A different molecular mechanism underlying antimicrobial and hemolytic actions of temporins A and L

Journal of Medicinal Chemistry

Volumn 51, Issue 8, 2008, Pages 2354-2362

  Carotenuto, Alfonso ^a   Malfi, Stefania ^a   Saviello, Maria Rosaria ^a   Campiglia, Pietro ^b   Gomez Monterrey, Isabel ^a   Mangoni, Maria Luisa ^c   Gaddi, Ludovica Marcellini Hercolani ^c   Novellino, Ettore ^a   Grieco, Paolo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DODECYL SULFATE SODIUM; DODECYLPHOSPHORYLCHOLINE; POLYPEPTIDE ANTIBIOTIC AGENT; TEMPORIN A; TEMPORIN L;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; CIRCULAR DICHROISM; DRUG MECHANISM; ERYTHROCYTE; HEMOLYSIS; MICELLIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; CIRCULAR DICHROISM; ERYTHROCYTES; HEMOLYSIS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; PHOSPHORYLCHOLINE; PROTEINS; SODIUM DODECYL SULFATE; SPECTROMETRY, MASS, FAST ATOM BOMBARDMENT; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 43049132172     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm701604t     Document Type: Article

References (60)

1. Boman, H. G. Innate immunity and the normal microflora. Immunol Rev. 2000, 173, 5-16.
2. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389-395.
3. Mangoni, M. L.; Miele, R.; Renda, T. G.; Barra, D.; Siminaco, M. The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. FASEB J. 2001, 15, 1431-1432.
4. Bulet, P.; Stocklin, R.; Menin, L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004, 198, 169-184.
5. Zaiou, M. Multifunctional antimicrobial peptides: therapeutic targets in several human diseases. J. Mol. Med. 2007, 85, 317-329.
6. Boman, H. G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 1995, 13, 61-92.
7. Boman, H. G. Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med. 2003, 254, 197-215.
8. Kimbrell, D. A.; Beutler, H. The evolution and genetics of innate immunity. Nat. Rev. Genet. 2001, 2, 256-267.
9. Hancock, R. E. W. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 2001, 1, 156-164.
10. Mookherjee, N.; Hancock, R. E. Cationic host defence peptides: innate immune regulatory peptides us a novel approach for treating infections. Cell. Mol. Life Sci. 2007, 64, 922-933.
11. Papagianni, M. Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol. Adv. 2003, 21, 465-199.
12. Rinaldi, A. C. Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol. 2002, 6, 799-804.
13. Simmaco, M.; Mignogna, G.; Canofeni, S.; Miele, R.; Mangoni, M. L.; Barra, D. Temporins, antimicrobial peptides from the European red frog Rana temporaria. Eur. J. Biochem. 1996, 242, 788-792.
14. Wade, D.; Silberring, J.; Soliymani, R.; Heikkinen, S.; Kilpeläinen, I.; Lankinen, H.; Kuusela, P. Antibacterial activities of temporin A analogs. FEBS Lett. 2000, 479, 6-9.
15. Wade, D.; Silveira, A.; Silberring, J.; Kunsela, P.; Lankinen, H. Antibiotic properties of novel synthetic temporin A analogs and a cccropin A-temporin A hybrid peptide. Protein Pept. Lett. 2000, 7, 349-357.
16. Wade, D. Unambiguous consensus sequences for temporin-like antibiotic peptides. Internet J. Chem. 2002, 5. 5. [Online. http://preprint.chemweb.com/biochem/0204002].
17. Mangoni, M. L. Temporins, anti-infective peptides with expanding properties. Cell. Mol. Life Sci. 2006, 63, 1060-1069.
18. Rinaldi, A. C.; Mangoni, M. L.; Rufo, A.; Luzi, C.; Barra, D.; Zhao, H.; Kinnunen, P. K. J.; Bozzi, A.; Di Giulio, A.; Simmaco, M. Temporin L: antimicrobial, hemolytic and cytotoxic activities, and effects on membrane permeabilization in lipid vesicles. Biochem. J. 2002, 368, 91-100.
