Transcriptome analysis of the Amazonian viper Bothrops atrox venom gland using expressed sequence tags (ESTs)

Toxicon

Volumn 53, Issue 4, 2009, Pages 427-436

  Neiva, Márcia ^a,b   Arraes, Fabricio B M ^e   de Souza, Jonso Vieira ^a   Rádis Baptista, Gandhi ^d   Prieto da Silva, Álvaro R B ^f   Walter, Maria Emilia M T ^e   Brigido, Marcelo de Macedo ^e   Yamane, Tetsuo ^c   López Lozano, Jorge Luiz ^g   Astolfi Filho, Spartaco ^a  

^a FEDERAL UNIVERSITY OF AMAZONAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Centro de Biotecnologia da Amazonia   (Brazil)

^d FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^e UNIVERSITY OF BRASILIA   (Brazil)

^f INSTITUTO BUTANTAN   (Brazil)

^g Instituto de Pesquisa Clínica Carlos Borborema   (Brazil)

Author keywords

Bothrops atrox; ESTs; Pit viper; Snake venom; Transcriptome; Venom toxins

Indexed keywords

BATROXOBIN; COMPLEMENTARY DNA; METALLOPROTEINASE; PHOSPHOLIPASE A2; VIPER VENOM;

ANIMAL EXPERIMENT; ARTICLE; BIOINFORMATICS; BLEEDING; BOTHROPS JARARACA; BOTHROPS JARARACUSSU; EXPRESSED SEQUENCE TAG; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; MALE; NONHUMAN; PARROT; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RAIN FOREST; SNAKE; SPECIES DIVERSITY; TRANSCRIPTOMICS;

ANIMALS; BOTHROPS; CROTALID VENOMS; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; MALE;

BOTHROPS; BOTHROPS ATROX; BOTHROPS INSULARIS; BOTHROPS JARARACA; BOTHROPS JARARACUSSU; CROTALINAE; VIPERINAE;

EID: 60749105470     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.01.006     Document Type: Article

References (68)

