Evolution and diversification of the Toxicofera reptile venom system

Journal of Proteomics

Volumn 72, Issue 2, 2009, Pages 127-136

  Fry, Bryan G ^a   Vidal, Nicolas ^b   van der Weerd, Louise ^c   Kochva, Elazar ^d   Renjifo, Camila ^e  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d TEL AVIV UNIVERSITY   (Israel)

^e PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA BUNGAROTOXIN; METALLOPROTEINASE; PROTEIN SUBUNIT; SARAFOTOXIN; SNAKE VENOM; VENOM;

AMINO ACID SEQUENCE; DENTITION; EVOLUTION; GENETIC VARIABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; REPTILE; REVIEW; TOXICOFERA;

AMINO ACID SEQUENCE; ANIMALS; BAYES THEOREM; COLUBRIDAE; EVOLUTION; EVOLUTION, MOLECULAR; MAGNETIC RESONANCE IMAGING; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REPTILES; SEQUENCE HOMOLOGY, AMINO ACID; SNAKES; VENOMS; VIPERIDAE;

REPTILIA;

EID: 60149097881     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.01.009     Document Type: Review

References (88)

1. Jackson K. The evolution of venom-delivery systems in snakes. Zool J Linn Soc 137 (2003) 337-354
2. Johnson R.G. The origin and evolution of the venomous snakes. Evolution 10 1 (1956) 56-65
3. Kardong K.V. Evolutionary patterns in advanced snakes. Am Zool 20 (1980) 269-282
4. Fry B.G., Scheib H., van der Weerd L., Young B., McNaughtan J., Ramjan S.F.R., et al. Evolution of an arsenal. Mol Cell Proteomics 7 2 (2008) 215-246
5. Vidal N., and Hedges S.B. Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. C R Biol 325 9 (2002) 987-995
6. Vidal N. Colubroid systematics: Evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. J Toxicol Toxin Rev 21 1-2 (2002) 21-41
7. Beaman K.R., Beck D.D., and McGurty B.M. The Beaded Lizard (Heloderma horridum) and Gila Monster (Heloderma suspectum): A bibliography of the family Helodermatidae. Smithson Herpetol Inf Serv 136 (2006) 1-66
8. 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 439 7076 (2006) 584-588
9. Jackson K. How tubular venom-conducting fangs are formed. J Morphol 252 (2002) 291-297
10. Jackson K. The evolution of venom-conducting fangs: insights from developmental biology. Toxicon 49 7 (2007) 975-981
11. Jackson K., and Fritts T.H. Evidence from tooth surface morphology for a posterior maxillary origin of the proteroglyph fang. Amphib-Reptil 16 (1995) 273-288
12. Kochva E. The development of the venom gland in the opisthoglyph snake Telescopus fallax with remarks on Thamnophis sirtalis (Colubridae, Reptilia). Copeia (1965) 147-154
13. Kardong K.W. Colubrid snakes and Duvernoy's "venom" glands. J Toxicol Toxin Rev 21 1 y 2 (2002) 1-19
14. Taub A.M. Comparative histological studies on Duvernoy's gland of colubrid snakes. Bull Am Mus Nat Hist 138 (1967) 1-50
15. Bogert C.M. Dentitional phenomena in cobras and other elapids with notes on adaptive modifications of the fangs. Bull Am Mus Nat Hist 131 (1943) 285-360
16. Cope E.D. The crocodilians, lizards, and snakes of North America. Reports of the US National Museum (1900) 153-1270
17. Marx H., and Rabb G.B. Phyletic analysis of fifty characters of advanced snakes. Fieldiana (Zool) 63 (1972) 1-321
18. Anthony J. Essai sur l'évolution anatomique de l'appareil venimeux des ophidiens. Ann des Sci Nat Zool 11 7-53 (1955)
19. Boulenger G.A. Catalogue of snakes in the British Museum (Natural History) vol. 1 (1893), Taylor & Francis, London