19. Mangoni, M. L.; Rinaldi, A. C.; Di Giulio, A.; Mignogna, G.; Bozzi, A.; Barra, D.; Simmaco, M. Structure - function relationships of temporins, small antimicrobial peptides from amphibian skin. Eur. J. Biochem. 2000, 267, 1447-1454.
20. Rinaldi, A. C.; Di Giulio, A.; Liberi, M.; Gualtieri, G.; Oratore, A.; Schinina, M. E.; Simmaco, M.; Bozzi, A. Effects of temporins on molecular dynamics and membrane permeabilization in lipid vesicles. J. Pept. Res 2001, 58, 213-220.
21. Zhao, H.; Rinaldi, A. C.; Di Giulio, A.; Simmaco, M.; Kinnunen, P. K. J. Interactions of the antimicrobial peptides temporins with model biomembranes. Comparison of temporins B and L. Biochemistry 2002, 41, 4425-4436.
22. Mangoni, M. L.; Sangar, J. M.; Dellisanti, M.; Barra, D.; Simmaco, M.; Rivas, L. Temporins, small antimicrobial peptides with leishmanicidal activity. J. Biol. Chem. 2005, 280, 984-990.
23. Mangoni, M. L.; Papo, N.; Barra, D.; Simmaco, M.; Bozzi, A.; Di Giulio, A.; Rinaldi, A. C. Effects of the antimicrobial peptide temporin L on cell morphology, membrane permeability and viability of Escherichia coli. Biochem. J. 2004, 380, 859-865.
24. Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1999, 1462, 55-70.
25. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1999, 1462, 1-10.
26. Yang, L.; Weiss, T. M.; Lehrer, R. I.; Huang, H. W. Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys. J. 2000, 79, 2002-2009.
27. Gidalevitz, D.; Ishitsuka, Y.; Muresan, A. S.; Konovalov, O.; Waring, A. J.; Lehrer, R. I.; Lee, K. Y. Interaction of antimicrobial peptide protegrin with biomemhranes. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 6302-6307.
28. Yeaman, M. R.; Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 2003, 55, 27-55.
29. Langham, A. A.; Khandelia, H.; Kaznessis, Y. N. How can a β-sheet peptide be both a potent antimicrobial and harmfully toxic? Molecular dynamics simulations of protegrin-1 in micelles. Biopolymers 2006, 84, 219-231.
30. Henry, G. D.; Sykes, B. D. Methods to study membrane protein structure in solution. Methods Enzymol. 1994, 239, 515-535.
31. Kallick, D. A.; Tessmer, M. R. Watts, C. R.; Li. C. Y. J. The use of dodecylphosphocholine micelles in solution NMR. J. Magn. Reson. B 1995, 109, 60-65.
32. Lee, S. A.; Kim, Y. K.; Lim, S. S.; Lim, W. L.; Ko, H.; Shin, S. Y.; Hahm, K. S.; Kim, Y. Solution structure and cell selectivity of piscidin 1 and its analogues. Biochemistry 2007, 46, 3653-3663.
33. van den Hooven, H. W. S.; Chris, A. E. M.; van de Kamp, M.; Konings, R. N. H.; Hilhers, C. W.; van de Ven, F. J. M. Three-dimensional structure of the lantibiotic nisin in the presence of membrane-mimetic micelles of dodecylphosphocholine and of sodium dodecylsulphate. Eur. J. Biochem. 1996, 235, 394-403.
34. Atherton, E.; Sheppard, R. C. Solid-Phase Peptide Synthesis: A Practical Approach; IRL Press: Oxford, U.K., 1989.
35. D'Ahramo, M.; Rinaldi, A. C.; Bozzi, A.; Amadei, A.; Mignogna, G.; Di Nola, A.; Aschi, M. Conformational behavior of temporin A and temporin L in aqueous solution: a computational/experimental study. Biopolymers 2006, 81, 215-224.
36. Kamysz, W.; Mickiewicz, B.; Rodziewicz-Motowidlo, S.; Greber, K.; Okroj, M. Temporin A and its retro-analogues: synthesis, conformational analysis and antimicrobial activities. J. Pept. Sci. 2006, 12, 533-537.
