Host-defence peptides of Australian anurans: Structure, mechanism of action and evolutionary significance

Peptides

Volumn 25, Issue 6, 2004, Pages 1035-1054

  Apponyi, Margit A ^a   Pukala, Tara L ^a   Brinkworth, Craig S ^a   Maselli, Vita M ^a   Bowie, John H ^a   Tyler, Michael J ^a   Booker, Grant W ^a   Wallace, John C ^a   Carver, John A ^b   Separovic, Frances ^c   Doyle, Jason ^d   Llewellyn, Lyndon E ^d  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Australian amphibians; Bioactive peptides; Evolution; Host defence peptides; Mass spectrometry; NMR; Pheromones; Skin secretions

Indexed keywords

ANTIFUNGAL AGENT; ANTIMALARIAL AGENT; AUREIN; CAERIDIN; CAERIN; CERULETIDE; CITROPIN; DAHLEIN; DYNASTIN; ELECTRIN; FLETCHERIN; FRENATIN; LESUEURIN; MACULATIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEPTIDE; POLYPEPTIDE ANTIBIOTIC AGENT; ROTHEIN; RUBELLIDIN; SEX PHEROMONE; SIGNIFERIN; SIGNIFERIN 1; SPLENDIPHERIN; TIGERININ; TRYPTOPHYLLIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; UPERIN; UPEROLEIN; VASOPRESSIN;

ANTIFUNGAL ACTIVITY; ANTIMALARIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; DNA FINGERPRINTING; FROG; HOST RESISTANCE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN STRUCTURE; REVIEW; SMOOTH MUSCLE; SPECIES DIFFERENTIATION; SPECIES IDENTIFICATION; TOAD;

ANIMALS; ANURA; AUSTRALIA; EVOLUTION; PEPTIDES;

AMPHIBIA; ANURA; MYOBATRACHIDAE;

EID: 2942597681     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2004.03.006     Document Type: Review

References (113)

