Novel venom proteins produced by differential domain-expression strategies in beaded lizards and gila monsters (genus Heloderma)

Molecular Biology and Evolution

Volumn 27, Issue 2, 2010, Pages 395-407

  Fry, Bryan G ^a   Roelants, Kim ^a,b   Winter, Kelly ^c   Hodgson, Wayne C ^c   Griesman, Laura ^a,c   Kwok, Hang Fai ^d   Scanlon, Denis ^a   Karas, John ^a   Shaw, Chris ^d   Wong, Lily ^c   Norman, Janette A ^a,e  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c MONASH UNIVERSITY   (Australia)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^e MUSEUM VICTORIA   (Australia)

Author keywords

Adaptive evolution; Byetta; Exendin; Heloderma; Molecular evolution; Protein; Toxin; Venom

Indexed keywords

BETA DEFENSIN; EXENDIN 1; EXENDIN 2; EXENDIN 3; EXENDIN 4; FOCAL ADHESION KINASE 2; GENE PRODUCT; GLUCAGON; HELOFENSIN; HELOKINESTATIN; NATRIURETIC FACTOR; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VENOM;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEADED LIZARD; BIOLOGICAL ACTIVITY; FEMALE; GENE DUPLICATION; GENETIC CODE; GENETIC VARIABILITY; HEART FUNCTION; HELODERMA SUSPECTUM; LIZARD; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROCESSING; RAT; TANDEM REPEAT;

AMINO ACID SEQUENCE; ANIMALS; AORTA, THORACIC; BAYES THEOREM; DNA, COMPLEMENTARY; FEMALE; GUINEA PIGS; ILEUM; LIZARDS; MALE; MOLECULAR SEQUENCE DATA; PEPTIDES; PHYLOGENY; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B2; SEQUENCE HOMOLOGY, AMINO ACID; VENOMS;

HELODERMA; HELODERMATIDAE; SQUAMATA;

EID: 74549160276     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp251     Document Type: Article

References (49)

