1471-2148-7-2, 1783844, 17233905.
60. Gibbs HL, Rossiter W. Rapid evolution by positive selection and gene gain and loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J Mol Evol 2008, 66:151-166. 10.1007/s00239-008-9067-7, 18253686.
61. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 2003, 19:530-536. 10.1016/j.tig.2003.08.004, 14550626.
62. Medstrand P, van de Lagemaat LN, Dunn CA, Landry JR, Svenback D, Mager DL. Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet Genome Res 2005, 110:342-345. 10.1159/000084966, 16093686.
63. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829. 10.1101/gr.074492.107, 2336801, 18349386.
64. Kumar S, Blaxter ML. Comparing de novo assemblers for 454 transcriptome data. BMC Genomics 2010, 11:571. 10.1186/1471-2164-11-571, 3091720, 20950480.
65. Flicek P, Birney E. Sense from sequence reads: methods for alignment and assembly. Nature Methods 2009, 6:S6-S12. 10.1038/nmeth.1376, 19844229.
66. Liu Q, Zhang X, Yin W, Li C, Huang Y, Qiu P, Su X, Hu S, Yan G. A catalog for transcripts in the venom gland of the Agkistrodon acutus: Identification of the toxins potentially involved in coagulopathy. Biochem Biophys Res Commun 2006, 341:522-531. 10.1016/j.bbrc.2006.01.006, 16438937.
67. Naamati G, Askenazi M, Linial M. ClanTox: a classifier of short animal toxins. Nucleic Acid Res 2009, 37:W363-W368. 10.1093/nar/gkp299, 2703885, 19429697.
68. He Q, He Q, Deng X, Yao L, Meng E, Liu Z, Liang S. ATDB: a uni-database platform for animal toxins. Nucleic Acids Res 2008, 36:D293-297. 2238984, 17933766.
69. Rawlings ND, Barrett AJ, Bateman A. MEROPS: the peptidase database. Nucleic Acids Res 2010, 38:D227-233. 10.1093/nar/gkp971, 2808883, 19892822.
70. 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 2006, 47:700-714. 10.1016/j.toxicon.2006.01.022, 16574175.
71. Georgieva D, Öhler M, Seifert J, von Bergen M, Arni RK, Genov N, Betzel C. Snake venomic of Crotalus durissus terrificus. Correlation with pharmacological activities. J Proteome Res 2010, 9:2302-2316. 10.1021/pr901042p, 20205475.
72. 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 2009, 8:3055-3067. 10.1021/pr900249q, 19371136.
73. Wermelinger LS, Dutra DLS, Oliveira-Carvalho AL, Soares MR, Bloch J, Zingali RB. Fast analysis of low molecular mass compounds present in snake venom: identification of ten new pyroglutamate-containing peptides. Rapid Commun Mass Spectrom 2005, 19:1703-1708. 10.1002/rcm.1973, 15912471.
74. Menin L, Perchuć A, Favreau P, Perret F, Michalet S, Schöni R, Wilmer M, Stöcklin R. High throughput screening of bradykinin-potentiating peptides in Bothrops moojeni snake venom using precursor ion mass spectrometry. Toxicon 2008, 51:1288-1302. 10.1016/j.toxicon.2008.02.019, 18471845.
75. Munekiyo SM, Mackessy SP. Presence of peptide inhibitors in rattlesnake venoms and their effects on endogenous metalloproteases. Toxicon 2005, 45:255-263. 10.1016/j.toxicon.2004.10.009, 15683863.
76. Wagstaff SC, Favreau P, Cheneval O, Laing GD, Wilkinson MC, Miller RL, Stöckin R, Harrison RA. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun 2008, 365:650-656. 10.1016/j.bbrc.2007.11.027, 18029259.
77. Huang KF, Chiou SH, Ko TP, Wang AH-J. Determinants of the inhibition of a Taiwan habu venom metalloprotease by its endogenous inhibitors revealed by X-ray crystallography and synthetic inhibitor analogues. Eur J Biochem 2002, 269:3047-3056.
78. Castoe TA, Poole AW, Gu W, Koning J, Daza JM, Smith EN, Pollock DD. Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Mol Ecol Res 2010, 10:341-347.
79. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JDA, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, Renjifo C, Rodríguez de la Vega RC. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genom Human Genet 2009, 10:483-511.
