Membrane association, electrostatic sequestration, and cytotoxicity of Gly-Leu-rich peptide orthologs with differing functions

Biochemistry

Volumn 43, Issue 26, 2004, Pages 8391-8409

  Vanhoye, Damien ^a   Bruston, Francine ^a   El Amri, Shaharazade ^a   Ladram, Ali ^a   Amiche, Mohamed ^a   Nicolas, Pierre ^a  

^a INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL MEMBRANES; ELECTROSTATICS; HYDROPHOBICITY; MICROORGANISMS; PROTEINS; SKIN; SURFACE PLASMON RESONANCE;

BIOLOGICAL ACTIVITY; ELECTROSTATIC SEQUESTRATION; HYDROPHOBIC INTERACTIONS; MEMBRANE ASSOCIATION;

BIOCHEMISTRY;

1,2 DIMYRISTOYLGLYCERO 3 PHOSPHATIDYLCHOLINE; 2 DIMYRISTOYLGLYCERO 3 PHOSPHATIDYLCHOLINE; 9 FLUORENYLMETHYL CHLOROFORMATE; AMINO ACID; COMPLEMENTARY DNA; GLYCINE; LEUCINE; PHOSPHOLIPID; RNA; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERICIDAL ACTIVITY; BILAYER MEMBRANE; BIOSENSOR; CIRCULAR DICHROISM; CYTOTOXICITY; ERYTHROCYTE; ESCHERICHIA COLI; FROG; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEMOLYSIS; HYDROPHOBICITY; MEMBRANE MODEL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURFACE PLASMON RESONANCE; TANDEM MASS SPECTROMETRY; TISSUE DISTRIBUTION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; ANURA; BASE SEQUENCE; BRAIN; CATIONS; CELL MEMBRANE; CIRCULAR DICHROISM; CLONING, MOLECULAR; CYTOPLASM; DNA, COMPLEMENTARY; ELECTROSTATICS; ERYTHROCYTES; ESCHERICHIA COLI; GLYCINE; HEMOLYSIS; INTESTINES; KINETICS; LEUCINE; LIPID BILAYERS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PEPTIDE BIOSYNTHESIS; PEPTIDES; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SKIN; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SURFACE PLASMON RESONANCE; TIME FACTORS; TISSUE DISTRIBUTION;

ANIMALIA; ANURA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; INSERTION SEQUENCES; NEGIBACTERIA; POSIBACTERIA;

EID: 3142545679     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0493158     Document Type: Article

References (87)