20. Kardong K.V. The evolution of the venom apparatus in snakes from colubrids to viperids and elapids. Mem Inst Butanan 46 (1982) 105-118
21. Vidal N., Delmas A.S., David P., Cruaud C., Couloux A., and Hedges S.B. The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. C R Biol 330 2 (2007) 182-187
22. Fry B.G., Wuster W., Ramjan S.F.R., Jackson T., Martelli P., and Kini R.M. Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications. Rapid Commun Mass Spectrom 17 18 (2003) 2047-2062
23. Kochva E. Development of the venom gland and trigeminal muscles in Vipera palaestinae. Acta Anat 52 (1963) 49-89
24. Kochva E. Oral glands of the Reptilia. In: Gans C.K., and Gans A. (Eds). Physiology B vol. 8 (1978), Academic Press, London 43-162
25. Vonk F.J., Admiraal J.F., Jackson K., Reshef R., de Bakker M.A., Vanderschoot K., et al. Evolutionary origin and development of snake fangs. Nature 454 7204 (2008) 630-633
26. Wollberg M., Kochva E., and Underwood G. On the rictal glands of some atractaspid snakes. Herpetol J 8 (1998) 137-143
27. Vidal N., and Hedges S.B. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C R Biol 328 10-11 (2005) 1000-1008
28. 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 15 3 (2005) 403-420
29. Patthy L. Modular assembly of genes and the evolution of new functions. Genetica 118 2-3 (2003) 217-231
30. Escoubas P., and Rash L. Tarantulas: eight-legged pharmacists and combinatorial chemists. Toxicon 43 5 (2004) 555-574
31. Froy O., Sagiv T., Poreh M., Urbach D., Zilberberg N., and Gurevitz M. Dynamic diversification from a putative common ancestor of scorpion toxins affecting sodium, potassium, and chloride channels. J Mol Evol 48 2 (1999) 187-196
32. Zhu S.Y., Huys I., Dyason K., Verdonck F., and Tytgat J. Evolutionary trace analysis of scorpion toxins specific for K-channels. Proteins Struct Funct Genet 54 2 (2004) 361-370
33. Fry B.G., Wuster W., Kini R.M., Brusic V., Khan A., Venkataraman D., et al. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J Mol Evol 57 1 (2003) 110-129
34. de la Vega R.C.R., Merino E., Becerril B., and Possani L.D. Novel interactions between K+ channels and scorpion toxins. Trends Pharmacol Sci 24 5 (2003) 222-227
35. Mouhat S., Jouirou B., Mosbah A., De Waard M., and Sabatier J.M. Diversity of folds in animal toxins acting on ion channels. Biochem J 378 (2004) 717-726
36. Chimienti F., Hogg R.C., Plantard L., Lehmann C., Brakch N., Fischer J., et al. Identification of SLURP-1 as an epidermal neuromodulator explains the clinical phenotype of Mal de Meleda. Hum Mol Genet 12 22 (2003) 3017-3024
37. Ibanez-Tallon I., Miwa J.M., Wang H.L., Adams N.C., Crabtree G.W., Sine S.M., et al. Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron 33 6 (2002) 893-903
38. Miwa J.M., Ibanez-Tallon I., Crabtree G.W., Sanchez R., Sali A., Role L.W., et al. lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23 1 (1999) 105-114
39. Carsi J.M., and Potter L.T. m1-Toxin isotoxins from the green mamba (Dendroaspis angusticeps) that selectively block m1 muscarinic receptors. Toxicon 38 2 (2000) 187-198
40. Carsi J.M., Valentine H.H., and Potter L.T. m2-toxin: A selective ligand for M2 muscarinic receptors. Mol Pharmacol 56 5 (1999) 933-937
