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

European Journal of Biochemistry

Volumn 270, Issue 6, 2003, Pages 1141-1153

  Doyle, Jason ^a   Brinkworth, Craig S ^b   Wegener, Kate L ^b   Carver, John A ^c   Llewellyn, Lyndon E ^a   Olver, Ian N ^b   Bowie, John H ^b   Wabnitz, Paul A ^b   Tyler, Michael J ^b  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Antibacterial; Anticancer; Citropin; nNOS activity

Indexed keywords

AUREIN; CITROPIN; DAHLEIN; LESUEURIN; NITRIC OXIDE SYNTHASE INHIBITOR; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

AMPHIBIA; ANTIMICROBIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; DRUG CYTOTOXICITY; ENZYME ACTIVITY; ENZYME INHIBITION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SKIN; STRUCTURE ACTIVITY RELATION;

AMPHIBIA; AMPHIBIAN PROTEINS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ANTINEOPLASTIC AGENTS; BACTERIA; DRUG SCREENING ASSAYS, ANTITUMOR; MICROBIAL SENSITIVITY TESTS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION;

AMPHIBIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 0344211838     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03462.x     Document Type: Article

References (81)

1. Bevins, C.L. & Zasloff, M. (1990) Peptides from frog skin. Ann. Rev. Biochem. 59, 395-414.
2. Lazarus, L.H. & Attila, M. (1993) The toad, ugly and venomous, wears yet a precious jewel in his skin. Prog. Neurobiol. 41, 473-507.
3. Erspamer, V. (1994) Bioactive secretions of the amphibian integument. In Amphibian Biology. The Integument. (Heatwole, H., ed.), Vol 1, 178-350.
4. Barra, D. & Simmaco, M. (1995) Amphibian skin: a pro-raising resource for antimicrobial peptides. Trends. Bioehem. 13, 205-209.
5. Anastasi, A., Erspamer, V. & Endean, R. (1968) The structure of caerulein. Arch. Biochem. Biophys. 125, 57-63.
6. Stone, D.J.M., Waugh, R.J., Bowie, J.H., Wallace, J.C. & Tyler, M.J. (1992) The structures of the caerins and caeridin 1 from Litoria splendida. J. Chem. Soc. Perkin Trans. 1, 3173-3179.
7. Wabnitz, P.A., Bowie, J.H. & Tyler, M.J. (1999) 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, 2498-2502.
8. Bowie, J.H., Wegener, K.L., Chia, B.C.S., Wabnitz, P.A., Carver, J.A., Tyler, M.J. & Wallace, J.C. (1999) Host defence antibacterial peptides from the skin secretions of Australian amphibians. Protein Peptide Lett. 6, 259-269.
9. Wegener, K.L., Wabnitz, P.A., Bowie, J.H., Carver, J.A., Wallace, J.C. & Tyler, M.J. (1999) Host defence peptides from the skin glands of the Australian Blue Mountains Tree Frog Litoria citropa. The antibacterial citropin 1 peptides. The solution structure of citropin 1.1. Eur. J. Biochem. 265, 627-635.
10. Wabnitz, P.A, Bowie, J.H., Wallace, J.C. & Tyler, M.J. (1999) The antibiotic citropin peptides from the Australian Tree Frog Litoria citropa. Structure determination using electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 13, 1724-1732.
11. Rozek, T., Wegener, K.L., Bowie, J.H., Olver, I.N., Carver, J.A., Wallace, J.C. & Tyler, M.J. (2000) 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, 5330-5341.
12. Monks, A., Scudiero, D., Skehan, P., Shoemaker, R., Paull, K., Vistica, D., Hose, C., Langley, J., Cronise, P. & Vaigro-Wolff, A. (1991) Feasibility of a high-flux anticancer drug screen using a diverse panel of of cultured human tumor cell lines. J. Natl Cancer Inst 83, 757-766 (see also http://dtp.nci.nih.gov)
13. Wong, H., Bowie, J.H. & Carver, J.A. (1997) The solution structure and activity of caerin 1.1, an antibiotic peptide from the Australian Tree Frog Litoria splendida. Eur. J. Biochem. 247, 545-557.