1. Beaman KR, Beck DD, McGurty BM. 2006. The beaded lizard (Heloderma horridum) and Gila monster (Heloderma suspec-tum): a bibliography of the family Helodermatidae. Smithsonian Herpetol Info Serv. 136:1-66.
2. Beck DD. 2005. Biology of Gila monsters and beaded lizards. Berkeley (CA): University of California Press.
3. Bloomgren G, Braun D, Kolterman O. 2008. Exenatide and rare adverse events\-reply. N Engl J Med. 358:1971-1972.
4. Bogert CM, del Campo RM. 1956. The gila monster and its allies. The relationships, habits, and behavior of the lizards of the family Helodermatidae. Bull Am Mus Nat History. 109:1-238.
5. Bouabboud CF, Kardassakis DG. 1988. Acute myocardial-infarction following a gila monster (Heloderma suspectum cinctum) bite. West J Med. 148:577-579.
6. Brown DE, Carmony NB. 1999. Gila monster: facts and folklore of America's Aztec lizard. Salt Lake City (UT): University of Utah Press
7. Calvete JJ, Marcinkiewicz C, Monleon D, Esteve V, Celda B, Juarez P, Sanz L. 2005. Snake venom disintegrins: evolution of structure and function. Toxicon 45:1063-1074.
8. Cantrell FL. 2003. Envenomation by the Mexican beaded lizard: a case report. J Toxicol Clin Toxicol. 41:241-244.
9. Chen TB, Bjourson AJ, Orr DF, Kwok H, Rao PF, Ivanyi C, Shaw C. 2002. Unmasking venom gland transcriptomes in reptile venoms. Anal Biochem. 311:152-156.
10. Chen TB, Kwok H, Ivanyi C, Shaw C. 2006. Isolation and cloning of exendin precursor cDNAs from single samples of venom from the Mexican beaded lizard (Heloderma horridum) and the Gila monster (Heloderma suspectum). Toxicon 47:288-295.
11. Chen YQE, Drucker DJ. 1997. Tissue-specific expression of unique mRNAs that encode proglucagon-derived peptides or exendin 4 in the lizard. J Biol Chem. 272:4108-4115.
12. de la Vega RCR, Merino E, Becerril B, Possani LD. 2003. Novel interactions between K\+ channels and scorpion toxins. Trends Pharmacol Sci. 24:222-227.
13. Ducancel F, Matre V, Dupont C, Lajeunesse E, Wollberg Z, Bdolah A, Kochva E, Boulain JC, Menez A. 1993. Cloning and sequence-analysis of cdnas encoding precursors of sarafotoxins\-evidence for an unusual rosary-type organization. J Biol Chem. 268:3052-3055.
14. Eng J, Andrews PC, Kleinman WA, Singh L, Raufman JP. 1990. Purification and structure of exendin-3, a new pancreatic secretagogue isolated from Heloderma horridum venom. J Biol Chem. 265:20259-20262.
15. Eng J, Kleinman WA, Singh L, Singh G, Raufman JP. 1992. Isolation and characterization of exendin-4, an exendin-3 analog, from Heloderma suspectum venom\-further evidence for an exendin receptor on dispersed acini from guinea-pig pancreas. J Biol Chem. 267:7402-7405.
16. Ezawa K, Oota S, Saitou N. 2006. Genome-wide search of gene conversions in duplicated genes of mouse and rat. Mol Biol Evol. 23:927-940.
17. Fox JW, Serrano SMT. 2008. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 275:3016-3030.
18. Fox JW, Serrano SMT. 2009. Timeline of key events in snake venom metalloproteinase research. J Proteom. 72:200-209.
19. Fry BG. 2005. 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. 15:403-420.
20. Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SFR, Vidal N, Poelmann RE, Norman JA. 2008. Evolution of an arsenal. Mol Cell Proteom. 7:215-246.
21. Fry BG, Vidal N, Norman JA, et al. (14 co-authors). 2006. Early evolution of the venom system in lizards and snakes. Nature 439:584-588.
22. Fry BG, Wickramaratana JC, Lemme S, Beuve A, Garbers D, Hodgson WC, Alewood P. 2005. Novel natriuretic peptides from the venom of the inland taipan (Oxyuranus micro-lepidotus): isolation, chemical and biological characterisation. Biochem Biophys Res Commun. 327:1011-1015.
23. Fry BG, Wroe S, Teeuwisse W, et al. (27 co-authors). 2009. A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus. Proc Natl Acad Sci USA. 106:8969-8974.
24. Fry BG, Wuster W, Kini RM, Brusic V, Khan A, Venkataraman D, Rooney AP. 2003. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J Mol Evol. 57:110-129.
25. Grundemar L, Hakanson R. 1992. Unlike vip, the vip-related peptides pacap, helodermin and helospectin suppress electrically evoked contractions of rat vas-deferens. Regul Peptides. 40:331-337.
26. Hayashi MAF, Ligny-Lemaire C, Wollberg Z, et al. (12 co-authors). 2004. Long-sarafotoxins: characterization of a new family of endothelin-like peptides. Peptides 25:1243-1251.