41. Rodriguezithurralde D., Mbugua P., and Karlsson E. Fasciculins, tight-binding acetylcholinesterase (ache) inhibitors isolated from Dendroaspis venoms. Arch Biol Med Exp 17 2 (1984) R173
42. de Weille J.R., Schweitz H., Maes P., Tartar A., and Lazdunski M. Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the L-type calcium channel. Proc Natl Acad Sci U S A 88 (1991) 2437-2440
43. Dryer S.E., and Chiappinelli V.A. Kappa-bungarotoxin - an intracellular study demonstrating blockade of neuronal nicotinic receptors by a snake neurotoxin. Brain Res 289 1-2 (1983) 317-321
44. Dubovskii P.V., Lesovoy D.M., Dubinnyi M.A., Konshina A.G., Utkin Y.N., Efremov R.G., et al. Interaction of three-finger toxins with phospholipid membranes: comparison of S- and P-type cytotoxins. Biochem J 387 (2005) 807-815
45. McDowell R.S., Dennis M.S., Louie A., Shuster M., Mulkerrin M.G., and Lazarus R.A. Mambin, a potent glycoprotein IIb-IIIa antagonist and platelet aggregation inhibitor structurally related to the short neurotoxins. Biochemistry 31 (1992) 4766-4772
46. Viljoen C.C., and Botes D.P. Snake-venom toxins - purification and amino-acid sequence of toxin ta2 from Dendroaspis angusticeps venom. J Biol Chem 249 2 (1974) 366-372
47. 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
48. Fox J.W., and Serrano S.M.T. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J 275 12 (2008) 3016-3030
49. Calvete J.J., Marcinkiewicz C., Monleón D., Esteve V., Celda B., Juárez P., et al. Snake venom disintegrins: evolution of structure and function. Toxicon 45 8 (2005) 1063-1074
50. Borgheresi R., Palma M.S., Ducancel F., Camargo A.C.M., and Carmona E. Expression and processing of recombinant sarafotoxins precursor in Pichia pastoris. Toxicon 39 8 (2001) 1211-1218
51. Hayashi M.A.F., Ligny-Lemaire C., Wollberg Z., Wery M., Galat A., Ogawa T., et al. Long-sarafotoxins: characterization of a new family of endothelin-like peptides. Peptides 25 8 (2004) 1243-1251
52. Barbouche R., Marrakchi N., Mabrouk K., Krifi M.N., Van Rietschoten J., Fenouillet E., et al. Anti-platelet activity of the peptides composing the Lebetin 1 family, a new class of inhibitors of platelet aggregation. Toxicon 36 12 (1998) 1939-1947
53. Soares M.R., Oliveira-Carvalho A.L., Wermelinger L.S., Zingali R.B., Ho P.L., Junqueira-de-Azevedo I.D.M., et al. Identification of novel bradykinin-potentiating peptides and C-type natriuretic peptide from Lachesis muta venom. Toxicon 46 1 (2005) 31-38
54. Wagstaff S.C., Favreau P., Cheneval O., Laing G.D., Wilkinson M.C., Miller R.L., et al. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun 365 4 (2008) 650-656
55. Teno A.M., Vieira C.A., Santoro M.M., Neves A.G.D., and Giglio J.R. Interchain disulfide bonds in crotamine self-association. J Biochem 107 6 (1990) 821-825
56. Souza D.H.F., Eugenio L.M., Fletcher J.E., Jiang M.S., Garratt R.C., Oliva G., et al. Isolation and structural characterization of a cytotoxic L-amino acid oxidase from Agkistrodon contortrix laticinctus snake venom: Preliminary crystallographic data. Arch Biochem Biophys 368 2 (1999) 285-290
57. Morita T. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon 45 8 (2005) 1099-1114
58. Juarez P., Comas I., Gonzalez-Candelas F., and Calvete J.J. Evolution of snake venom disintegrins by positive Darwinian selection. Mol Biol Evol 25 11 (2008) 2391-2407