14. Shai, Y.C. (1995) Molecular recognition between membrane-scanning peptides. Trends Biochem. Sci. 20, 460-464.
15. Bechinger, B. (1997) Structure and function of channel forming peptides; magainins, cecropins, melittin and alamethicin. J. Membr. Biol. 156, 197-211.
16. Matsuzaki, K. (1998) Magainins as paradigm for the mode of pore forming polypeptides. Biochim. Biophys. Acta 1376, 391-400.
17. Doyle, J., Llewellyn, L.E., Brinkworth, C.S., Bowie, J.H., Wegener, K.L., Rozek, T., Wabnitz, P.A., Wallace, J.C. & Tyler, M.J. (2002) 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, 100-109.
18. Waugh, R.J., Raftery, M.J., Bowie, J.H., Tyler, M.J. & Wallace, J.C. (1996) The structures of the frenatin peptides from the skin secretion of the Giant Tree Frog Litoria infrafrenata. J. Peptide Sci. 2, 117-1124.
19. Bredt, D.S., Hwang, P.M., Glatt, C.L., Lowenstein, C., Reed, R.R. & Snyder, S.H. (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P450 reductase. Nature 351, 714-718.
20. Marietta, M.A. (1993) Nitric oxide synthase and mechanism. J. Biol. Chem. 268, 12231-12234.
21. Marietta, M.A. (1994) Nitric oxide synthase: aspects concerning structure and catalysis. Cell 78, 927-930.
22. Pfeiffer, S., Mayer, B. & Hemmens, B. (1999) Nitric oxide: a protective or pathogenic molecule. Angew. Chem. Int. Ed. Engl. 38, 1715-1731.
23. Forsen, S. (1995) Calcium induced structural changes and domain autonomy in calmodulin. Nature Struct. Biol. 2, 777-783.
24. Venema, R.C., Sayegh, H.S., Kent, J.D. & Harrison, D.G. (1996) Identification, characterisation and comparison of the calmodulin-binding domains of nitric oxide synthases. J. Biol. Chem. 271, 6435-6440.
25. Lee, S.J. & Stull, J.T. (1998) Calmodulin-dependent regulation of inducible and neuronal nitric oxide synthase. J. Biol. Chem. 273, 27430-27437.
26. Matsuda, H. & Iyanagi, T. (1999) Calmodulin activated intramolecular transfer beteen the two flavins of neuronal nitric oxide synthase. Biochim. Biophys. Acta 1473, 345-355.
27. Sautebin, L., Rombola, L., Di Rosa, M., Caliendo, G., Perissutti, E., Grieco, P., Severino, B. & Santagada, V. (2000) Synthesis and structure-activity of antisense peptides corresponding to the region for CaM-binding domain of the inducible nitric oxide synthase. Eur. J. Med. Chem. 35, 727-732.
28. Watanabe, Y., Hu, Y. & Hidaka, H. (1997) Identification of a specific amino acid cluster in the calmodulin binding domain of nNOS. FEBS Lett. 403, 75-78.
29. Choi, W.S., Chang, M.S., Han, J.W., Hong, S.Y. & Lee, H.W. (1997) Identification of NOS in Staphyococcas aureus. Biochem. Biophys. Res. Commun. 237, 554-558.
30. Morita, H., Yoshikawa, H., Sakata, R., Nagata, Y. & Tanaka, H. (1997) Synthesis of nitric oxide from the two equivalent guanidino nitrogens of 1-arginine by Lactobacillus fermentum. J. Bacteriol. 179, 7812-7815.
31. Choi, W.S., Seo, D.W., Chang, M.S., Han, J.W., Paik, W.K. & Lee, H.W. (1998) Methylestersof 1-arginine and N-nitro-L-arginine induce nitric oxide synthase in Staphyloccoccus aureus. Biochem. Biophys. Res. Commun. 246, 431-435.
32. Er, H., Turkoz, Y., Ozerol, I.H. & Uzmez, E. (1998) Effect of NOS inhibition in experimental Pseudomonas keratitis in rabbits. Eur. J. Opthalmol. 8, 137-141.
33. Maeji, N.J., Bray, A.M., Valerio, R.M. & Wang, W. (1995) Larger scale multi-pin peptide synthesis. Pept. Res. 8, 33-38.
34. Jorgensen, J.H., Cleeland, W.A., Craig, G., Doern, M., Ferraro, J., Finegold, C.M., Hansen, S.L., Jenkins, S.G., Novick, W.J., Pfaller, M.A., Preston, D.A., Reller, L.B. & Swenson, J.M. (1993) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 3rd approved standard. Natl Committee Clin. Laboratory Stand. 33, 1-12. (Document M7-A3).