1. Anastasi A., Erspamer V., Endean R. Isolation and amino acid sequence of caerulein, the active decapeptide of the skin of Hyla caerulea. Arch. Biochem. Biophys. 125:1968;57-68
2. Andreu D., Ubach J., Boman A., Wahlin B., Wade D., Merrifield R.B., et al. Shortened cecropin A-melittin hybrids - significant size reduction retains potent antibiotic activity. FEBS Lett. 296:1992;190-194
3. Apponyi MA, Booker GW, Bowie JH. Unpublished observations.
4. Apponyi MA, Bowie JH. Unpublished observations.
5. Barker J, Grigg GC, Tyler MJ. A field guide to Australian frogs. NSW: Surrey Beatty and Sons; 1995.
6. Barra D., Simmaco M. Amphibian skin: a promising resource for antimicrobial peptides. TIBTECH. 13:1995;205-209
7. Barsukov IL, Lian L. Structure determination from NMR data. I. Analysis of NMR data. In: Roberts, GCK, editor. NMR of macromolecules: a practical approach. New York: Oxford University Press; 1993. p. 315-57.
8. Bevins C.L., Zasloff M. Peptides from frog skin. Annu. Rev. Biochem. 59:1990;395-414
9. Biemann K., Martin S.A. Mass spectrometric determination of the amino acid sequence of peptides and proteins. Mass Spectrom. Rev. 6:1987;1-76
10. Billiar T.R. Nitric oxide, novel biology with clinical relevance. Ann. Surg. 221:1995;339-349
11. Bilusich D., Brinkworth C.S., McAnoy A.M., Bowie J.H. The fragmentation of (M-H)-anions derived from underivatized peptides. The side chain loss of H2S from Cys. A joint experimental and theoretical study. Rapid Commun. Mass Spectrom. 17:2003;2488-2494
12. Birch MC. Pheromones 32. Amsterdam: North-Holland; 1974.
13. Bowie J.H., Brinkworth C.S., Dua S. Collision-induced fragmentations of the (M-H)-parent anions of underivatized peptides: an aid to structure determination and some unusual negative ion cleavages. Mass Spectrom. Rev. 21:2002;87-107
14. Bowie J.H., Chia B.C.S., Tyler M.J. Host defence peptides from the skin glands of Australian amphibians: a powerful chemical arsenal. Pharmacol. News. 5:1998;16-21
15. Bowie J.H., Wegener K.L., Chia B.C.S., Wabnitz P.A., Carver J.A., Tyler M.J., et al. Host defence antibacterial peptides from skin secretions of Australian amphibians. The relationship between structure and activity. Protein Peptide Lett. 6:1999;259-270
16. Bradford A.M., Bowie J.H., Tyler M.J., Wallace J.C. New antibiotic uperin peptides from the dorsal glands of the Australian toadlet Uperoleia mjobergii. Aust. J. Chem. 49:1996;1325-1331
17. Bradford A.M., Raftery M.J., Bowie J.H., Tyler M.J., Wallace J.C., Adams G.W., et al. Novel uperin peptides from the dorsal glands of the Australian Flood Plain Toadlet Uperoleia inundata. Aust. J. Chem. 49:1996;475-484
18. Bradford A.M., Raftery M.J., Bowie J.H., Wallace J.C., Tyler M.J. Peptides from Australian frogs - the structures of the dynastins from Limnodynastes salmini and fletcherin from Limnodynastes fletcheri. Aust. J. Chem. 46:1993;1235-1244
19. Brinkworth C.S., Bowie J.H., Tyler M.J., Wallace J.C. A comparison of the host defence skin peptides of the New Guinea Tree frog (Litoria genimaculata) and the Fringed Tree frog (Litoria eucnemis). The link between the caerin and the maculatin antimicrobial peptides. Aust. J. Chem. 55:2002;605-610
20. Brinkworth C.S., Dua S., McAnoy A.M., Bowie J.H. Negative ion fragmentations of deprotonated peptides: backbone cleavages directed through both Asp and Glu. Rapid Commun. Mass Spectrom. 15:2001;1965-1973
21. Chen T, Orr DF, O'Rourke M, McLynn C, Biourson AJ, McLean S, et al. Pachymedusa dacnocolor tryptophyllin-1; structural characterization, pharmacological activity and cloning of precursor cDNA. Regulatory peptides, in press.
22. Chia B.C.S., Carver J.A., Lindner R.A., Bowie J.H., Wong H., Lie W. Caerin 4.1, an antibiotic peptide from the Australian tree frog Litoria caerulea. The NMR-derived solution structure. Aust. J. Chem. 53:2000;257-265
23. Chia B.C.S., Carver J.A., Mulhern T.D., Bowie J.H. Maculatin 1.1, an antimicrobial peptide from the Australian tree frog, Litoria genimaculata. Solution structure and biological activity. Eur. J. Biochem. 267:2000;1894-1908