27. Hooker KR, Caravati EM. 1994. Gila monster envenomation. Ann Emerg Med. 24:731-735.
28. Junqueira-de-Azevedo IDM, Ho PL. 2002. 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 299:279-291.
29. Komori Y, Nikai T, Sugihara H. 1988. Purification and characterization of a lethal toxin from the venom of Heloderma horridum horridum. Biochem Biophys Res Commun. 154:613-619.
30. Kwok HF, Chen T, O'Rourke M, Ivanyi C, Hirst D, Shaw C. 2008. Helokinestatin: a new bradykinin B-2 receptor antagonist decapeptide from lizard venom. Peptides 29:65-72.
31. Mebs D. 1969a. Purification and properties of a kinin liberating enzyme from venom of Heloderma suspectum. Naunyn-Schmiedebergs Archiv Pharmakol. 264:280.
32. Mebs D. 1969b. Isolation and properties of kallikrein from venom of gila monster (Heloderma suspectum). Hoppe-Seylers Z Physiol Chem. 350:821.
33. Mochcamorales J, Martin BM, Possani LD. 1990. Isolation and characterization of helothermine, a novel toxin from Heloderma horridum horridum (Mexican beaded lizard) venom. Toxicon 28:299-309.
34. Morrissette J, Kratzschmar J, Haendler B, et al. (11 co-authors). 1995. PRIMARY Structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors. Biophys J. 68: 2280-2288.
35. Mouhat S, Jouirou B, Mosbah A, De Waard M, Sabatier JM. 2004. Diversity of folds in animal toxins acting on ion channels. Biochem J. 378:717-726.
36. Neidigh JW, Fesinmeyer RM, Prickett KS, Andersen NH. 2001. Exendin-4 and glucagon-like-peptide-1: NMR structural comparisons in the solution and micelle-associated states. Biochemistry 40:13188-13200.
37. Nikai T, Imai K, Sugihara H, Tu AT. 1988. Isolation and characterization of horridum toxin with arginine ester hydrolase activity from Heloderma horridum (beaded lizard) venom. Arch Biochem Biophys. 264:270-280.
38. Nobile M, Magnelli V, Lagostena L, Mochcamorales J, Possani LD, Prestipino G. 1994. The toxin helothermine affects potassium currents in newborn rat cerebellar granule cells. J Membr Biol. 139:49-55.
39. Nobile M, Noceti F, Prestipino G, Possani LD. 1996. Helothermine, a lizard venom toxin, inhibits calcium current in cerebellar granules. Exp Brain Res. 110:15-20.
40. Parker DS, Raufman JP, Odonohue TL, Bledsoe M, Yoshida H, Pisano JJ. 1984. Amino-acid-sequences of helospectins, new members of the glucagon superfamily, found in gila monster venom. J Biol Chem. 259:1751-1755.
41. Soares MR, Oliveira-Carvalho AL, Wermelinger LS, Zingali RB, Ho PL, Junqueira-de-Azevedo IDM, Diniz MRV. 2005. Identification of novel bradykinin-potentiating peptides and C-type natriuretic peptide from Lachesis muta venom. Toxicon 46:31-38.
42. Strimple PD, Tomassoni AJ, Otten EJ, Bahner D. 1997. Report on envenomation by a Gila monster (Heloderma suspectum) with a discussion of venom apparatus, clinical findings, and treatment. Wild Environ Med. 8:111-116.
43. Takasaki C, Tamiya N, Bdolah A, Wollberg Z, Kochva E. 1988. Sarafotoxins-s6-several isotoxins from Atractaspis engaddensis (burrowing asp) venom that affect the heart. Toxicon 26: 543-548.
44. Tsueshita T, Onyukusel H, Sethi V, Gandhi S, Rubinstein I. 2004. Helospectin I and II evoke vasodilation in the intact peripheral microcirculation. Peptides 25:65-69.
45. Uddman R, Goadsby PJ, Jansen-Olesen I, Edvinsson L. 1999. Helospectin-like peptides: immunochemical localization and effects on isolated cerebral arteries and on local cerebral blood flow in the cat. J Cereb Blood Flow Metab. 19:61-67.
46. Utaisincharoen P, Mackessy SP, Miller RA, Tu AT. 1993. Complete primary structure and biochemical-properties of gilatoxin, a serine-protease with kallikrein-like and angiotensin-degrading activities. J Biol Chem. 268:21975-21983.
47. Vidal N, Hedges SB. 2005. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C R Biol. 328:1000-1008.
48. Wagstaff SC, Favreau P, Cheneval O, Laing GD, Wilkinson MC, Miller RL, Stocklin R, Harrison RA. 2008. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun. 365:650-656.
49. Wagstaff SC, Harrison RA. 2006. Venom gland EST analysis of the saw-scaled viper, Echis ocellatus, reveals novel alpha(9)beta(1) integrin-binding motifs in venom metalloproteinases and a new group of putative toxins, renin-like aspartic proteases. Gene 377:21-32.