The antibacterial action of protamine: Evidence for disruption of cytoplasmic membrane energization in Salmonella typhimurium

Microbiology

Volumn 142, Issue 12, 1996, Pages 3389-3397

  Aspedon, Arden ^a   Groisman, Eduardo A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antimicrobial peptide; Membrane potential; Protamine; Salmonella

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CYTOTOXIN; LEUCINE; PEPTIDE; PROLINE; PROTAMINE;

AMINO ACID TRANSPORT; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERICIDAL ACTIVITY; CELL MEMBRANE POTENTIAL; CELL RESPIRATION; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; MEMBRANE DAMAGE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SALMONELLA TYPHIMURIUM;

EID: 0030444342     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/13500872-142-12-3389     Document Type: Article

References (39)

1. Agerberth, B., Lee, J.-Y., Bergman, T., Carlquist, M., Boman, H. G., Mutt, V. & Jörnvall, H. (1991). Amino acid sequence of PR-39. Eur J Biochem 202, 849-854.
2. Berger, E. A. (1973). Different mechanisms of energy coupling for the active transport of proline and glutamine in Escherichia coli. Proc Natl Acad Sci USA 70, 1514-1518.
3. Boman, H. G. (1995). Peptide antibiotics and their role in innate immunity. Annu Rev Immunol 13, 61-92.
4. Boman, H. G., Agerberth, B. & Boman, A. (1993). Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun 61, 2978-2984.
5. Booth, I. R. (1985). Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49, 359-378.
6. Busse, H.-J., Wörstmann, C. & Bakker, E. P. (1992). The bactericidal action of streptomycin: membrane permeabilization caused by the insertion of mistranslated proteins into the cytoplasmic membrane of Escherichia coli and subsequent caging of the antibiotic inside the cells due to degradation of these proteins. J Gen Microbiol 138, 551-561.
7. Carroll, S. F. & Martinez, R. J. (1981). Antibacterial peptide from normal rabbit serum. 3. Inhibition of microbial electron transport. Biochemistry 20, 5988-5994.
8. Christensen, B., Fink, J., Merrifield, R. B. & Mauzerall, D. (1988). Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc Natl Acad Sci USA 85, 5072-5076.
9. Duclohier, H., Molle, G. & Spach, G. (1989). Antimicrobial peptide magainin 1 from Xenopus skin forms anion-permeable channels in planar lipid bilayers. Biophys J 56, 1017-1021.
10. Fields, P. I., Groisman, E. A. & Heffron, F. (1989). A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243, 1059-1062.
11. García-Véscovi, E., Soncini, F. & Groisman, E. A. (1994). The role of the PhoP/PhoQ regulon in Salmonella virulence. Res Microbiol 145, 473-480.
12. Groisman, E. A. (1994). How bacteria resist killing by host-defense peptides. Trends Microbiol 2, 444-449.
13. Groisman, E. A., Heffron, F. & Solomon, F. (1992a). Molecular genetic analysis of the Escherichia coli phoP locus. J Bacteriol 174, 486-491.
14. Groisman, E. A., Parra-Lopez, C., Salcedo, M., Lipps, C. J. & Heffron, F. (1992b). Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci USA 89, 11939-11943.
15. Hiemstra, P. S., Eisenhauer, P. B., Harwig, S. S. L., van den Baselaar, M. T., van Furth, R. & Lehrer, R. I. (1993). Antimicrobial proteins of murine macrophage. Infect Immun 61, 3038-3046.
16. Hirsch, J. G. (1958). Bactericidal action of histone. J Exp Med 107, 925-944.
17. Johansen, C., Gill, T. & Gram, L. (1995). Antibacterial effect of protamine assayed by impedimetry. J Appl Bacteriol 78, 297-303.
18. Kagan, B. L., Selsted, M. E., Ganz, T. & Lehrer, R. I. (1990). Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc Natl Acad Sci USA 87, 210-214.
19. Kaiser, E. T. & Kézdy, F. J. (1987). Peptides with affinity for membranes. Annu Rev Biophys Biophys Chem 16, 561-581.
20. Kashket E. R. (1985). The proton motive force in bacteria : a critical assessment of methods. Annu Rev Microbiol 39, 219-242.
21. Klein, W. L. & Boyer, P. D. (1972). Energization of active transport by Escherichia coli. J Biol Chem 247, 7257-7265.
22. Lehrer, R. I., Barton, A., Daher, K. A., Harwig, S. S. L., Ganz, T. & Selsted, M. E. (1989). Interaction of human defensins with Escherichia coli. J Clin Invest 84, 553-561.
23. Louie, A. J. & Dixon, G. H. (1974). Enzymatic modifications of the protamines. II. Separation and characterization of phosphorylated species of protamines from trout testis. Can J Biochem 52, 536-546.
24. Maloney, P. C. (1987). Coupling to an energized membrane: role of ion-motive gradients in the transduction of metabolic energy. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 222-243. Edited by F. C. Neidhardt, J. L. Ingraham, K. Brooks Low, B. Magasanik, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
25. Miller, B. F., Abrams, R., Dorfman, A. & Klein, M. (1942). Antibacterial properties of protamine and histone. Science 96, 428-430.
26. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
27. Mochan, B. S., Elliott, W. B. & Nicholls, P. (1973). Patterns of cytochrome oxidase inhibition by polycations. Bioenergetics 4, 329-345.
28. Parra-Lopez, C., Baer, M. T. & Groisman, E. A. (1993). Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J 12, 4053-4062.
29. Parra-Lopez, C., Lin, R., Aspedon, A. & Groisman, E. A. (1994). A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. EMBO J 13, 3964-3972.
30. Person, P. & Fine, A. S. (1961). Reversible inhibition of cytochrome system components by macromolecular polyions. Arch Biochem Biophys 94, 392-404.
31. Person, P., Zipper, H., Fine, A. S. & Mora, P. T. (1964). Macroion interactions involving cytochrome system components. J Biol Chem 239, 4159-4162.
32. Shioi, J. & Taylor, B. L. (1984). Oxygen taxis and proton motive force in Salmonella typhimurium. J Biol Chem 259, 10983-10988.
33. Skerlavaj, B., Romeo, D. & Gennaro, R. (1990). Rapid membrane permeabilization and inhibition of vital functions of Gram-negative bacteria by bactenecins. Infect Immun 58, 3724-3730.
34. Smith, J. J., Travis, S. M., Greenberg, E. P. & Welsh, M. J. (1996). Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85, 229-236.
35. Soboh, F., Khoury, A. E., Zamboni, A. C., Davidson, D. & Mittelman, M. W. (1995). Effects of ciprofloxacin and protamine sulfate combinations against catheter-associated Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 39, 1281-1286.
36. Vaara, M. (1981). Increased outer membrane resistance to ethylenediaminetetraacetate and cations in novel lipid A mutants. J Bacteriol 148, 426-434.
37. Vaara, M. (1992). Agents that increase the permeability of the outer membrane. Microbiol Rev 56, 395-411.
38. Westerhoff, H. V., Juretic, D., Hendler, R. W. & Zasloff, M. (1989). Magainins and the disruption of membrane-linked free-energy transduction. Proc Natl Acad Sci USA 86, 6597-6601.
39. Zasloff, M. (1992). Antibiotic peptides as mediators of innate immunity. Curr Opin Immunol 4, 3-7.