Cyclization increases the antimicrobial activity and selectivity of arginine- and tryptophan-containing hexapeptides

Biochemistry

Volumn 43, Issue 28, 2004, Pages 9140-9150

  Dathe, Margitta ^a   Nikolenko, Heike ^a   Klose, Jana ^a   Bienert, Michael ^a  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOLOGICAL MEMBRANES; POLYPEPTIDES; POSITIVE IONS; SUBSTITUTION REACTIONS; SYNTHESIS (CHEMICAL);

ANTIMICROBIAL ACTIVITIES; CONFORMATIONAL RIGIDITY;

BIOCHEMISTRY;

AMINO ACID; ARGININE; ARGINYLARGINYL BETA (NAPHTH 1 YL)ALANINE BETA (NAPHTH 1 YL)ALANYLARGINYLPHENYLALANINE; ARGINYLARGINYLTRYPTOPHANYLTRYPTOPHANYLARGINYLPHENYLALANINE; ARGINYLARGINYLTYROSYLTYROSYLARGINYLPHENYLALANINE; HEXAPEPTIDE; LYSINE; LYSYLLYSYLTRYPTOPHANYLTRYPTOPHANYLYSYLPHENYLALANINE; NAPHTHYL GROUP; POLYPEPTIDE ANTIBIOTIC AGENT; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIMICROBIAL ACTIVITY; ARTICLE; ARTIFICIAL MEMBRANE; CALORIMETRY; CYCLIZATION; DRUG CONFORMATION; DRUG DESIGN; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; HYDROPHOBICITY; LIPID BILAYER; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PARTITION COEFFICIENT; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SPECTROSCOPY; TITRIMETRY;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ARGININE; BACILLUS SUBTILIS; CYCLIZATION; ESCHERICHIA COLI; LIPOSOMES; OLIGOPEPTIDES; PEPTIDES, CYCLIC; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TRYPTOPHAN;

BACTERIA (MICROORGANISMS); INSERTION SEQUENCES; NEGIBACTERIA; POSIBACTERIA;

EID: 3142691160     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035948v     Document Type: Article

References (62)