35. 3H]saxitoxin binding to tetrodotoxin-resistant and - sensitive sodium channels. A two-site structural model of ion/toxin interaction. J. General Physiol. 101, 153-182.
36. Fersht, A. Enzyme Structure and Mechanism. W.H. Freeman, New York, NY, USA
37. 1H-NMR spectra of proteins via double quantum filtering. Biochem, Biophys. Res. Commun. 117, 479-485.
38. 1H NMR spectra via two-dimensional homonuclear Hartmann-Hahn spectroscopy. J. Am. Chem. Soc. 107, 2820-2821.
39. Jeener, J., Meier, B.H., Bachman, P. & Ernst, R.R. (1979) Investigation of exchange processes by two- dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
40. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967-974.
41. John, B.K., Plant, D., Webb, P. & Hurd, R.E. (1992) Effective combination of gradients and crafted RF pulses for water suppression in biological samples. J. Magn. Reson. 98, 200-206.
42. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110, 7870-7872.
43. Kay, L.E., Keifer, P. & Saaringen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
44. 12 through the use of new two-dimensional NMR experiments. J. Am. Chem. Soc. 108, 4285-4294.
45. Goddard, T.D. & Kneller, D.G. SPARKY 3. University of California, San Francisco.
46. Xu, R.X., Word, J.M., Davis, D.G., Rink, M.J., Willard, D.H. & Gampe, R.T. (1995) Solution structure of the human pp60c-src SH2 domain complexed with a phosphorylated tyrosine penta-peptide. Biochemistry 34, 2107-2121.
47. Brunger, A.T. (1992) A system for X-ray crystallography and NMR. X-PLOR Version 3.851. Yale University, New Haven, CT.
48. Brunger, A.T. & Nilges, M. (1993) Computational Challenges for macromolecular structure determination by X-ray crystallography and solution NMR-spectroscopy. Q. Rev. Biophys. 26, 49-125.
49. Nilges, M., Kuszewski, J. & Brunger, A.T. (1992) Sampling Properties of Simulated Annealing. In Proceedings of the NATO Advanced Research Workshop on Computational Aspects of the Study of Biological Macromolecules (N.M.R.), Il Ciocco, Italy.
50. Folmer, R.H.A., Hilbers, C.W., Konings, R.N.H. & Nilges, M. (1997) Floating stereospecific assignment revisited - application to an 18 kDa protein and comparison with J-coupling data. J. Biomol. NMR 9, 245-258.
51. Engh, R.A. & Huber, R. (1991) Accurate bond and angle parameters for x-ray protein structure refinement. Acta Crystallog. A 47, 392-400.
52. Koradi, R., Billeter, M. & Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
53. Wegener, K.L., Brinkworth, C.S., Bowie, J.H., Wallace, J.C. & Tyler, M.J. (2001) Bioactive dahlein peptides from the Australian frog Litoria dahlii. Sequence determination by electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 15, 1726-1734.
54. Sonnichsen, F.D., Van Eyk, J.A., Hodges, R.S. & Sykes, B.D. (1992) Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide. Biochemistry 31, 8790-8798.
55. Ragan, R. & Balaram, P. (1996) A model for the interaction of trifluoroethanol with peptides and proteins. Int. J. Peptide Protein Res. 48, 328-336.
56. Schonbrunner, N., Wey, J., Engels, J., George, H. & Kiefhaber, T. (1996) Native like β-structure in a trifluoroethanol-induced partially folded state of the all β-sheet protein tendamistat. J. Mol. Biol. 260, 432-445.
57. Dong, A., Matsura, J., Manning, M.C. & Carpenter, J.F. (1998) Intermolecular b-sheet results from trifluoroethanol-induced nonnative α-helical structure in β-sheet predominant proteins - infrared and circular dichroism spectroscopic study. Arch. Biochem. Biophys. 355, 275-281.
58. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
