Venom gland transcriptomes of two elapid snakes (Bungarus multicinctus and Naja atra) and evolution of toxin genes

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Jiang, Yu ^a,b   Li, Yan ^c   Lee, Wenhui ^a   Xu, Xun ^a   Zhang, Yue ^a   Zhao, Ruoping ^a   Zhang, Yun ^a   Wang, Wen ^a  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA BUNGAROTOXIN; COMPLEMENTARY DNA; LECTIN; NATRIURETIC FACTOR; NEUROTOXIN; PHOSPHOLIPASE A2; SERINE PROTEINASE INHIBITOR; SNAKE VENOM; THREE FINGER TOXIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; DNA LIBRARY; EXPRESSED SEQUENCE TAG; GENE STRUCTURE; GENETIC CONSERVATION; MOLECULAR PROBE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FAMILY; SEQUENCE ANALYSIS; SNAKE; TANDEM REPEAT; UNINDEXED SEQUENCE; ANIMAL; CHEMISTRY; GENE EXPRESSION PROFILING; GENETICS; MOLECULAR CLONING; MOLECULAR EVOLUTION;

BACTERIA (MICROORGANISMS); BUNGARUS; BUNGARUS MULTICINCTUS; ELAPIDAE; NAJA; NAJA ATRA; SERPENTES;

ANIMALS; BUNGARUS; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CLONING, MOLECULAR; COBRA; ELAPID VENOMS; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING;

EID: 78650724989     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-1     Document Type: Article

References (56)