1. Alape-Giron A., Sanz L., Escolano J., Flores-Díaz M., Madrigal M., Sasa M., and Calvete J.J. Snake enomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J. Proteome Res. 7 (2008) 3556-3571
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Andrião-Escarso S.H., Soares A.M., Rodrigues V.M., Angulo Y., Diaz C., Lomonte B., Gutiérrez J.M., and Giglio J.R. Myotoxic phospholipases A2 in Bothrops snake venoms: effect of chemical modifications on the enzymatic and pharmacological properties of bothropstoxins from Bothrops jararacussu. Biochimie 82 (2000) 755-763
4. Arocas V., Castro H.C., Zingali R.B., Guillin M.C., Jandrot-Perrus M., Bon C., and Wisner A. Molecular cloning and expression of bothrojaracin, a potent thrombin inhibitor from snake venom. Eur. J. Biochem. 248 (1997) 550-557
5. Brígido M.M., Walter M.E., Oliveira A.G., Inoue M.K., Anjos D.S., Sandes E.F., Gondim J.J., Carvalho M.J., Almeida Jr. N.F., and Felipe M.S. Bioinformatics of the Paracoccidioides brasiliensis EST Project. Genet. Mol. Res. 4 (2005) 203-215
6. Castoe T.A., and Parkinson C.L. Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol. Phylogenet. Evol. 39 (2006) 91-110
7. Chippaux J.P., Williams V., and White J. Snake venom variability: methods of study, results and interpretation. Toxicon 29 (1991) 1279-1303
8. Cidade D.A.P., Simão T.A., Dávila A.M.R., Wagner G., Junqueira-de-Azevedo I.L.M., Ho P.L., Bond C., Zingalie R.B., and Albano R.M. Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern. Toxicon 48 (2006) 437-461
9. Cordella-Miele E., Miele L., and Mukherjee A.B. Identification of a specific region of low molecular weight phospholipases A2 (residues 21-40) as a potential target for structure-based design of inhibitors of these enzymes. PNAS 90 (1993) 10290-10294
10. Daltry J.C., Wuster W., and Thorpe R.S. Diet and snake venom evolution. Lett. Nat. 379 (1996) 537-540
11. Duvernell D.D., and Turner B.J. Swimmer 1, a new low-copy-number LINE family in teleost genomes with sequence similarity to mammalian L1. Mol. Biol. Evol. 15 (1998) 1791-1793
12. Dunn R.D., and Broady K.W. Snake inhibitors of phospholipase A2 enzymes. Biochimica et Biophysica Acta 1533 (2001) 29-37
13. Fernandez J.H., Neshich G., and Camargo A.C.M. Using bradykinin-potentiating peptide structures to develop new antihypertensive drugs. Genet. Mol. Res. 3 (2004) 554-563
14. Fernandez J.H., Silva C.A., Assakura M.T., Camargo A.C.M., and Serrano S.M.T. Molecular cloning, functional expression and molecular modeling of bothrostatin, a new highly active disintegrin from Bothrops jararaca venom. Biochem. Biophys. Res. Commun. 329 (2005) 457-464
15. Fox J.W., and Serrano S.M.T. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 45 (2005) 969-985
16. Francischetti I.M., My-Pham V., Harrison J., Garfield M.K., and Ribeiro J.M. Bitis gabonica (Gaboon viper) snake venom gland: toward a catalog for the full-length transcripts (cDNA) and proteins. Gene 337 (2004) 55-69
17. Freedman R.B., Hirst T.R., and Tuite M.F. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19 (1994) 331-336
18. Furtado M.F., Travaglia-Cardoso S.R., and Rocha M.M. Sexual dimorphism in venom of Bothrops jararaca (Serpentes:Viperidae). Toxicon 48 (2006) 401-410
19. Green P. PHRAP Documentation (1996), University of Washington, Seattle. http://bozeman.mbt.washington.edu/phrap.docs/phrap.html Available from:
20. Guércio R.A.P., Shevchenko A., Shevchenko A., López-Lozano J.L., Paba J., Sousa M.V., and Ricart C.A.O. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox. Proteome Sci. 4 (2006) 11
21. Gutiérrez J.M., Rucavado A., Escalante T., and Díaz C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon 45 (2005) 997-1011
22. Hayashi M.A.F., and Camargo A.C.M. The bradykinin-potentiating peptides from venom gland and brain of Bothrops jararaca contain highly site specific inhibitors of the somatic angiotensin-converting enzyme. Toxicon 45 (2005) 1163-1170
23. Hirabayashi J., Kusunoki T., and Kasai K. Complete primary structure of a galactose-specific lectin from the venom of the rattlesnake Crotalus atrox. Homologies with Ca2C-dependenttype lectins. J. Biol. Chem. 266 4 (1991) 2320-2326
24. Hite L.A., Jia L.G., Bjarnason J.B., and Fox J.W. cDNA sequences for four snake venom metalloproteinases: structure, classification and their relationship to mammalian reproductive proteins. Arch. Biochem. Biophys. 308 (1994) 182-191
25. Huang X., and Madan A. CAP3: a DNA sequence assembly program. Genome Res. 9 (1999) 868-877