59. 15N random coil NMR chemical shifts of the common amino acids. Investigations of nearest neighbour effects. J. Biomol. NMR 5, 67-81.
60. Pastore, A. & Saudek, V. (1990) The relationship between chemical shift and secondary structure. J. Magn. Reson. 90, 165-176.
61. Wishart, D.S., Richards, F.M. & Sykes, B.D. (1991) Relationship between NMR chemical shift and protein secondary structure. J. Mol. Biol. 222, 311-333.
62. Wishart, D.S., Richards, F.M. & Sykes, B.D. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651.
63. 13C chemical-shift data. J. Biomol. NMR 4, 171-180.
64. Zhou, N.E., Zhu, B.-Y., Sykes, B.D. & Hodges, R.S. (1992) Relationship between amide proton chemical shifts and hydrogen bonding in amphipathic α-helical peptides. J. Am. Chem. Soc. 114, 4320-4326.
65. Kuntz, I.D., Kosen, P.A. & Craig, E.C. (1991) Amide chemical shifts in many helices in peptides and proteins are periodic. J. Am. Chem. Soc. 113, 1406-1408.
66. Pallaghy, P.K., Duggan, B.M., Pennington, M.W. & Norton, R.S. (1993) 3-Dimensional structure in solution of the calcium channel blocker ω-conotoxin. J. Mol. Biol. 234, 405-420.
67. Morris, A.L., MacArthur, M.W., Hutchinson, E.G. & Thornton, J.M. (1992) Stereochemical quality of protein structure coordinates. Proteins 12, 345-364.
68. Bradford, A.M., Raftery, M.J., Bowie, J.H., Tyler, M.J., Wallace, J.C., Adams, G.W. & Severini, C. (1996) Novel uperin peptides from the dorsal glands of the Australian Flood Plain Toadlet Uperoleia inundata. Aust. J. Chem. 49, 475-484.
69. Richardson, J.S. & Richardson, D.C. (1988) Amino acid preferences for specific locations at the ends of α-helices. Science 240, 1648-1652.
70. Epand, R.M., Shai, Y.C., Segrest, J.P. & Anantharamaiah, G.M. (1995) Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers 37, 319-338.
71. Zubay, G. (1986) Biochemistry, Addison-Wesley Publishers Co, Massachussetts, pp. 507-509.
72. Conner, J., Bucana, C., Fidler, I.J. & Schroit, A.J. (1989) Differentiation dependent expression of phosphatidyl serine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipid by prothrombin complex formation. Proc. Natl Acad. Sci. USA 86, 3184-3188.
73. Utsugi, T., Schroit, A.J., Conner, J., Bucana, C. & Fidler, I.J. (1991) Elevated expression of phosphatidyl serine in the outer membrane leaflet of human tumor cells and recognition of activated human blood monocycles. Cancer Res. 51, 3062-3066.
74. Tytler, E.M., Anantharamaiah, G.M., Walker, D.E., Mishra, V.K., Palgunachari, M.N. & Segrest, J.P. (1995) Molecular basis for prokaryotic specificity of magainin-induced lysis. Biochemistry 34, 4393-4401.
75. Malencik, D.A. & Anderson, S.R. (1982) Binding of simple peptides, hormones and neurotransmitters by calmodulin. Biochemistry 21, 3480-3486.
76. Ikura, M., Kay, L.E., Krinks, M. & Bax, A. (1991) Triple resonance multidimensional NMR study of calmodulin complexed with the binding domain of skeletal muscle myosin light-chain kinase: indication of a conformational change in the central helix. Biochemistry 30, 5498-5504.
77. Ikura, M., Clore, G.M., Gronenborn, A.M., Zhu, G., Klere, C.B. & Bax, A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638.
78. Scaloni, A., Miraglia, N., Orru, S., Amodeo, P., Motta, A., Marino, G. & Pucci, P. (1998) Topology of the calmodulin-melittin complex. J. Mol. Biol. 277, 945-958.
79. 2+ pump. Biochemistry 38, 12320-12332.
80. Hiramatsu, K., Aritaka, N., Hanaki, H., Kawasaki, S., Hosoda, Y., Hori, S., Fukuchi, Y. & Kobayashi, I. (1997) Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350, 1670-1673.
81. Hancock, R.E.W. (1997) Peptide antibiotics. Lancet 349, 418-422.