1. Bai, J. Z., Saafi, E. L., Zhang, S., and Cooper, G. J. (1999) Role of Ca2+ in apoptosis evoked by human amylin in pancreatic islet-cells, Biochem. J. 343, 53-61.
2. Mirzabekov, T., Lin, M. C., and Kagan, B. L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin, J. Biol. Chem. 271, 1988-92.
3. Lin, M. C., Mirzabekov, T., and Kagan, B. L. (1997) Channel formation by a neurotoxic prion protein fragment, J. Biol. Chem. 272, 44-47.
4. Kagan, B. L., Hirakura, Y., Azimov, R., Azimova, R., and Lin, M. C. (2002) The channel hypothesis of Alzheimer's disease: Current status, Peptides 23, 1311-1315.
5. Gallo, R. L., Murakami, M., Ohtake, T., and Zaiou, M. (2002) Biology and clinical relevance of naturally occurring antimicrobial peptides, J. Allergy Clin. Immunol. 110, 823-831.
6. Hancock, R. E., and Patrzykat, A. (2002) Clinical development of cationic antimicrobial peptides: from natural to novel antibiotics, Curr. Drug Targets Infect. Disord. 2, 79-83.
7. Zasloff, M. (2002) Antimicrobial peptides in health and disease, New Engl. J. Med. 347, 1151-60.
8. Kourie, J. I., and Shorthouse, A. A. (2000) Properties of cytotoxic peptide-formed ion channels, Am. J. Physiol. Cell Physiol. 278, C1063-1087.
9. Brogden, K. A., Ackermann, M., McCray, P. B., Jr., and Tack, B. F. (2003) Antimicrobial peptides in animals and their role in host defences, Int. J. Antimicrob. Agents. 22, 465-78.
10. Kuhn-Nentwig, L. (2003) Antimicrobial and cytolytic peptides of venomous arthropods, Cell. Mol. Life Sci. 60, 2651-68.
11. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms, Nature 415, 389-95.
12. Ganz, T. (2001) Antimicrobial proteins and peptides in host defense, Semin. Respir. Infect. 16, 4-10.
13. Hancock, R. E. (2001) Cationic peptides: effectors in innate immunity and novel antimicrobial, Lancet Infect. Dis. 1, 156-64.
14. Gennaro, R., and Zanett, i M. (2000) Structural features and biological activities of the cathelicidin-derived antimicrobial peptides, Biopolymers 55, 31-49.
15. Tossi, A., Sandri, L., and Giangaspero, A. (2000) Amphipathic, alpha-helical antimicrobial peptides, Biopolymers 55, 4-30.
16. Bulet, P., Hetru, C., Dimarcq, J. L., and Hoffmann, D. (1999) Antimicrobial peptides in insects; structure and function, Dev Comp Immunol. 23, 329-44.
17. Epand, R. M., and Vogel, H. J. (1999) Diversity of antimicrobial peptides and their mechanisms of action, Biochim. Biophys. Acta 1462, 11-28.
18. Andreu, D., and Rivas, L. (1998) Animal antimicrobial peptides: an overview, Biopolymers 47, 415-33.
19. Simmaco, M., Mignogna, G., and Barra, D. (1998) Antimicrobial peptides from amphibian skin: what do they tell us?, Biopolymers 47, 435-50.
20. Brahmachary, M., Krishnan, S. P., Koh, J. L., Khan, A. M., Seah, S. H., Tan, T. W., Brusic, V., and Bajic, V. B. (2004) ANTI-MIC: a database of antimicrobial sequences, Nucleic Acids Res. 32, D586-9.
21. Wang, Z., and Wang, G. (2004) APD: the antimicrobial peptide database, Nucleic Acids Res. 32, D590-2.
22. Wade, D., and Englund, J. (2002) Synthetic antibiotic peptides database, Protein Pept. Lett. 9, 53-7.
23. Tossi, A. A database with more than 400 entries. http///www. bbcm.univ.trieste.it/~tossi/search.html.
24. Ehrenstein, G., and Lecar, H. (1977) Electrically gated ionic channels in lipid bilayers, Q. Rev. Biophys. 10, 1-34.
25. Pouny, Y., Rapaport, D., Mor, A., Nicolas, P., and Shai, Y. (1992) Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipids membranes, Biochemistry 31, 12416-23.
26. Matsuzaki, K. (1998) Magainins as paradigm for the mode of action of pore forming polypeptides, Biochim. Biophys. Acta 1376, 391-400.
27. Hancock, R. E. (1999) Peptide antibiotics, Antimicrob. Agents Chemother. 93, 1317-23.
28. Huang, H. W. (2000) Action of antimicrobial peptides: 2-state model, Biochemistry 39, 8347-52.
29. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides, Biopolymers 66, 236-48.
30. Conlon, J. M., Kolodziejek, J., and Nowotny, N. (2004) Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents, Biochim. Biophys. Acta 1696, 1-14.
31. Apponyi, M. A., Pukala, T. L., Brinkworth, C. S., Maselli, V. M., Bowie, J. H., Tyler, M. J., Booker, G. W., Wallace, J. C., Carver, J. A., Separovic, F., Doyle, J., and Llewellyn, L. E. (2004) Host-defense peptides of Australian Anurans: structure, mechanism of action and evolutionary significance, Peptides, in press.
32. Nascimento, A. C., Fontes, W., Sebben, A., and Castro, M. S. (2003) Antimicrobial peptides from anurans skin secretions, Protein Pept. Lett. 10, 227-38.
33. Nicolas, P., Vanhoye, D., and Amiche, M. (2003) Molecular strategies in biological evolution of antimicrobial peptides, Peptides 24, 1669-80.