24. Chia B.C.S., Carver J.A., Mulhern T.D., Bowie J.H. The solution structure of uperin 3.6, an antibiotic peptide from the granular dorsal glands of the Australian toadlet, Uperoleia mjobergii. J. Peptide Res. 54:1999;137-145
25. Clark D.P., Durell S., Maloy W.L., Zasloff M. Ranalexin - a novel antimicrobial peptide from bullfrog (Rana catesbeiana) skin, structurally related to the bacterial antibiotic, polymyxin. J. Biol. Chem. 269:1994;10849-10855
26. Clore G.M., Gronenborn A.M. Determination of three-dimensional structures of proteins and nucleic acids in solution by nuclear magnetic resonance spectroscopy. Crit. Rev. Biochem. Mol. Biol. 24:1989;479-564
27. Crane B.R., Arvai A.S., Gachhui R., Wu C., Ghosh D.K., Getzoff E.D., et al. The structure of nitric oxide synthase oxygenase domain and inhibitor complexes. Science. 278:1997;425-431
28. Cruciani R.A., Barker J.L., Zasloff M., Chen H., Colamonici O. Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc. Natl. Acad. Sci. USA. 88:1991;3792-3796
29. Dathe M., Wieprecht T. Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta Biomembr. 1462:1999;71-87
30. Dessauer H.C., Nevo E. Geographic variation of blood and liver proteins in cricket frogs. Biochem. Genet. 3:1969;171-188
31. Doyle J., Brinkworth C.S., Wegener K.L., Carver J.A., Llewellyn L.E., Olver I.N., et al. nNOS inhibition antimicrobial and anticancer activity of the amphibian skin peptide, citropin 1.1 and synthetic modifications: the solution structure of a modified citropin 1.1. Eur. J. Biochem. 270:2003;1141-1153
32. Doyle J., Llewellyn L.E., Brinkworth C.S., Bowie J.H., Wegener K.L., Rozek T., et al. Amphibian peptides that inhibit neuronal nitric oxide synthase: the isolation of lesueurin from the skin secretion of the Australian Stony Creek Frog Litoria lesueuri. Eur. J. Biochem. 269:2002;100-109
33. Epand R.M., Shai Y.C., Segrest J.P., Anantharamaiah G.M. Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers. 37:1995;319-338
34. Erspamer V. Bioactive secretions of the amphibian integument. In: Heatwole H, editor. Amphibian biology: the integument. vol. 1. Norton, NSW: Surrey, Beatty and Sons; 1994. p. 178-350.
35. Erspamer V., Erspamer G.F., Mazzanti G., Endean R. Active peptides in the skins of one hundred amphibian species from Australia and Papua New Guinea. Comp. Biochem. Physiol. 77C:1984;99-108
36. Erspamer V., Melchiorri P., Erspamer G.F., Montecucchi P.C., de Castiglione R. Phyllomedusa skin: a huge factory and store-house of a variety of active peptides. Peptides. 6:1985;7-12
37. Evans JNS. Biomolecular NMR spectroscopy. Oxford: Oxford University Press; 1995. p. 55-77.
38. Ganz T. Biosynthesis of defensins and other antimicrobial peptides. In: Marsh J, Goode J, editors. Antimicrobial peptides. Ciba Foundation Symposium 186. London: John Wiley and Sons; 1994.
39. Gozzini L., Montecucchi P.C., Erspamer V., Melchiorri P. Tryptophyllins from extracts of Phyllomedusa rhodei skin: new tetra-, penta- and heptapeptides. Int. J. Peptide Protein. Res. 25:1985;323-329
40. Guttman SI. Biochemical techniques and problems in anuran evolution. In: JL, V, editors. Evolutionary biology of the anurans. Contemporary research on major problems. Columbia: University of Missouri Press; 1973. p. 183-203.
41. Hensmann M., Booker G.W., Panayotou G., Boyd J., Linacre J., Waterfield M., et al. Phosphopeptide binding to the N-terminal SH2 domain of the p85-alpha subunit of PI 3′-kinase: a heteronuclear NMR study. Protein Sci. 3:1994;1020-1030
42. Ingram G., Corben C. Litoria electrica: a new tree frog from western Queensland. Mem. Qld. Mus. 28:1993;475-478
43. Kikuyama S., Toyoda F., Ohmiya Y., Matsuda K., Tanaka S., Hayashi H. Sodefrin: a female-attracting peptide pheromone in newt cloacal glands. Science. 267:1995;1643-1645
44. Klee C.B., Vanaman T.C. Calmodulin. Adv. Protein Chem. 35:1982;213-321
45. Lazarus L.H., Attila M. The toad, ugly and venomous, wears yet a precious jewel in his skin. Prog. Neurobiol. 41:1993;473-507
46. Lincoln J, Hoyle CHV, Burnstock G. Nitric oxide in health and disease. Cambridge: Cambridge University Press; 1997