1. Zasloff, M. (2002) Antimicrobial peptides of multilamellar organisms, Nature 415, 389-395.
2. Hancock, R. E. (1997) Peptide antibiotics, Lancet 349, 418-422.
3. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solidstate NMR spectroscopy, Biochim. Biophys. Acta 1462, 157-183.
4. Tomita, M., Takase, M., Bellamy, W., and Shimamura, S. (1994) A review: the active peptide of lactoferrin, Acta Paediatr. Jpn. 36, 585-591.
5. Staubitz, P., Peschel, A., Nieuwenhuizen, W. F., Otto, M., Gotz, F., Jung, G., and Jack, R. W. (2001) Structure-function relationships in the tryptophan-rich, antimicrobial peptide indolicidin, J. Pept. Sci. 7, 552-564.
6. Nagpal, S., Gupta, V., Kaur, K. J., and Salunke, D. M. (1999) Structure-function analysis of tritrypticin, an antibacterial peptide of innate immune origin, J. Biol. Chem. 274, 23296-23304.
7. Blondelle, S. E., Takahashi, E., Dinh, K. T., and Houghten, R. A. (1995) The antimicrobial activity of hexapeptides derived from synthetic combinatorial libraries, J. Appl. Bacteriol. 78, 39-46.
8. Strom, M. B., Rekdal, O., and Svendsen, J. S. (2002) Antimicrobial activity of short arginine- and tryptophan-rich peptides, J. Pept. Sci. 8, 431-437.
9. Strom, M. B., Haug, B. E., Skar, M. L., Stensen, W., Stiberg, T., and Svendsen, J. S. (2003) The pharmacophore of short cationic antibacterial peptides, J. Med. Chem. 46, 1567-1570.
10. Muta, T., Fujimoto, T., Nakajima, H., and Iwanaga, S. (1990) Tachyplesins isolated from hemocytes of Southeast Asian horseshoe crabs (Carcinoscorpius rotundicauda and Tachypleus gigas): identification of a new tachyplesin, tachyplesin III, and a processing intermediate of its precursor, J. Biochem. (Tokyo) 108, 261-266.
11. Nakamura, T., Furunaka, H., Miyata, T., Tokunaga, F., Muta, T., Iwanaga, S., Niwa, M., Takao, T., and Shimonishi, Y. (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure, J. Biol. Chem. 263, 16709-16713.
12. Vogel, H. J., Schibli, D. J., Jing, W., Lohmeier-Vogel, E. M., Epand, R. F., and Epand, R. M. (2002) Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides, Biochem. Cell Biol. 80, 49-63.
13. Haug, B. E., Skar, M. L., and Svendsen, J. S. (2001) Bulky Aromatic Amino Acids Increase the Antibacterial Activity of 15-Residue Bovin Lactoferricin Derivatives, J. Pept. Sci. 7, 425-432.
14. Wu, M. H., and Hancock, R. E. W. (1999) Improved derivatives of bactenecin, a cyclic dodecameric antimicrobial cationic peptide, Antimicrob. Agents Chemother. 43, 1274-1276.
15. Kokryakov, V. N., Harwig, S. S., Panyutich, E. A., Shevchenko, A. A., Aleshina, G. M., Shamova, O. V., Korneva, H. A., and Lehrer, R. I. (1993) Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins, FEBS Lett. 327, 231-236.
16. Romeo, D., Skerlavaj, B., Bolognesi, M., and Gennaro, R. (1988) Structure and bactericidal activity of an antibiotic dodecapeptide purified from bovine neutrophils, J. Biol. Chem. 263, 9573-9575.
17. Agerberth, B., Lee, J. Y., Bergman, T., Carlquist, M., Boman, H. G., Mutt, V., and Jornvall, H. (1991) Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides, Eur. J. Biochem. 202, 849-854.
18. Kang, J. H., Lee, M. K., Kim, K. L., and Hahm, K. S. (1996) Structure-biological activity relationships of 11-residue highly basic peptide segment of bovine lactoferrin, Int. J. Pept. Protein Res. 48, 357-363.
19. van't Hof, W., Veerman, E. C. I., Helmerhorst, E. J., and Nieuw Amerongen, A. V. (2001) Antimicrobial Peptides: Properties and Applikation, Biol. Chem. 382, 597-619.
20. Hwang, P. M., Zhou, N., Shan, X., Arrowsmith, C. H., and Vogel, H. J. (1998) Structure-function relationships of antimicrobial peptides, Biochemistry 37, 4288-4298.
21. Schibli, D. J., Hwang, P. M., and Vogel, H. J. (1999) The structure of the antimicrobial active center of lactoferricin B bound to sodium dodecyl sulfate micelles, FEBS Lett. 446, 213-217.