37. Zhao, H; Kinnunen, P. K. Binding of the antimicrobial peptide temporin L to liposomes assessed by Trp fluorescence. J. Biol. Chem. 2002, 277, 25170-25177.
38. Wüthrich, K. In NMR of Proteins and Nucleic Acids: John Wiley & Sons, Inc.: New York, 1986.
39. (a) Piantini, U.; Sorensen, O. W.; Ernst, R. K. Multiple quantum filters for elucidating NMR coupling network. J. Am. Chem. Soc. 1982, 104, 6800-6801.
40. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 1983, 113, 967-974.
41. Braunschweiler, L.; Ernst, R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 1983, 53, 521-528.
42. Jenner, J.; Meyer, B. H.; Bachman, P.; Ernst, R. R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 1979, 71, 4546-4553.
43. Bartels, C.; Xia, T.; Billeter, M.; Guentert, P.; Wütrich, K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 1995, 6, 1-10.
44. (a) Wishart, D. S.; Sykes, B. D.; Richards, F. M. The chemical shift index: a fast method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 1992, 31, 1647-1651.
45. (b) Andersen, N. H.; Liu, Z.; Prickett, K. S. Efforts toward deriving the CD spectrum of a 30101 helix in aqueous medium. FEBS Lett. 1996, 399, 47-52.
46. Güntert, P.; Mumenthaler, C.; Wüthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 1997, 273, 283-298.
47. (a) Brown, L. R.; Bösch, C.; Wüthrich, K. Location and orientation relative to the micelle surface for glucagon in mixed micelles with dodecylphosphocholine: EPR and NMR studies. Biochim. Biophys. Acta 1981, 642, 296-312.
48. (b) Lindberg, M.; Jarvet, J.; I angel, U.; Grasland, A. Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 2001, 40, 3141-3149.
49. Shai, Y. Molecular recognition between membrane-spanning polypeptides. Trends Biochem. Sci. 1995, 20, 460-464.
50. Matsuzaki, K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1998, 1376, 391-400.
51. Wu, M.; Maier, E.; Benz, R.; Hancock, R. E. W. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 1999, 38, 7235-7242.
52. Wieprecht, T.; Dathe, M.; Epand, R. M.; Beyermann, M.; Krause, E.; Maloy, W. L.; MacDonald, D. L.; Bienert, M. Peptide hydrophobicity controls the activity and selectivity of magainin 2 amide in interaction with membranes. Biochemistry 1997, 36, 6124-6132.
53. Sharon, M.; Oren, Z.; Shai, Y.; Anglisier, J. 2D-NMR and ATR-FTIR study of the structure of a cell-selective diaslcrcomcr of melittin and its orientation in phospholipids. Biochemistry 1999, 38, 15305-15316.
54. Valenti, P.; Visca, P.; Antonini, G.; Orsi, N. Antifungal activity of ovotransferrin towards genus Candida. Mycopathologia 1985, 89, 169-175.
55. States, D. J.; Haberkorn, R. A.; Ruben, D. J. A two-dimensional nuclear Overhauser experiment with pure absorption phase in four quadrants. J. Magn. Reson. 1982, 48, 286-292.
56. Hwang, T. L.; Shaka, A. J. Water suppression that works. Excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. 1995, 112, 275-279.
57. Delaglio, F.; Grzesick, S.; Vuister, G. W.; Zhu, C.; Pfeifer, J.; Bax, A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995, 6, 277-93.
58. Maple, J.; Dinur, U.; Hagler, A. T. Derivation of force fields for molecular mechanics and dynamics from ab initio energy surface. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 5350-5354.
59. Koradi, R.; Billeter, M.; Wüthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 1996, 14, 51-55.
60. Hutchinson, E. G.; Thornton, J. M. PROMOTIF - a program to identify and analyze structural motifs in proteins. Protein Sci. 1996, 5, 212-220.