26. Itoh N., Tanaka N., Mihashi S., and Yamashina I. Molecular cloning and sequence analysis of cDNA for batroxobin, a thrombin-like snake venom enzyme. J. Biol. Chem. 262 (1987) 3132-3135
27. Jia L.G., Wang X.M., Shannon J.D., Bjarnason J.B., and Fox J.W. Inhibition of platelet aggregation by the recombinant cysteine-rich domain of the hemorragic snake venom metalloproteinase, atrolysin A. Arch. Biochem. Biophys. 373 (2000) 281-286
28. Junqueira-de-Azevedo, I.L.M., Ching, A.T.C., Carvalho, E., Faria, F., Nishiyama, Jr. M.Y., Ho, P.L., Diniz, M.R.V., 2006. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of Cobra (Elapidae) venoms: implications for snake toxin repertoire evolution genetics. 173, 877-889.
29. Junqueira-de-Azevedo I.L.M., and 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 299 (2002) 279-291
30. Junqueira-de-Azevedo I.L.M., Farsky S.H.P., Oliveira M.L.S., and Ho P.L. Molecular cloning and expression of a functional snake venom vascular endothelium growth factor (VEGF) from the Bothrops insularis, pit viper. J. Biol. Chem. 276 (2001) 39836-39842
31. Kamiguti A.S., Gallagher P., Marcinkiewicz C., Theakston R.D.G., Zuzel M., and Fox J.W. Identification of sites in the cysteine-rich domain of the class PIII snake venom metalloproteinases responsible for inhibition of platelet function. FEBS Lett. 549 (2003) 129-134
32. Kashima S., Roberto P.G., Soares A.M., Astolfi-Filho S., Pereira J.O., Giuliati S., Faria Jr. M., Xavier M.A.S., Fontes M.R.M., Giglio J.R., and França S.C. Analysis of Bothrops jararacussu venomous gland transcriptome focusing on structural and functional aspects1: I - gene expression profile of highly expressed phospholipases A2. Biochimie 86 (2004) 211-219
33. Kini R.M., and Chan Y.M. Accelerated evolution and molecular surface of venom phospholipase A2 enzymes. J. Mol. Evol. 48 (1999) 125-132
34. Kishimoto M., and Takahashi T. Molecular cloning of HR1a and HR1b, high molecular hemorrhagic factors, from Trimeresurus flavoviridis venom. Toxicon 40 (2002) 1369-1375
35. Lee W.H., Zhuang Q.Y., and Zhang Y. Cloning and characterization of a blood coagulation factor IX-binding protein from the venom of Trimeresurus stejnegeri. Toxicon 41 (2003) 765-772
36. Long M. A new function evolved from gene fusion. Genome Res. 10 (2000) 1655-1657
37. Long M., Betran E., Thornton K., and Wang W. The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4 (2003) 865-875
38. López-Lozano J.L., Sousa M.V., Ricart C.A., Chávez-Olortégui C., Sanchez E.F., Muniz E., Buhrnheim P.F., and Morhy L. Ontogenetic variation of metalloproteinases and plasma coagulant activity in venoms of wild Bothrops atrox specimens from Amazonian rain forest. Toxicon 40 (2002) 997-1006
39. Markland F.S. Snake venoms and the hemostatic system. Toxicon 36 (1998) 1749-1800
40. Matsui T., Fujimura Y., and Titani K. Snake venom proteases affecting hemostasis and thrombosis. Biochim. Biophys. Acta 1477 (2000) 146-156
41. Masuda S., Hayashi H., Atoda H., Morita T., and Araki S. Purification, cDNA cloning and characterization of the vascular apoptosis-inducing protein, HV1, from Trimeresurus flavoviridis. Eur. J. Biochem. 268 11 (2001) 3339-3345
42. Melgarejo A.R. Serpentes peçonhentas do Brasil. In: Cardoso J.L.C., França F.O.S., Wen F.H., Malaque C.M.S., and Haddad Jr. V. (Eds). Animais peçonhentos no Brasil: biologia, clínica e terapêutica dos acidentes (2003), Sarvier, São Paulo 72-86
43. Oispov A.V., Levashov M.Y., Tsetlin V.I., and Utkin Y.N. Cobra venom contains a pool of cysteine-rich secretory proteins. Biochem. Biophys. Res. Commun. 328 (2005) 177-182
44. Otero-Patiño R., Cardoso J.L.C., Higashi H.G., Nunez V., Diaz A., Toro M.F., Garcia M.E., Sierra A., Garcia L.F., Moreno A.M., Medina M.C., Castañeda N., Silva-Diaz J.F., Murcia M., Cardenas S.Y., Dias da Silva W.D., and The Regional Group on Antivenom Therapy Research (Regather). A randomized, blinded, comparative trial of one pepsin-digested and two whole IgG antivenoms for Bothrops snake bites in uraba, Colombia. Am. J. Trop. Med. Hyg. 58 2 (1998) 183-189
45. Pahari S., Mackessy S.P., and 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. 8 (2007) 115
46. Paine M.J., Desmond H.P., Theakston R.D., and Crampton J.M. Purification, cloning, and molecular characterization of a high molecular weight hemorragic metalloproteinase, jararhagin, from Bothrops jararaca venom. Insights into the disintegrin gene family. J. Biol. Chem. 267 (1992) 22869-22876