22. Dathe, M., Schümann, M., Wieprecht, T., Winkler, A., Beyermann, M., Krause, E., Matsuzaki, K., Murase, O., and Bienert, M. (1996) Peptide helicity and membrane surface charge modulate the balance of electrostatic and hydrophobic interactions with lipid bilayers and biological membranes, Biochemistry 35, 12612-12622.
23. Dathe, M., Meyer, J., Beyermann, M., Maul, B., Hoischen, C., and Bienert, M. (2002) General aspects of peptide selectivity towards lipid bilayers and cell membranes studied by variation of the structural parameters of amphipathic helical model peptides, Biochim. Biophys. Acta 1558, 171-186.
24. Dathe, M., Nikolenko, H., Beyermann, M., and Bienert, M. (2002) Cyclization increases the antimicrobial activity and selectivity of tryptophan and arginine containing hexapeptides, Biophys. J. 82, 561a.
25. Beyermann, M., and Bienert, M. (1992) Synthesis of difficult peptide sequences: a comparison of Fmoc- and Boc-technique, Tetrahedron Lett. 33, 3745-3748.
26. Ehrlich, A., Heyne, H.-U., Winter, R., Beyermann, M., Carpino, L. A., and Bienert, M. (1996) Rapid cyclization on all-L-pentapeptides by means of 1-hydroxy-7-azabenzotriazole-derived uronium and phosphonium reagents, J. Org. Chem. 61, 8831-8838.
27. New, R. B. C. (1990) Characterization of liposomes, in Liposomes a practical approach (New, R. R. C., Ed.) pp 105-161, IRL Press/Oxford University Press, Oxford.
28. Böttcher, C. J. F., Van Gent, C. M., and Pries, C. (1961) A rapid and sensitive sub-micro phosphorus determination, Anal. Chim. Acta 24, 203-204.
29. London, E., and Feigenson, G. W. (1981) Fluorescence quenching in model membranes. 1. Characterization of quenching caused by a spin-labeled phospholipid, Biochemistry 20, 1932-1938.
30. Chattopadhyay, A., and London, E. (1987) Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids, Biochemistry 26, 39-45.
31. Abrams, F. S., and London, E. (1993) Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup, Biochemistry 32, 10826-10831.
32. Talbot, J. C., Thiaudiere, E., Vincent, M., Gallay, J., Siffert, O., and Dufourcq, J. (2001) Dynamics and orientation of amphipathic peptides in solution and bound to membranes: a steady-state and time-resolved fluorescence study of staphylococcal delta-toxin and its synthetic analogues, Eur. Biophys. J. 147-161.
33. Seelig, J. (1997) Titration calorimetry of lipid-peptide interactions, Biochim. Biophys. Acta 1331, 103-116.
34. McLaughlin, S. (1989) The electrostatic properties of membranes, Annu. Rev. Biophys. Biophys. Chem. 18, 113-136.
35. Seelig, J., Nebel, S., Ganz, P., and Bruns, C. (1993) Electrostatic and nonpolar peptide-membrane interactions. Lipid binding and functional properties of somatostatin analogues of charge z = +1 to z = +3, Biochemistry 32, 9714-9721.
36. Wieprecht, T., Beyermann, M., and Seelig, J. (1999) Binding of antibacterial magainin peptides to electrically neutral membranes: thermodynamics and structure, Biochemistry 38, 10377-10387.
37. Krause, E., Beyermann, M., Dathe, M., Rothemund, S., and Bienert, M. (1995) Location of an amphipathic alpha-helix in peptides using reversed-phase HPLC retention behavior of D-amino acid analogs, Anal. Chem. 67, 252-258.
38. Kondejewski, L. H., Jelokhani Niaraki, M., Farmer, S. W., Lix, B., Kay, C. M., Sykes, B. D., Hancock, R. E. W., and Hodges, R. S. (1999) Dissociation of antimicrobial and hemolytic activities in cyclic peptide diastereomers by systematic alterations in amphipathicity, J. Biol. Chem. 274, 13181-13192.
39. Fauchere, J. L., Charton, M., Kier, L. B., Verloop, A., and Pliska, V. (1988) Amino acid side chain parameters for correlation studies in biology and pharmacology, Int. J. Pept. Protein Res. 32, 269-278.
40. Black, S. D., and Mould, D. R. (1990) Development of hydrophobicity parameters to analyze proteins which bear post- or cotranslational modifications, Anal. Biochem. 193, 72-82.
41. Woody, R. W. (1994) Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins, Eur. Biophys. J. 23, 253-262.