1. Calvete JJ, Sanz L, Angulo Y, Lomonte B, Gutierrez JM. Venoms, venomics, antivenomics. FEBS Lett 2009, 583(11):1736-1743. 10.1016/j.febslet.2009.03.029, 19303875.
2. Fry BG, Vidal N, Norman JA, Vonk FJ, Scheib H, Ramjan SF, Kuruppu S, Fung K, Hedges SB, Richardson MK, et al. Early evolution of the venom system in lizards and snakes. Nature 2006, 439(7076):584-588. 10.1038/nature04328, 16292255.
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(2):215-246.
4. 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(2):127-136. 10.1016/j.jprot.2009.01.009, 19457354.
5. 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(3):403-420. 10.1101/gr.3228405, 551567, 15741511.
6. Kordis D, Gubensek F. Adaptive evolution of animal toxin multigene families. Gene 2000, 261(1):43-52. 10.1016/S0378-1119(00)00490-X, 11164036.
7. Fry BG, Wuster W, Kini RM, Brusic V, Khan A, Venkataraman D, Rooney AP. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J Mol Evol 2003, 57(1):110-129. 10.1007/s00239-003-2461-2, 12962311.
8. Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MA, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, et al. Evolutionary origin and development of snake fangs. Nature 2008, 454(7204):630-633. 10.1038/nature07178, 18668106.
9. Kelly C, Barker N, Villet M, Broadley D. Phylogeny, biogeography and classification of the snake superfamily Elapoidea: a rapid radiation in the late Eocene. Cladistics 2009, 25(1):38-63.
10. Pahari S, Bickford D, Fry BG, Kini RM. Expression pattern of three-finger toxin and phospholipase A2 genes in the venom glands of two sea snakes, Lapemis curtus and Acalyptophis peronii: comparison of evolution of these toxins in land snakes, sea kraits and sea snakes. BMC Evol Biol 2007, 7:175. 10.1186/1471-2148-7-175, 2174459, 17900344.
11. Doley R, Tram NN, Reza MA, Kini RM. Unusual accelerated rate of deletions and insertions in toxin genes in the venom glands of the pygmy copperhead (Austrelaps labialis) from Kangaroo island. BMC Evol Biol 2008, 8:70. 10.1186/1471-2148-8-70, 2287176, 18307759.
12. Leao LI, Ho PL, Junqueira-de-Azevedo L. Transcriptomic basis for an antiserum against Micrurus corallinus (coral snake) venom. BMC Genomics 2009, 10:112. 10.1186/1471-2164-10-112, 2662881, 19291316.
13. Ching AT, Rocha MM, Paes AF, Pimenta DC, de Fatima DFM, 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(18):4417-4422. 10.1016/j.febslet.2006.07.010, 16857193.
14. Rowan E. What does [beta]-bungarotoxin do at the neuromuscular junction?. Toxicon 2001, 39(1):107-118. 10.1016/S0041-0101(00)00159-8, 10936627.
15. Pawlak J, Mackessy SP, Sixberry NM, Stura EA, Le Du MH, Menez R, Foo CS, Menez A, Nirthanan S, Kini RM. Irditoxin, a novel covalently linked heterodimeric three-finger toxin with high taxon-specific neurotoxicity. FASEB J 2009, 23(2):534-545. 10.1096/fj.08-113555, 18952712.
16. Li J, Zhang H, Liu J, Xu K. Novel genes encoding six kinds of three-finger toxins in Ophiophagus hannah (king cobra) and function characterization of two recombinant long-chain neurotoxins. Biochem J 2006, 398(2):233-242. 10.1042/BJ20060004, 1550305, 16689684.
17. Jeyaseelan K, Poh SL, Nair R, Armugam A. Structurally conserved alpha-neurotoxin genes encode functionally diverse proteins in the venom of Naja sputatrix. FEBS Lett 2003, 553(3):333-341. 10.1016/S0014-5793(03)01039-1, 14572646.
18. Tamiya T, Fujimi TJ. Molecular evolution of toxin genes in Elapidae snakes. Mol Divers 2006, 10(4):529-543. 10.1007/s11030-006-9049-x, 17096076.
19. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591. 10.1093/molbev/msm088, 17483113.
20. Li W-H. Molecular Evolution. Sinauer 1997, Sunderland, MA.
21. Kuhn P, Deacon AM, Comsa DS, Rajaseger G, Kini RM, Uson II, Kolatkar PR. The atomic resolution structure of bucandin, a novel toxin isolated from the malayan krait, determined by direct methods. erratum. Acta Crystallogr D Biol Crystallogr 2000, 56(Pt 12):1702. 10.1107/S090744490001739X, 11092952.
22. Heinrikson RL, Krueger ET, Keim PS. Amino acid sequence of phospholipase A2-alpha from the venom of Crotalus adamanteus. A new classification of phospholipases A2 based upon structural determinants. J Biol Chem 1977, 252(14):4913-4921.
23. Fujimi TJ, Kariya Y, Tsuchiya T, Tamiya T. Nucleotide sequence of phospholipase A(2) gene expressed in snake pancreas reveals the molecular evolution of toxic phospholipase A(2) genes. Gene 2002, 292(1-2):225-231. 10.1016/S0378-1119(02)00682-0, 12119117.
24. Yuan C, He Q, Peng K, Diao J, Jiang L, Tang X, Liang S. Discovery of a distinct superfamily of Kunitz-type toxin (KTT) from tarantulas. PLoS One 2008, 3:10.
25. Harvey AL, Karlsson E. Protease inhibitor homologues from mamba venoms: facilitation of acetylcholine release and interactions with prejunctional blocking toxins. Br J Pharmacol 1982, 77(1):153-161. 2044661, 6751453.
26. Ogawa T, Chijiwa T, Oda-Ueda N, Ohno M. Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon 2005, 45(1):1-14. 10.1016/j.toxicon.2004.07.028, 15581677.
27. Matsui T, Fujimura Y, Titani K. Snake venom proteases affecting hemostasis and thrombosis. Biochim Biophys Acta 2000, 1477(1-2):146-156. 10.1016/S0167-4838(99)00268-X, 10708855.
28. Guo XX, Zeng L, Lee WH, Zhang Y, Jin Y. Isolation and cloning of a metalloproteinase from king cobra snake venom. Toxicon 2007, 49(7):954-965. 10.1016/j.toxicon.2007.01.003, 17337026.