59. Bilgrami S., Tomar S., Yadav S., Kaur P., Kumar J., Jabeen T., et al. Crystal structure of schistatin, a disintegrin homodimer from saw-scaled viper (Echis carinatus) at 2.5 angstrom resolution. J Mol Biol 341 3 (2004) 829-837
60. Osipov A.V., Kasheverov I.E., Makarova Y.V., Starkov V.G., Vorontsova O.V., Ziganshin R.K., et al. Naturally occurring disulfide-bound dimers of three-fingered toxins - a paradigm for biological activity diversification. J Biol Chem 283 21 (2008) 14571-14580
61. Grant G.A., AlRabiee R., Xu X.L., and Zhang Y.P. Critical interactions at the dimer interface of kappa-bungarotoxin, a neuronal nicotinic acetylcholine receptor antagonist. Biochemistry 36 11 (1997) 3353-3358
62. Joubert F.J., and Viljoen C.C. Snake-venom-amino-acid-sequence of the subunits of 2 reduced and s-carboxymethylated proteins(c8s2 and c9s3) from Dendroaspis angusticeps venom. Hoppe-Seyler Z Physiol Chem 360 8 (1979) 1075-1090
63. Pawlak J., Mackessy S.P., Sixberry N.M., Stura E.A., Le Du M.H., Menez R., et al. Irditoxin, a novel covalently linked heterodimeric three-finger toxin with high taxon-specific neurotoxicity. FASEB J (2008) fj.08-113555
64. Banerjee Y., Mizuguchi J., Iwanaga S., and Kini R.M. Hemextin AB complex, a unique anticoagulant protein complex from Hemachatus haemachatus (African Ringhals cobra) venom that inhibits clot initiation and factor VIIa activity. J Biol Chem 280 52 (2005) 42601-42611
65. Mancheva I., Kleinschmidt T., Aleksiev B., and Braunitzer G. Sequence homology between phospholipase and its inhibitor in snake-venom - the primary structure of phospholipase-a2 of vipoxin from the venom of the bulgarian viper (Vipera ammodytes ammodytes, serpentes). Biol Chem Hoppe-Seyler 368 4 (1987) 343-352
66. Ramazanova A.S., Zavada L.L., Starkova V.G., Kovyazina I.V., Subbotina T.F., Kostyukhina E.E., et al. Heterodimeric neurotoxic phospholipases A(2) - The first proteins from venom of recently established species Vipera nikolskii: Implication of venom composition in viper systematics. Toxicon 51 4 (2008) 524-537
67. 2+-independent catalytic mechanism. Biochim Biophys Acta Proteins Proteomics 1784 4 (2008) 591-599
68. Faure G., Choumet V., Bouchier C., Camoin L., Guillaume J.L., Monegier B., et al. The origin of the diversity of crotoxin isoforms in the venom of Crotalus durissus terrificus. Eur J Biochem 223 1 (1994) 161-164
69. 2 from cobra venom - experimental and modeling study. Protein Eng 4 2 (1990) 171-176
70. Dubourdieu D.J., Kawaguchi H., and Shier W.T. Molecular-weight variations in the diversity of phospholipase-a2 forms in reptile venoms. Toxicon 25 3 (1987) 333-343
71. Dufton M.J. Classification of elapid snake neurotoxins and cytotoxins according to chain-length - evolutionary implications. J Mol Evol 20 2 (1984) 128-134
72. Fohlman J. Comparison of 2 highly toxic australian snake-venoms - taipan (Oxyuranus s. scutellatus) and the fierce snake (Parademansia microlepidotus). Toxicon 17 2 (1979) 170-172
73. Fohlman J., Eaker D., Karlsson E., and Thesleff S. Taipoxin, an extremely potent presynaptic neurotoxin from venom of Australian snake taipan (Oxyuranus s. scutellatus) - isolation, characterization, quaternary structure and pharmacological properties. Eur J Biochem 68 2 (1976) 457-469
