Identical Skin Toxins by Convergent Molecular Adaptation in Frogs

Current Biology

Volumn 20, Issue 2, 2010, Pages 125-130

  Roelants, Kim ^a,b   Fry, Bryan G ^b   Norman, Janette A ^b,c   Clynen, Elke ^d   Schoofs, Liliane ^d   Bossuyt, Franky ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MUSEUM VICTORIA   (Australia)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

EVO_ECOL

Indexed keywords

CERULETIDE; TOXIN;

ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; EVOLUTION; FROG; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE HOMOLOGY; SKIN; XENOPUS;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; CAERULEIN; EVOLUTION; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RANIDAE; SEQUENCE HOMOLOGY, AMINO ACID; SKIN; TOXINS, BIOLOGICAL; XENOPUS;

ANURA; LITORIA; VERTEBRATA;

EID: 74449092525     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2009.11.015     Document Type: Article

References (40)

1. Bowie J.H., and Tyler M.J. Host defense peptides from Australian amphibians: Caerulein and other neuropeptides. In: Kastin A.J. (Ed). Handbook of Biologically Active Peptides (2006), Academic Press, San Diego, CA 283-289
2. Wechselberger C., and Kreil G. Structure of two cDNAs encoding cholecystokinin precursors from the brain of Xenopus laevis. J. Mol. Endocrinol. 14 (1995) 357-364
3. Johnsen A.H. Phylogeny of the cholecystokinin/gastrin family. Front. Neuroendocrinol. 19 (1998) 73-99
4. Vigna S.R. Evolution of the cholecystokinin and gastrin peptides and receptors. Am. Zool. 40 (2000) 287-295
5. Pincus M.R., Carty R.P., Chen J., Lubowsky J., Avitable M., Shah D., Scheraga H.A., and Murphy R.B. On the biologically active structures of cholecystokinin, little gastrin, and enkephalin in the gastrointestinal system. Proc. Natl. Acad. Sci. USA 84 (1987) 4821-4825
6. Anastasi A., Erspamer V., and Endean R. Isolation and structure of caerulein, an active decapeptide from the skin of Hyla caerulea. Experientia 23 (1967) 699-700
7. Anastasi A., Bertaccini G., Cei J.M., De Caro G., Erspamer V., and Impicciatore M. Structure and pharmacological actions of phyllocaerulein, a caerulein-like nonapeptide: Its occurrence in extracts of the skin of Phyllomedusa sauvagei and related Phyllomedusa species. Br. J. Pharmacol. 37 (1969) 198-206
8. Anastasi A., Bertaccini G., Cei J.M., De Caro G., Erspamer V., Impicciatore M., and Roseghini M. Presence of caerulein in extracts of the skin of Leptodactylus pentadactylus labyrinthicus and of Xenopus laevis. Br. J. Pharmacol. 38 (1970) 221-228
9. Montecucchi P., Falconieri Erspamer G., Visser J., and Visser J. Occurrence of Asn2, Leu5-caerulein in the skin of the African frog Hylambates maculatus. Experientia 33 (1977) 1138-1139
10. Wabnitz P.A., Bowie J.H., and Tyler M.J. Caerulein-like peptides from the skin glands of the Australian Blue Mountains tree frog Litoria citropa. Part 1. Sequence determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 13 (1999) 2498-2502
11. Richter K., Egger R., and Kreil G. Sequence of preprocaerulein cDNAs cloned from skin of Xenopus laevis. A small family of precursors containing one, three, or four copies of the final product. J. Biol. Chem. 261 (1986) 3676-3680
12. Vlasak R., Wiborg O., Richter K., Burgschwaiger S., Vuust J., and Kreil G. Conserved exon-intron organization in two different caerulein precursor genes of Xenopus laevis. Additional detection of an exon potentially coding for a new peptide. Eur. J. Biochem. 169 (1987) 53-58
13. Ali M.F., Soto A., Knoop F.C., and Conlon J.M. Antimicrobial peptides isolated from skin secretions of the diploid frog, Xenopus tropicalis (Pipidae). Biochim. Biophys. Acta 1550 (2001) 81-89
14. Johnsen A.H., Jonson L., Rourke I.J., and Rehfeld J.F. Elasmobranchs express separate cholecystokinin and gastrin genes. Proc. Natl. Acad. Sci. USA 94 (1997) 10221-10226
15. Shimodaira H., and Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16 (1999) 1114-1116
16. Goldman A.S., and Lichten M. Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc. Natl. Acad. Sci. USA 97 (2000) 9537-9542
17. McGrath C.L., Casola C., and Hahn M.W. Minimal effect of ectopic gene conversion among recent duplicates in four mammalian genomes. Genetics 182 (2009) 615-622