80. Nei M, Gu X, Sitnikova T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 1997, 94:7799-7806. 10.1073/pnas.94.15.7799, 33709, 9223266.
81. Fry BG. 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. 10.1101/gr.3228405, 551567, 15741511.
82. Kashima S, Roberto PG, Soares AM, Astolfi-Filho S, Pereira JO, Giuliati S, Faria J, Xavier MAS, Fontes MRM, Giglio JR, França SC. Analysis of Bothrops jararacussu venomous gland transcriptome focusing on structural and functional aspects: gene expression profile of highly expressed phopholipases A2. Biochimie 2004, 86:211-239. 10.1016/j.biochi.2004.02.002, 15134836.
83. Cidade DAP, Simão TA, Dávila AMR, Wagner G, Junqueira-de-Azevedo ILM, Ho PL, Bon C, Zingali RB, Albano RM. Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern. Toxicon 2006, 48:437-461. 10.1016/j.toxicon.2006.07.008, 16905169.
84. Neiva M, Arraes FB, de Souza JV, Rádis-Baptista G, Prieto da Silva AR, Walter ME, Brigido MM, Yamane T, López-Lozano JL, Astolfi-Filho S. Transcriptome analysis of the Amazonian viper Bothrops atrox venom gland using expressed sequence tags (ESTs). Toxicon 2009, 53:427-4. 10.1016/j.toxicon.2009.01.006, 19708221.
85. Doley R, Kini RM. Protein complexes in snake venom. Cell Mol Life Sci 2009, 66:2851-2871. 10.1007/s00018-009-0050-2, 19495561.
86. Juárez P, Comas I, González-Candelas F, Calvete JJ. Evolution of snake venom disintegrins by positive Darwinian selection. Mol Biol Evol 2008, 25:2391-2407. 10.1093/molbev/msn179, 18701431.
87. Lu Q, Navdaev A, Clemetson JM, Clemetson KJ. Snake venom C-type lectins interacting with platelet receptors. Structure-function relationships and effects on haemostasis. Toxicon 2005, 45:1089-1098. 10.1016/j.toxicon.2005.02.022, 15876445.
88. Walker JR, Nagar B, Young NM, Hirama Y, Rini JM. X-ray crystal structure of a galactose-specific C-type lectin possessing a novel decameric quaternary structure. Biochemistry 2004, 43:3783-3792. 10.1021/bi035871a, 15049685.
89. Freedman RB, Hirst TR, Tuite MF. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 1994, 19:331-336. 10.1016/0968-0004(94)90072-8, 7940678.
90. Yao Y, Zhou Y, Wang C. Both the isomerase and chaperone activities of protein disulfide isomerase are required for the reactivation of reduced and denatured acidic phospholipase A2. EMBO J 1997, 16:651-658. 10.1093/emboj/16.3.651, 1169667, 9034346.
91. Fleischmann J, Liu H, Wu CP. Polyadenylation of ribosomal RNA by Candida albicans also involves the small subunit. BMC Mol Biol 2004, 5:17. 10.1186/1471-2199-5-17, 522811, 15461824.
92. Kuai L, Fang F, Butler JS, Sherman F. Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2004, 101:8581-8586. 10.1073/pnas.0402888101, 423237, 15173578.
93. Decuypere S, Vandesompele J, Yardley V, De Donckeri S, Laurent T, Rijal S, Llanos-Cuentas A, Chappuis F, Arevalo J, Dujardin JC. Differential polyadenylation of ribosomal RNA during post-transcriptional processing in Leishmania. Parasitology 2005, 131:121-329. 10.1017/S0031182005007341, 16038403.
94. Slomovic S, Laufer D, Geiger D, Schuster G. Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol Cell Biol 2005, 25:6427-6435. 10.1128/MCB.25.15.6427-6435.2005, 1190340, 16024781.
95. 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 2007, 8:115. 10.1186/1471-2199-8-115, 2242803, 18096037.
96. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2003, 100:3889-3894. 10.1073/pnas.0635171100, 153018, 12660367.
97. Preiss T, Baron-Benhamou J, Ansorge W, Hentze MW. Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Mol Biol 2003, 10:1039-1047.