74. Fohlman J., Lind P., and Eaker D. Taipoxin, an extremely potent presynaptic snake-venom neurotoxin - elucidation of primary structure of acidic carbohydrate-containing taipoxin-subunit, a prophospholipase homolog. FEBS Lett 84 2 (1977) 367-371
75. Lind P. Amino-acid-sequence of the beta-1 isosubunit of taipoxin, an extremely potent pre-synaptic neurotoxin from the Australian snake taipan (Oxyuranus s. scutellatus). Eur J Biochem 128 1 (1982) 71-75
76. Lind P., and Eaker D. Amino-acid-sequence of the alpha-subunit of taipoxin, an extremely potent pre-synaptic neurotoxin from the Australian snake taipan (Oxyuranus s. scutellatus). Eur J Biochem 124 3 (1982) 441-447
77. Fry B.G., Wickramaratna J.C., Hodgson W.C., Alewood P.F., Kini R.M., Ho H., et al. Electrospray liquid chromatography/mass spectrometry fingerprinting of Acanthophis (Death Adder) venoms: taxonomic and toxinological implications. Rapid Commun Mass Spectrom 16 6 (2002) 600-608
78. Su M.J., Coulter A.R., Sutherland S.K., and Chang C.C. The pre-synaptic neuromuscular blocking effect and phospholipase-a2 activity of textilotoxin, a potent toxin isolated from the venom of the Australian brown snake, Pseudonaja textilis. Toxicon 21 1 (1983) 143-151
79. Wilson H.I., Nicholson G.M., Tyler M.I., and Howden M.E.H. Induction of giant miniature end-plate potentials during blockade of neuromuscular-transmission by textilotoxin. Naunyn-Schmiedebergs Arch Pharmacol 352 1 (1995) 79-87
80. Tyler M.I., Barnett D., Nicholson P., Spence I., and Howden M.E.H. Studies on the subunit structure of textilotoxin, a potent neurotoxin from the venom of the Australian common brown snake (Pseudonaja textilis). Biochim Biophys Acta 915 2 (1987) 210-216
81. Aquilina J.A. The major toxin from the Australian Common Brown Snake is a hexamer with unusual gas-phase dissociation properties. Proteins (2008) 10.1002/prot.22259
82. Kwong P.D., McDonald N.Q., Sigle P.B., and Hendrickson W.A. Structure of beta(2)-bungarotoxin - potassium channel binding by kunitz modules and targeted phospholipase action. Structure 3 10 (1995) 1109-1119
83. Possani L.D., Martin B.M., Yatani A., Mochcamorales J., Zamudio F.Z., Gurrola G.B., et al. Isolation and physiological characterization of taicatoxin, a complex toxin with specific effects on calcium channels. Toxicon 30 11 (1992) 1343-1364
84. Brown A.M., Yatani A., Lacerda A.E., Gurrola G.B., and Possani L.D. Neurotoxins that act selectively Studies on the subunit structure of textilotoxin, a potent neurotoxin from the venom of the Australian common brown snake (Pseudonaja textilis) on voltage-dependent cardiac calcium channels. Circ Res 61 4 Pt 2 (1987) I6-9
85. Keogh J.S., Shine R., and Donnellan S. Phylogenetic relationships of terrestrial Australo-Papuan elapid snakes (subfamily Hydrophiinae) based on cytochrome b and 16S rRNA sequences. Mol Phylogenet Evol 10 1 (1998) 67-81
86. Lawson R., Slowinski J.B., Crother B.I., and Burbrink F.T. Phylogeny of the Colubroidea (Serpentes): New evidence from mitochondrial and nuclear genes. Mol Phylogenet Evol 37 2 (2005) 581-601
87. Vidal N., Branch W.R., Pauwels O.S.G., Hedges S.B., Broadley D.G., Wink M., et al. Dissecting the major African snake radiation: a molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia). Zootaxa 1945 (2008) 51-66
88. Vidal N., and Hedges S.B. The molecular evolutionary tree of lizards, snakes, and amphisbaenians. C R Biol (2009) 10.1016/j.crvi.2008.07.010