42. Ladokhin, A. S., Selsted, M. E., and White, S. H. (1997) Bilayer interactions of indolicidin, a small antimicrobial peptide rich in tryptophan, proline, and basic amino acids, Biophys. J. 72, 794-805.
43. Woolley, G. A., Dunn, A., and Wallace, B. A. (1992) Gramicidin-lipid interactions induce specific tryptophan side-chain conformations, Biochem. Soc. Trans. 20, 864-867.
44. Grishina, I. B., and Woody, R. W. (1994) Contributions of tryptophan side chains to the circular dichroism of globular proteins: exciton couplets and coupled oscillators, Faraday Discuss. 245-262.
45. Burstein, E. A., Vendenkina, N. S., and Ivkova, M. N. (1973) Fluorescence and the location of tryptophan residues in protein molecules, Photochem. Photobiol. 18, 263-279.
46. Wimley, W. C., Creamer, T. P., and White, S. H. (1996) Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides, Biochemistry 35, 5109-5124.
47. Liu, L. P., and Deber, C. M. (1997) Anionic phospholipids modulate peptide insertion into membranes, Biochemistry 36, 5476-5482.
48. Schibili, D. J., Epand, R. F., Vogel, H. J., and Epand, R. M. (2002) Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions, Biochem. Cell Biol. 80, 667-677.
49. Huang, C. H., and Charlton, J. P. (1972) Interactions of phosphatidylcholine vesicles with 2-p-toluidinylnaphthalene-6-sulfonate, Biochemistry 11, 735-740.
50. Ladokhin, A. S., and Holloway, P. W. (1995) Fluorescence of membrane-bound tryptophan octyl ester: a model for studying intrinsic fluorescence of protein-membrane interactions, Biophys. J. 69, 506-517.
51. Rozek, A., Friedrich, C. L., and Hancock, R. E. (2000) Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles, Biochemistry 39, 15765-15774.
52. Friedrich, C. L., Rozek, A., Patrzykat, A., and Hancock, R. E. (2001) Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria, J. Biol. Chem. 276, 24015-24022.
53. Jing, W., Hunter, H. N., Hagel, J., and Vogel, H. J. (2003) Influence of tryptophan on lipid binding of linear amphipathic cationic antimicrobial peptides, J. Pept. Res. 61, 219-229.
54. Oishi, O., Yamashita, S., Nishimoto, E., Lee, S., Sugihara, G., and Ohno, M. (1997) Conformations and orientations of aromatic amino acid residues of tachyplesin I in phospholipid membranes, Biochemistry 36, 4352-4359.
55. Matsuzaki, K. (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes, Biochim. Biophys. Acta 1462, 1-10.
56. Haug, B. E., and Svendsen, J. S. (2001) The role of tryptophan in the antibacterial activity of a 15-residue bovine lactoferricin peptide, J. Pept. Sci. 7, 190-196.
57. Blondelle, S. E., and Lohner, K. (2000) Combinatorial libraries: A tool to design antimicrobial and antifungal peptide analogues having lyric specificities for structure-activity relationship studies, Bioplymers 55, 74-87.
58. Little, R. G., Kelner, D. N., Lim, E., Burke, D. J., and Conlon, P. J. (1994) Functional domains of recombinant bactericidal/permeability increasing protein (rBPI23), J. Biol. Chem. 269, 1865-1872.
59. Elass-Rochard, E., Roseanu, A., Legrand, D., Trif, M., Salmon, V., Motas, C., Montreuil, J., and Spik, G. (1995) Lactoferrin-lipopolysaccharide interaction: involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide, Biochem. J. 312, 839-845.
60. O'Leary, W. M., and Wilkinson, S. G. (1988) Gram-positive bacteria, in Microbial lipids (Ratledge, C., and Wilkinson, S. G., Eds.) pp 117-201, Academic Press Ltd., London.
61. Wilkinson, S. G. (1988) Gram-negative bacteria, in Microbial lipids (Ratledge, C., and Wilkinson, S. G., Eds.) pp 299-488, Academic Press Ltd., London.
62. Fernandez-Lopez, S., Kim, H.-S., Choi, E. C., Delgado, M., Granja, J. R., Khasanov, A., Kraehenbuehl, K., Long, G., Weinberger, D. A., Wilcoxen, K. M., and Ghadir M. R. (2001) Antibacterial agents based on the cyclic D,L-alpha-peptide architecture, Nature 412, 452-455.