29. Inoue K, Takei Y. Molecular evolution of the natriuretic peptide system as revealed by comparative genomics. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 2006, 1(1):69-76.
30. St Pierre L, Flight S, Masci PP, Hanchard KJ, Lewis RJ, Alewood PF, de Jersey J, Lavin MF. Cloning and characterisation of natriuretic peptides from the venom glands of Australian elapids. Biochimie 2006, 88(12):1923-1931. 10.1016/j.biochi.2006.06.014, 16908092.
31. Trajanovska S, Donald J. Molecular cloning of natriuretic peptides from the heart of reptiles: loss of ANP in diapsid reptiles and birds. General and comparative endocrinology 2008, 156(2):339-346. 10.1016/j.ygcen.2008.01.013, 18295764.
32. Baxter G. The natriuretic peptides. Basic research in cardiology 2004, 99(2):71-75. 10.1007/s00395-004-0457-8, 14963664.
33. Fry BG, Wickramaratana JC, Lemme S, Beuve A, Garbers D, Hodgson WC, Alewood P. Novel natriuretic peptides from the venom of the inland taipan (Oxyuranus microlepidotus): isolation, chemical and biological characterisation. Biochem Biophys Res Commun 2005, 327(4):1011-1015. 10.1016/j.bbrc.2004.11.171, 15652496.
34. Ho PL, Soares MB, Maack T, Gimenez I, Puorto G, Furtado MF, Raw I. Cloning of an unusual natriuretic peptide from the South American coral snake Micrurus corallinus. Eur J Biochem 1997, 250(1):144-149. 10.1111/j.1432-1033.1997.00144.x, 9432002.
35. Schweitz H, Vigne P, Moinier D, Frelin C, Lazdunski M. A new member of the natriuretic peptide family is present in the venom of the green mamba (Dendroaspis angusticeps). J Biol Chem 1992, 267(20):13928-13932.
36. Reza MA, Swarup S, Kini RM. Structure of two genes encoding parallel prothrombin activators in Tropidechis carinatus snake: gene duplication and recruitment of factor X gene to the venom gland. J Thromb Haemost 2007, 5(1):117-126. 10.1111/j.1538-7836.2006.02266.x, 17239167.
37. Li S, Wang J, Zhang X, Ren Y, Wang N, Zhao K, Chen X, Zhao C, Li X, Shao J, et al. Proteomic characterization of two snake venoms: Naja naja atra and Agkistrodon halys. Biochem J 2004, 384(Pt 1):119-127. 1134095, 15285721.
38. Kulkeaw K, Chaicumpa W, Sakolvaree Y, Tongtawe P, Tapchaisri P. Proteome and immunome of the venom of the Thai cobra, Naja kaouthia. Toxicon 2007, 49(7):1026-1041. 10.1016/j.toxicon.2007.01.019, 17379268.
39. Olamendi-Portugal T, Batista CV, Restano-Cassulini R, Pando V, Villa-Hernandez O, Zavaleta-Martinez-Vargas A, Salas-Arruz MC, Rodriguez de la Vega RC, Becerril B, Possani LD. Proteomic analysis of the venom from the fish eating coral snake Micrurus surinamensis: novel toxins, their function and phylogeny. Proteomics 2008, 8(9):1919-1932. 10.1002/pmic.200700668, 18384102.
40. Dokmetjian JC, Del Canto S, Vinzon S, de Jimenez Bonino MB. Biochemical characterization of the Micrurus pyrrhocryptus venom. Toxicon 2009, 53(3):375-382. 10.1016/j.toxicon.2008.12.015, 19135468.
41. 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.
42. De Smet W. The nuclear Feulgen-DNA content of the vertebrates (especially reptiles), as measured by fluorescence cytophotometry, with notes on the cell and chromosome size. Acta Zool Pathol Antverp 1981, 76:119-167.
43. Clarke L, Carbon J. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome. Cell 1976, 9(1):91-99. 10.1016/0092-8674(76)90055-6, 788919.
44. Fujimi TJ, Nakajyo T, Nishimura E, Ogura E, Tsuchiya T, Tamiya T. Molecular evolution and diversification of snake toxin genes, revealed by analysis of intron sequences. Gene 2003, 313:111-118. 10.1016/S0378-1119(03)00637-1, 12957382.
45. Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res 1999, 9(9):868-877. 10.1101/gr.9.9.868, 310812, 10508846.
46. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340(4):783-795. 10.1016/j.jmb.2004.05.028, 15223320.
47. Wang Z, Miyake T, Edwards SV, Amemiya CT. Tuatara (Sphenodon) genomics: BAC library construction, sequence survey, and application to the DMRT gene family. J Hered 2006, 97(6):541-548. 10.1093/jhered/esl040, 17135461.
48. Wang W, Xu HL, Lin LP, Su B, Wang YQ. Construction of a BAC library for Chinese amphioxus Branchiostoma belcheri and identification of clones containing Amphi-Pax genes. Genes Genet Syst 2005, 80(3):233-236. 10.1266/ggs.80.233, 16172535.
49. Chiu CH, Amemiya CT, Carr JL, Bhargava J, Hwang JK, Shashikant CS, Ruddle FH, Wagner GP. A recombinogenic targeting method to modify large-inserts for cis-regulatory analysis in transgenic mice: construction and expression of a 100-kb, zebrafish Hoxa-11b-lacZ reporter gene. Dev Genes Evol 2000, 210(2):105-109. 10.1007/s004270050016, 10664153.
50. Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W. A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 1998, 8(9):967-974. 310774, 9750195.
51. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
52. Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17(1):32-43.
53. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599. 10.1093/molbev/msm092, 17488738.
54. Felsenstein J. PHYLIP (phylogeny inference package) version 3.6. Distributed by the author Department of Genome Sciences, University of Washington, Seattle 2005,
55. Schmidt H, Strimmer K, Vingron M, Von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18(3):502. 10.1093/bioinformatics/18.3.502, 11934758.
56. Yang Z, Nielsen R, Goldman N, Pedersen AM. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155(1):431-449. 1461088, 10790415.