34. Rinaldi, A. C. (2002) Antimicrobial peptides from amphibian skin: an expanding scnenario, Curr. Opin. Chem. Biol. 6, 799-804.
35. Nicolas, P., and Mor, A. (1995) Peptides as weapons against microorganisms in the chemical defense system of vertebrates, Annu. Rev. Microbiol. 49, 277-304.
36. Park, I. Y., Cho, J. H., Kim, K. S., Kim, Y. B., and Kim, S. C. (2004) Helix stability confers salt resistance upon helical antimicrobial peptides, J. Biol. Chem.
37. Dennison, S. R., Harris, F., and Phoenix, D. A. (2003) Factors determining the efficacy of alpha helical antimicrobial peptides, Protein Pept. Lett. 10, 497-502.
38. Papo, N., and Shai, Y. (2003) Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides 24, 1693-703.
39. Powers, J. P., and Hancock, R. E. (2003) The relationship between peptide structure and antibacterial activity, Peptides 24, 1681-91.
40. 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 structure parameters of amphipathic helical model peptides, Biochim. Biophys. Acta 1558, 171-86.
41. Kustanovich, I., Shalev, D. E., Mikhlin, M., Gaidukov, L., and Mor, A. (2002) Structural requirements for potent versus selective cytotoxicyty for antimicrobial dermaseptin S4 derivatives, J. Biol. Chem. 277, 16941-51.
42. Tochi, T., Epand, R. F., Epand, R. M., and Matsuzaki, K. (2002) Position-dependent hydrophobicity of the antimicrobial magainin peptide affects the mode of peptide-lipid interaction and selectivity, Biochemistry 41, 10723-31.
43. Giangaspero, A., Sandri, L., and Tossi, A. (2001) Amphipathic alpha helical peptides, Eur. J. Biochem. 268, 5589-600.
44. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-phase NMR spectroscopy, Biochim. Biophys. Acta 1462, 157-83.
45. Blondelle, S. E., Lohner, K., and Aguilar, M. (1999) lipid-induced conformation and lipid binding properties of cytolytic and antimicrobial peptides: determination and biological specificity, Biochim. Biophys. Acta 1462, 89-108.
46. Matsuzaki, K. (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as arche-types, Biochim. Biophys. Acta 1462, 1-10.
47. Sitaram, N., and Nagaraj, R. (1999) Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity, Biochim. Biophys. Acta 1462, 29-54.
48. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell nonselective membrane-lytic peptides, Biochim. Biophys. Acta 1462, 55-70.
49. Hwang, P. M., and Vogel, H. J. (1998) Structure-function relationships of antimicrobial peptides, Biochem. Cell. Biol. 76, 235-46.
50. Lai, R., Liu, H., Hui Lee, W., Zhang, Y. (2002) An anionic antimicrobial peptide from toad Bombina maxima, Biochem. Biophys. Res. Commun. 295, 796-9.
51. Zhang, J., and Rosenberg, H. (2002) Complementary advantageous substitutions in the evolution of an antiviral Rnase of higher primates, Proc. Natl. Acad. Sci. U.S.A. 99, 5486-91.
52. Amiche, M., Séon, A., Pierre, T. N., Nicolas, P. (1999) The dermaseptin precursors: a protein family with a common preproregion and a variable C-terminal antimicrobial domain, FEBS Lett. 456, 352-6.
53. Chen, T., Tang., L., and Shaw, C. (2003) Identification of three novel Phyllomedusa sauvagei dermaseptins by cloning from a skin secretion-derived cDNA library, Regul. Peptides 116, 139-46.
54. Brand, G. D., Leite, J. R., Silva, L. P., Albuquerque, S., Prates, M. V., Azevedo, R. B., Carregaro, V., Da Silva, J. S., Sa, V. C., Brandao, R. A., and Bloch, C. Jr. (2002) Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta. Anti-Trypanosoma cruzi activity without cytotoxicity to mammalian cells, J. Biol. Chem. 277, 49332-40.
55. Wechselberger, C. (1998) Cloning of cDNAs encoding new peptides of the dermaseptin-family, Biochim. Biophys. Acta 1388, 279-83.
56. Charpentier, S., Amiche, M., Mester, Y., Vouille, V., Le Caer, J. P., Nicolas, P., and Delfour, A. (1998) Structure, Synthesis and molecular cloning of dermaseptins B, a family of skin peptide antibiotics, J. Biol. Chem. 273, 14690-96.
57. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular cloning. A Laboratory manual, 2nd ed. Cold Spring Harbor laboratory, Cold Spring Harbor, NY.
58. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res. 24, 4876-82.
59. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol. 16, 111-20.
60. Swofford, D. L. (1999) PAUP: phylogenetic analysis using parsimony and other methods. Version 4. Sinauer Associates. Sunderland, Mass
61. Ina, Y. (1995) New methods for estimating the numbers of synonymous and nonsynonymous substitutions, J. Mol. Evol. 40, 190-226.
62. Jukes, T. H., and Cantor, C. R. (1969) Evolution of protein molecules, pp 21-132 in Mammalian Protein Metabolism, ed. H. N. Munro. Academic Press, New York.