18. Shubin N., Tabin C., and Carroll S. Deep homology and the origins of evolutionary novelty. Nature 457 (2009) 818-823
19. Drummond A.J., Ho S.Y.W., Phillips M.J., and Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4 (2006) e88
20. San Mauro D., Vences M., Alcobendas M., Zardoya R., and Meyer A. Initial diversification of living amphibians predated the breakup of Pangaea. Am. Nat. 165 (2005) 590-599
21. Roelants K., Gower D.J., Wilkinson M., Loader S.P., Biju S.D., Guillaume K., Moriau L., and Bossuyt F. Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. USA 104 (2007) 887-892
22. Zhang J., Nielsen R., and Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22 (2005) 2472-2479
23. Rourke I.J., Rehfeld J.F., Møller M., and Johnsen A.H. Characterization of the cholecystokinin and gastrin genes from the bullfrog, Rana catesbeiana: Evolutionary conservation of primary and secondary sites of gene expression. Endocrinology 138 (1997) 1719-1727
24. Liu X., Wang Y., Cheng L., Song Y., and Lai R. Isolation and cDNA cloning of cholecystokinin from the skin of Rana nigrovittata. Peptides 28 (2007) 1540-1544
25. Prud'homme B., Gompel N., Rokas A., Kassner V.A., Williams T.M., Yeh S.D., True J.R., and Carroll S.B. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440 (2006) 1050-1053
26. Colosimo P.F., Hosemann K.E., Balabhadra S., Villarreal Jr. G., Dickson M., Grimwood J., Schmutz J., Myers R.M., Schluter D., and Kingsley D.M. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307 (2005) 1928-1933
27. Geffeney S.L., Fujimoto E., Brodie III E.D., Brodie Jr. E.D., and Ruben P.C. Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 434 (2005) 759-763
28. Feldman C.R., Brodie Jr. E.D., Brodie III E.D., and Pfrender M.E. The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc. Natl. Acad. Sci. USA 106 (2009) 13415-13420
29. Mundy N.I., Badcock N.S., Hart T., Scribner K., Janssen K., and Nadeau N.J. Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303 (2004) 1870-1873
30. Kingsley E.P., Manceau M., Wiley C.D., and Hoekstra H.E. Melanism in peromyscus is caused by independent mutations in agouti. PLoS ONE 4 (2009) e6435
31. Shapiro M.D., Summers B.R., Balabhadra S., Aldenhoven J.T., Miller A.L., Cunningham C.B., Bell M.A., and Kingsley D.M. The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr. Biol. 19 (2009) 1140-1145
32. Steiner C.C., Römpler H., Boettger L.M., Schöneberg T., and Hoekstra H.E. The genetic basis of phenotypic convergence in beach mice: Similar pigment patterns but different genes. Mol. Biol. Evol. 26 (2009) 35-45
33. Wood T.E., Burke J.M., and Rieseberg L.H. Parallel genotypic adaptation: When evolution repeats itself. Genetica 123 (2005) 157-170
34. Fry B.G., Roelants K., Champagne D.E., Scheib H., Tyndall J.D.A., King G.F., Nevalainen T.J., Norman J.A., Lewis R.J., Norton R.S., et al. The toxicogenomic multiverse: Convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics Hum. Genet. 10 (2009) 483-511
35. Aminetzach Y.T., Srouji J.R., Kong C.Y., and Hoekstra H.E. Convergent evolution of novel protein function in shrew and lizard venom. Curr. Biol. 19 (2009) 1925-1931
36. Rokas A., and Carroll S.B. Frequent and widespread parallel evolution of protein sequences. Mol. Biol. Evol. 25 (2008) 1943-1953
37. Castoe T.A., de Koning A.P.J., Kim H.-M., Gu W., Noonan B.P., Naylor G., Jiang Z.J., Parkinson C.L., and Pollock D.D. Evidence for an ancient adaptive episode of convergent molecular evolution. Proc. Natl. Acad. Sci. USA 106 (2009) 8986-8991
38. Conlon J.M., Sonnevend A., Patel M., Camasamudram V., Nowotny N., Zilahi E., Iwamuro S., Nielsen P.F., and Pál T. A melittin-related peptide from the skin of the Japanese frog, Rana tagoi, with antimicrobial and cytolytic properties. Biochem. Biophys. Res. Commun. 306 (2003) 496-500
39. Suzuki H., Conlon J.M., and Iwamuro S. Evidence that the genes encoding the melittin-related peptides in the skins of the Japanese frogs Rana sakuraii and Rana tagoi are not orthologous to bee venom melittin genes: Developmental- and tissue-dependent gene expression. Peptides 28 (2007) 2061-2068
40. Bollback J.P., and Huelsenbeck J.P. Parallel genetic evolution within and between bacteriophage species of varying degrees of divergence. Genetics 181 (2009) 225-234