47. Low BS. Evidence from parotoid - gland secretions. In: Blair WF, editor. Evolution in the genus Bufo. Austin: University of Texas Press; 1972. p. 244-64.
48. Low BS. Unpublished observations.
49. Marcotte I., Wegener K.L., Lam Y., Chia B.C.S., de Planque M.R.R., Bowie J.H., et al. Interaction of antimicrobial peptides from Australian amphibians with lipid membranes. Chem. Phys. Lipids. 122:2003;107-120
50. Maselli V, Musgrave I, Bowie JH, Tyler MJ. Unpublished observations.
51. Maselli V, Pukala TL, Bowie JH, Tyler MJ. Unpublished observations.
52. Matsuzaki K., Sugishita K., Fujii N., Miyajima K. Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2. Biochemistry. 34:1995;3423-3429
53. McDonnell P.A., Opella S.J. Effect of detergent concentration on multidimensional solution NMR spectra of membrane proteins in micelles. J. Magn. Res. B. 102:1993;120-125
54. Montecucchi P.C., Gozzini L., Erspamer V., Melchiorri P. The primary structure of tryptophan containing peptides from skin extracts of Phyllomedusa rhodei (tryptophyllins). Int. J. Peptide Protein Res. 24:1984;276-285
55. Mutschmann F, Berger L, Zwart P, Gaedicke C. Chytridiomycosis in amphibians - first report in Europe http://www.ncbi.nlm.nih.gov/entrez/query. fcgi?cmd=Retrieve&db=PubMed&list_11084755&dopt=Abstract.
56. Myers C.W., Daly J.W., Garroffo H.M., Wisnieski A., Cover J.F.J. Discovery of the Costa Rican poison frog Dendrobates granuliferus in sympatry with Dendrobates pumilio, and comments on taxonomic use of skin alkaloids. Am. Mus. Novit. 3144:1995;1-21
57. 2+-dependent regulation of beat frequency of cilia in Paramecium. J. Cell Sci. 65:1984;223-231
58. Nelson J.W., Kallenbach N.R. Stabilization of the ribonuclease S-peptide a-helix by trifluoroethanol. Proteins Struct. Funct. Genet. 1:1986;211-217
59. Pukala T.L., Brinkworth C.S., Carver J.A., Bowie J.H. Investigating the importance of the flexible hinge in caerin 1.1: the solution structures and activity of two synthetically modified caerin peptides. Biochemistry. 43:2004;937-944
60. Raftery M.J., Bradford A.M., Bowie J.H., Wallace J.C., Tyler M.J. Peptides from Australian frogs - the structures of the dynastins from the Banjo frogs Limnodynastes interioris, Limnodynastes dumerilii and Limnodynastes terraereginae. Aust. J. Chem. 46:1993;833-842
61. Rajan R., Balaram P. A model for the interaction of trifluoroethanol with peptides and proteins. Int. J. Peptide Protein Res. 48:1996;328-336
62. Rang HP, Dale MM, Ritter JM. Nitric oxide, editors. In: Pharmacology. Edinburgh: Churchill Livingstone; 1999. p. 188-97.
63. Renda T., D'Este L., Buffa R., Usellini L., Capella C., Vaccaro R., et al. Tryptophyllin-like immunoreactivity in rat adenohypophysis. Peptides. 6:1985;197-202
64. Resnick N.M., Maloy W.L., Guy H.R., Zasloff M. A novel endopeptidase from Xenopus that recognizes a-helical secondary structure. Cell. 66:1991;541-554
65. Rollins-Smith LA, Bowie JH, Tyler MJ. Unpublished observations.
66. Rollins-Smith L.A., Carey C., Conlon J.M., Reinert L.K., Doersam J.K., Bergman T., et al. Antimicrobial activity of Temporin family peptides against the Chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Agent Chemother. 47:2003;1157-1160
67. Rollman S.M., Houck L.D., Feldhoff R.C. Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science. 285:1999;1907-1909
68. Rozek T., Bowie J.H., Wallace J.C., Tyler M.J. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. Part 2. Sequence determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 14:2000;2002-2011
69. Rozek T., Waugh R.J., Steinborner S.T., Bowie J.H., Tyler M.J., Wallace J.C. The maculatin peptides from the skin glands of the tree frog Litoria genimaculata - a comparison of the structures and antibacterial activities of maculatin 1.1 and caerin 1.1. J. Peptide Sci. 4:1998;111-115
70. Rozek T., Wegener K.L., Bowie J.H., Olver I.N., Carver J.A., Wallace J.C., et al. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis. The solution structure of aurein 1.2. Eur. J. Biochem. 267:2000;5330-5341
71. Sai K.P., Jagannadham M.V., Vairaman M., Rajii N.P., Devi A.S., Nagaraj R. Tigerinins: novel antimicrobial peptides from the Indian frog Rana tigerina. J. Biol. Chem. 276:2001;2701-2707