63. Pierre, T. N., Seon, A. A., Amiche, M., and Nicolas, P. (2000) Phylloxin, a novel peptide antibiotic of the dermaseptin family of antimicrobial/opioid peptide precursors, Eur. J. Biochem. 267, 370-8.
64. Wilm, M., and Mann, M. (1996) Analytical properties of the nanoelectrospray ion source, Anal. Chem. 68, 1-8
65. Roepstorff, P., and Fohlman, M. (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides, J. Biomed. Mass. Spectrom. 11, 601-6.
66. Honig, B., and Nicholls, A. (1995) Classical electrostatics in biology and chemistry, Science 268, 1144-49.
67. Hagler, A. T., Stren, P. S., Sharon, R., Becker, J. M., and Naider, F. (1979) Computer simulation of the conformational properties of oligopeptides. Comparison of the theoretical methods and analysis of experimental results, J. Am. Chem. Soc 101, 6842-52.
68. Amiche, M., Séon, A., Wroblewski, H., and Nicolas, P. (2000) Isolation of dermatoxin from frog skin, an antibacterial peptide encoded by a novel member of the dermaseptin genes family, Eur. J. Biochem. 267, 4583-92,
69. Matsuzaki, K., Murase, O., Sugishita, K., Yoneyama, S., Akada, K., Ueha, M., Nakamura, A., and Kobayashi, S. (2000) Optical characterization of liposomes by right angle light scattering and turbidity measurements. Biochim. Biophys. Acta Biomembranes 1467, 219-226.
70. Zhong, L., and Johnson, W. C., Jr. (1992) Environment affects amino acid preference for secondary structure, Proc. Natl. Acad. Sci. U S A. 89, 4462-65.
71. Mozsolits H., Wirth H. J., Werkrneister J., and Aguilar M. I. (2001) Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance, Biochim. Biophys. Acta 1512, 64-76.
72. Deleage, G., Blanchet, C., and Geourjon, C. (1997) Secondary consensus prediction. Protein structure prediction. Implications for the biologist, Biochimie 79, 681-6.
73. Li, S. C., Kim, P. K., and Deber, C. M. (1995) Manipulation of peptide conformations by fine-tuning of the environment and/or the primary sequence, Biopolymers 35, 667-75.
74. Li, S. C., and Deber, C. M. (1992) Glycine and β-branched residues support and modulate peptide helicity in membrane environments, FEBS Lett. 311, 217-20.
75. Johnson, J. E., Xie, M., Singh, L. M. R., Edge, R., and Cornell, R. (2003) Both acidic and basic amino acids in an amphitropic enzyme CTP: phosphochotine cytidyltransferase, dictate its selectivity for anionic membranes, J. Biol. Chem. 278, 514-22.
76. Segrest, J. P., De Loof, H., Dohlman, J. G., Brouillette, C. G., and Anantharamaiah, G. M. (1990) Amphipathic helix motif-classes and properties, Proteins 8, 103-17.
77. Gaidukov, L., Fish, A., and Mor, A. (2003) Analysis of membrane-binding properties of dermaseptin analogues: relationships between binding and cytotoxicity, Biochemistry 42, 12866-74.
78. Chia, C. S. B., Torres, J., Cooper, M. A., Arkin, I. T., and Bowie, J. H. (2002) The orientation of the antibiotic peptide maculatin 1.1 in DMPG and DMPC lipid bilayers. Support for a poreforming mechanism, FEBS Lett. 512, 47-51.
79. Papo, N., and Shai, Y. (2003) Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides, Biochemistry 42, 458-66.
80. Blondelle, S. E., Lohner, K., and Aguilar, M. (1999) Lipid-induced conformation and lipid-binding properties of cytolytic and antimicrobial peptides: determination and biological specificity, Biochim. Biophys. Acta 1462, 89-108.
81. Hicks, R. P., Mones, E., Kim, H., Koser, B. W., Nichols, D. A., and Bhattacharjee, A. K. (2003) Comparison of the conformation and electrostatic surface properties of magainin peptides bound to sodium dodecyl sulfate and dodecylphosphocholine micelles, Biopolymers 68, 459-70.
82. Lequin, O., Bruston, F., Convert, O., Chassaing, G., and Nicolas, P. (2003) Helical structure of dermaseptin B2 in a membrane-mimetic environment, Biochemistry 42, 10311-10323.
83. Duda, T. F., Vanhoye, D., and Nicolas, P. (2002) Roles of diversifying selection and coordinated evolution in the evolution of amphibian antimicrobial peptides, Mol. Biol. Evol. 19, 858-864.
84. Ota, T., Sitnikova, T., and Nei, M. (2000) Evolution of vertebrate immunoglobulin variable gene segments, Curr. Top. Microbiol. Immunol. 248, 221-245.
85. Hughes, A. L. (1997) Rapid evolution of immunoglobulin superfamily C2 domains expressed in immune system cells, Mol. Biol. Evol. 14, 1-5.
86. Duellman, W. E., and Trueb, L. (1994) Biology of Amphibians, John Hopkins University Press, London, U.K.
87. Simmaco, M., Mignogna, G., Barra, D., and Bossa, F. (1994) Antimicrobial peptides from skin secretions of Rana esculenta. Molecular cloning of cDNAs encoding esculentin and brevinins and isolation of new active peptides, J. Biol. Chem. 269, 11956-11961.