47. Pardal P.P.d.O., Souza S.M., Monteiro M.R.C.d.C., Fan H.W., Cardoso J.L.C., França F.O.S., Tomy S.C., Sano-Martins I.S., Sousa-e-Silva M.C.C., Colombini M., Kodera N.F., Moura-da-Silva A., Cardoso D.F., Velarde D.T., Kamiguti A.S., Theakston R.D.G., and Warrell R.D.G. Clinical trial of two antivenoms for the treatment of Bothrops and Lachesis bites in the north-eastern Amazon region of Brazil. Trans. R. Soc. Trop. Med. Hyg. 98 (1994) 28-42
48. Saguchi K., Hagiwara-Saguchi Y., Murayama N., Ohi H., Fujita Y., Camargo A.C., Serrano S.M., and Higuchi S. Molecular cloning of serine proteinases from Bothrops jararaca venom gland. Toxicon 46 (2005) 72-83
49. Salazar A.M., Rodriguez-Acosta A., Girón M.E., Aguilar I., and Guerrero B. A comparative analysis of the clotting and fibrinolytic activities of the snake venom (Bothrops atrox) from different geographical areas in Venezuela. Thromb. Res. 120 (2007) 95-104
50. Saldarriaga M.M., Otero R., Núñez V., Toro M.F., Díaz A., and Gutiérrez J.M. Ontogenetic variability of Bothrops atrox and Bothrops asper snake venoms from Colômbia. Toxicon (2003) 405-411
51. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: a Laboratory Manual. second ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
52. Sanger F., Nicklen S., and Calson A.R. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 5463-5467
53. Schultz J., Copley R.R., Doerks T., Ponting C.P., and Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28 (2000) 231-234
54. 2+ and requires an intact N-terminal domain. Mol. Biol. Cell 7 9 (1996) 1359-1374
55. Sen U., Vasudevan S., Subbarao G., McClintock R.A., Celikel R., Ruggeri Z.M., and Varughese K.I. Crystal structure of the von Willebrand factor modulator botrocetin. Biochemistry 40 (2001) 345-352
56. Shin Y., Okuyama I., Hasegawa J., and Morita T. Molecular cloning of glycoprotein Ib-binding protein, flavocetin A, which inhibits platelet aggregation. Thromb. Res. 99 (2000) 239-247
57. Takeya H., Nishida S., Miyata T., Kawada S., Saisaka Y., Morita T., and Iwanaga S. Coagulation factor X activating enzyme from Russell's viper venom (RW-X). A novel metalloproteinase with disintegrin (platelet aggregation inhibitor)-like and C-type lectin-like domains. J. Biol. Chem. 267 (1992) 14109-14117
58. Trummal K., Tonismagi K., Siigur E., Aaspollu A., Lopp A., Sillat T., Saat R., Kasak L., Tammiste I., Kogerman P., Kalkkinen N., and Siigur J. A novel metalloprotease from Vipera lebetina venom induces human endothelial cell apoptosis. Toxicon 46 (2005) 46-61
59. Usami Y., Fujimura Y., Suzuki M., Ozeki Y., Nishio K., Fukui H., and Titani K. Primary structure of two-chain botrocetin, a von Willebrand factor modulator purified from the venom of Bothrops jararaca. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 928-932
60. Vasconcelos A.T.R., and Brazilian National Genome Project Consortium. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 11660-11665
61. Wang S.H., Shen X.C., Yang G.Z., and Wu X.F. cDNA cloning and characterization of Agkistin, a new metalloproteinase from Agkistrodon halys. Biochem. Biophys. Res. Commun. 301 (2003) 298-303
62. Weis W.I., Kahn R., Fourme R., Drickamer K., and Hendrickson W.A. Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science 254 (1991) 1608-1615
63. Weis W.I., Drickamer K., and Hendrickson W.A. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360 (1992) 127-134
64. Yamazaki Y., and Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon 44 (2004) 227-231
65. You K., Seo H.J., Chung K.H., and Kim D.S. A novel metalloprotease from Gloydius halys venom induces endothelial cell apoptosis through its protease and disintegrin-like domains. J. Biochem. 134 5 (2003) 739-749
66. Zha X.D., Huang H.S., Zhou L.Z., and Xu K.S. Thrombin-like enzymes from venom gland of Deinagkistrodon acutus: cDNA cloning, mechanism of diversity and phylogenetic tree construction. Acta Pharmacologica Sinica 27 (2006) 184-192
67. Zhang B., Liu Q., Yin W., Zhang X., Huang Y., Luo Y., Qiu P., Su X., Yu J., Hu S., and Yan G. Transcriptome analysis of Deinagkistrodon acutus venomous gland focusing on cellular structure and functional aspects using expressed sequence tags. BMC Genomics 7 (2006) 152
68. Zuliani J.P., Fernandes C.M., Zamuner S.R., Gutiérrez J.M., and Teixeira C.F.P. Inflammatory events induced by Lys-49 and Asp-49 phospholipases A2 isolated from Bothrops asper snake venom: role of catalytic activity. Toxicon 45 (2005) 335-346