72. Sansom M.S.P. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 55:1991;139-235
73. Shai Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by a-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta. 1462:1999;55-70
74. Shai Y., Oren Z. From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides. 22:2001;1629-1641
75. Simmaco M., Mignogna G., Barra D. Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers. 47:1998;435-450
76. Smith T.G., Kim B., Hong H., Desser S.S. Intraerythrocytic development of species of Hepatazoon infecting Ranid frogs: evidence for convergence of life cycle characteristics among Apicomplexans. J. Parasitol. 86:2000;451-458
77. Speare R, Berger L. Chytridiomycosis in amphibians in Australia http://www.jcu.edu.au/school/phtm/PHTM/frogs/chyspec.htm
78. Steinborner ST, Bowie JH, Tyler MJ. Unpublished observations.
79. Steinborner S.T., Bowie J.H., Tyler M.J., Wallace J.C. An unusual combination of peptides from the skin glands of Ewings tree frog, Litoria ewingi - sequence determination and antimicrobial activity. Aust. J. Chem. 50:1997;889-894
80. Steinborner S.T., Currie G.J., Bowie J.H., Wallace J.C., Tyler M.J. New antibiotic caerin 1 peptides from the skin secretion of the Australian tree frog Litoria chloris - comparison of the activities of the caerin 1 peptides from the genus Litoria. Int. J. Peptide Protein Res. 51:1998;121-126
81. Steinborner S.T., Gao C.W., Raftery M.J., Waugh R.J., Blumenthal T., Bowie J.H., et al. The structures of four tryptophyllin and three rubellidin peptides from the Australian red tree frog Litoria rubella. Aust. J. Chem. 47:1994;2099-2108
82. Steinborner S.T., Wabnitz P.A., Bowie J.H., Tyler M.J. The application of mass spectrometry to the study of evolutionary trends in amphibians. Rapid Commun. Mass Spectrom. 10:1996;92-95
83. Steinborner S.T., Wabnitz P.A., Waugh R.J., Bowie J.H., Gao C.W., Tyler M.J., et al. The structures of new peptides from the Australian Red Tree Frog Litoria rubella - the skin peptide profile as a probe for the study of evolutionary trends of amphibians. Aust. J. Chem. 49:1996;955-963
84. Steinborner S.T., Waugh R.J., Bowie J.H., Wallace J.C., Tyler M.J., Ramsay S.L. New caerin antibacterial peptides from the skin glands of the Australian tree frog Litoria xanthomera. J. Peptide Sci. 3:1997;181-185
85. Steinborner S.T., Waugh R.J., Bowie J.H., Wallace J.C., Tyler M.J., Ramsey S.L. New caerin antibiotic peptides from the skin glands of the Australian tree frog Litoria xanthomera. Sequence determination by mass spectrometry. Rapid. Commun. Mass Spectrom. 11:1997;997-1101
86. Stone D.J.M., Bowie J.H., Tyler M.J., Wallace J.C. The structure of caerin 1.1, a novel antibiotic peptide from Australian tree frogs. J. Chem. Soc. Chem. Commun. 72:1992;1224-1225
87. Stone DJM, Waugh RJ, Bowie JH, Wallace JC, Tyler MJ. Peptides from Australian frogs. The structures of the caerins from Litoria caerulea. J. Chem. Res. (S) 1993;138-9; (M) 1993;910-36.
88. Stone DJM, Waugh RJ, Bowie JH, Wallace JC, Tyler MJ. Peptides from Australian frogs. The structures of the caerins from Litoria caerulea. J. Chem. Res. (S) 1993;138-9; (M) 1993;910-36.
89. Stone DJM, Waugh RJ, Bowie JH, Wallace JC, Tyler MJ. Peptides from Australian frogs. Structures of the caerins and caeridin 1 from Litoria splendida. J. Chem. Soc. Perkin Trans. I 1992;3173-78.
90. Stone D.J.M., Waugh R.J., Bowie J.H., Wallace J.C., Tyler M.J. Peptides from Australian frogs. The structures of the caerins from Litoria caerulea. J. Chem. Res. (S) (M). 138:1993;910-936
91. Stuehr DJ, Ghosh S. Enzymology of nitric oxide synthases. In: Mayer B, editor. Nitric oxide. Handbook of experimental pharmacology. Berlin: Springer-Verlag; 2000:33-70.
92. Sutcliffe MJ. Structure determination from NMR data II. Computational approaches. In: Roberts GCK, editor. NMR of macromolecules: a practical approach. New York: Oxford University Press; 1993:359-90.
93. Tilley L, Maselli V, Bowie JH. Unpublished observations.
94. Tossi A., Tarantino C., Romeo D. Design of synthetic antimicrobial peptides based on sequence analogy and amphipathicity. Eur. J. Biochem. 250:1997;549-558