98. MacKay VL, Li X, Flory MR, Turcott E, Law GL, Serikawa KA, Xu XL, Lee H, Goodlett DR, Aebersold R, Zhao LP, Morris DR. Gene expression in yeast responding to mating pheromone: Analysis by high-resolution translation state analysis and quantitative proteomics. Mol Cell Proteomics 2004, 3:478-489. 10.1074/mcp.M300129-MCP200, 14766929.
99. Law GL, Bickel KS, MacKay VL, Morris DR. The undertranslated transcriptome reveals widespread translational silencing by alternative 5' transcript leaders. Genome Biol 2005, 6:R111. 10.1186/gb-2005-6-13-r111, 1414110, 16420678.
100. 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 2010, 9:4234-4241. 10.1021/pr100545d, 20590130.
101. Castoe TA, Daza JM, Smith EN, Sasa MM, Kuch U, Campbell JA, Chippindale PT, Parkinson CL. Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. J Biogeogr 2009, 36:88-103.
102. Crother BI, Campbell JA, Hillis DM. Phylogeny and historical biogeography of the palm pitvipers, genus Bothriechis: biochemical and morphological evidence. Biology of the Pitvipers 1992, 1-19. Selva: Tyler, TX, Campbell JA, Brodie EDJr.
103. Kuhner MK, Felsenstein J. A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol Biol Evol 1994, 11:459-468.
104. Deng HW, Fu YX. The effects of variable mutation rates across sites on the phylogenetic estimation of effective population size or mutation rate of DNA sequences. Genetics 1996, 144:1271-1281. 1207618, 8913767.
105. Yang Z. Among-site rate variation and its impact on phylogenetic analyses. Tree 1996, 11:367-372.
106. Castoe TA, Sasa MM, Parkinson CL. Modeling nucleotide evolution at the mesoscale: the phylogeny of the Neotropical pitvipers of the Porthidium group (Viperidae: Crotalinae). Mol Phylogenet Evol 2005, 37:881-898. 10.1016/j.ympev.2005.05.013, 16024260.
107. Castoe TA, Parkinson CL. Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylogenet Evol 2006, 39:91-110. 10.1016/j.ympev.2005.12.014, 16504544.
108. Castoe TA, Chippindale PT, Campbell JA, Ammermann LK, Parkinson CL. Molecular systematics of the Middle American jumping pitvipers (genus Atropoides) and phylogeography of the Atropoides nummifer complex. Herpetologica 2003, 59:420-431.
109. Paine MJ, Desmond HP, Theakston RDG, Crampton JM. Gene expression in Echis carinatus (carpet viper) venom glands following milking. Toxicon 1992, 30:379-386. 10.1016/0041-0101(92)90534-C, 1626320.
110. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen Y, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim J, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380. 1464427, 16056220.
111. Smit AFA, Hubley R, Green P. RepeatMasker (release of January 2009). , http://repeatmasker.org
112. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
113. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610, 16081474.
114. The Gene Ontology Consortium Gene ontology: tool for the unification of biology. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651, The Gene Ontology Consortium.
115. Lomonte B, Escolano J, Fernández J, Sanz L, Angulo Y, Gutiérrez JM, Calvete JJ. Snake venomics and antivenomics of the arboreal neotropical pitvipers Bothriechis lateralis and Bothriechis schlegelii. J Proteome Res 2008, 7:2445-2457. 10.1021/pr8000139, 18444672.
116. 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 2008, 7:708-719. 10.1021/pr700610z, 18161938.
117. Alape-Girón A, Sanz L, Escolano J, Flores-Díaz M, Madrigal M, Sasa M, Calvete JJ. Snake venomics of the lancehead pitviper Bothrops asper: geographic individual and ontogenetic variations. J Proteome Res 2008, 7:3556-3571. 10.1021/pr800332p, 18557640.
118. Calvete JJ, Sanz L, Cid P, de la Torre P, Flores-Díaz M, dos Santos MC, Borges A, Bremo A, Angulo Y, Lomonte B, Alape-Girón A, Gutiérrez JM. 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. 10.1021/pr9008749, 19863078.
119. Papadopoulos JS, Agarwala R. COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 2007, 23:1073-1079. 10.1093/bioinformatics/btm076, 17332019.
120. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113. 10.1186/1471-2105-5-113, 517706, 15318951.