95. Tyler M.J., Davies M., Martin A.A. A new species of large, green tree frog from Northern Western Australia. Trans. R. Soc. S. Aust. 101:1977;133-138
96. Tyler M.J., Stone D.J.M., Bowie J.H. A novel method for the release and collection of dermal, glandular secretions from the skin of frogs. J. Pharm. Toxicol. Methods. 28:1992;199-200
97. Vanhoye D., Brustion F., Nicolas P., Amiche M. Antimicrobial peptides from hylid and ranid frogs originated from a 150-million-year-old ancestral precursor with a conserved signal peptide but hypermutable antimicrobial domain. Eur. J. Biochem. 270:2003;2068-2081
98. Wabnitz PA. PhD thesis. Department of Chemistry, University of Adelaide, Adelaide; 1999.
99. Wabnitz P.A., Bowie J.H., 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. R. Commun. Mass Spectrom. 13:1999;2498-2502
100. Wabnitz P.A., Bowie J.H., Tyler M.J., Wallace J.C., Smith B.P. Differences in the skin peptides of the male and female Australian tree frog Litoria splendida - the discovery of the aquatic male sex pheromone splendipherin, together with Phe8 caerulein and a new antibiotic peptide caerin 1.10. Eur. J. Biochem. 267:2000;269-275
101. Wabnitz P.A., Bowie J.H., Wallace J.C., Tyler M.J. The citropin peptides from the skin glands of the Australian Blue Mountains Tree Frog Litoria citropa. Part 2: sequence determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 13:1999;1724-1732
102. Wabnitz P.A., Bowie J.H., Wallace J.C., Tyler M.J. Peptides from the skin glands of the Australian Buzzing Tree Frog Litoria electrica. Comparison with the skin peptides of the Red Tree Frog Litoria rubella. Aust. J. Chem. 52:1999;639-645
103. Wabnitz P.A., Bowie J.H., Tyler M.J., Wallace J.C., Smith B.P. Differences in the skin peptides in male and female Australian tree frog Litoria splendida. Eur. J. Biochem. 267:2000;269-275
104. Wabnitz P.A., Walters H., Tyler M.J., Wallace J.C., Bowie J.H. First record of host defence peptides in tadpoles. The magnificent tree frog Litoria splendida. J. Peptide Res. 52:1998;477-481
105. Waugh R.J., Raftery M.J., Bowie J.H., Wallace J.C., Tyler M.J. The structures of the frenatin peptides from the skin secretions of the giant tree frog Litoria infrafrenata. J. Peptide Sci. 2:1996;117-124
106. Waugh R.J., Stone D.J.M., Bowie J.H., Wallace J.C., Tyler M.J. Peptides from Australian frogs. The structures of the caerins and caeridins from Litoria gilleni. J. Chem. Res. (S) (M). 139:1993;937-961
107. Wegener K.L., Brinkworth C.S., Bowie J.H., Wallace J.C., Tyler M.J. Bioactive dahlein peptides from the skin secretions of the Australian aquatic frog Litoria dahlii: sequence determination by electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 15:2001;1726-1734
108. Wegener K.L., Wabnitz P.A., Carver J.A., Bowie J.H., Chia B.C.S., Wallace J.C., et al. Host defence peptides from the skin glands of the Australian Blue Mountains Tree Frog Litoria citropa. Solution structure of the antibacterial peptide citropin 1.1. Eur. J. Biochem. 265:1999;627-637
109. Wieprecht T., Dathe M., Schumann M., Krause E., Beyermann M., Bienert M. Conformational and functional study of magainin 2 in model membrane environments using the new approach of systematic double-D-amino acid replacement. Biochemistry. 35:1996;10844-10853
110. Wong H., Bowie J.H., Carver J.A. The solution structure and activity of caerin 1.1, an antimicrobial peptide from the Australian green tree frog, Litoria splendida. Eur. J. Biochem. 247:1997;545-557
111. Xu R.X., Word J.M., Davis D.G., Rink M.J., Willard D.H., Gampe R.T. Solution structure of the human pp60c-src SH2 domain complexed with a phosphorylated tyrosine pentapeptide. Biochemistry. 34:1995;2107-2121
112. Yamamoto K., Kawai Y., Hayashi T., Ohe Y., Hayashi H., Toyoda F., et al. Silefrin, a sodefrin-like pheromone in the abdominal gland of the sword-tailed newt, Cynops ensicauda. FEBS Lett. 472:2000;267-270
113. Zadina J.E., Hackler L., Ge L., Kastin A.J. A potent and selective endogenous agonist for the μ-opiate receptor. Nature. 386:1997;499-502