Platelet microbicidal proteins and neutrophil defensin disrupt the Staphylococcus aureus cytoplasmic membrane by distinct mechanisms of action

Journal of Clinical Investigation

Volumn 101, Issue 1, 1998, Pages 178-187

  Yeaman, Michael R ^a,b,e   Bayer, Arnold S ^a,b   Koo, Su Pin ^a   Foss, Wendy ^c   Sullam, Paul M ^c,d  

^a St John's Cardiovascular Research Center   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UCLA MEDICAL CENTER   (United States)

Author keywords

Antimicrobial peptide; Host defense; Microbicidal; Platelet; Transmembrane potential

Indexed keywords

DEFENSIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROPIDIUM IODIDE;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; HOST RESISTANCE; INFECTION RESISTANCE; MEMBRANE DAMAGE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RABBIT; STAPHYLOCOCCUS AUREUS; THROMBOCYTE; TRANSMISSION ELECTRON MICROSCOPY;

EID: 0031984629     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI562     Document Type: Article

References (42)

1. Yeaman, M.R., S.M. Puentes, D.C. Norman, and A.S. Bayer. 1992. Partial purification and staphylocidal activity of thrombin-induced platelet microbicidal protein. Infect. Immun. 60:1202-1209.
2. Yeaman, M.R., Y.-Q. Tang, A.J. Shen, A.S. Bayer, and M.E. Selsted. 1997. Purification and in vitro activities of rabbit platelet microbicidal proteins. Infect. Immun. 65:1023-1031.
3. Tang, Y.Q., M.R. Yeaman, and M.E. Selsted. 1995. Purification, characterization, and antimicrobial properties of peptides released from thrombin-induced human platelets. Blood. 86:910a. (Abstr. 3626)
4. Tang, Y.Q., M.R. Yeaman, and M.E. Selsted. 1995. Microbicidal and synergistic activities of human platelet factor-4 (hPF-4) and connective tissue activating peptide-3 (CTAP-3). Blood. 86:556a. (Abstr. 2212)
5. Wu, T., M.R. Yeaman, and A.S. Bayer. 1994. In vitro resistance to platelet microbicidal protein correlates with endocarditis source among staphylococcal isolates. Antimicrob. Agents Chemother. 38:729-732.
6. Yeaman, M.R., A. Ibrahim, S.G. Filler, A.S. Bayer, J.E. Edwards, and M.A. Ghannoum. 1993. Thrombin-induced rabbit platelet microbicidal protein is fungicidal in vitro. Antimicrob. Agents Chemother. 37:546-553.
7. Drake, T.A., and M. Pang. 1988. Staphylococcus aureus induces tissue factor expression in cultured human cardiac valve endothelium. J. Infect. Dis. 157:749-756.
8. Drake, T.A., and M. Pang. 1989. Effects of interleukin-1, lipopolysaccharide, and streptococci on procoagulant activity of cultured human cardiac valve endothelial and stromal cells. Infect. Immun. 57:507-512.
9. Bancsi, M.J.L.M.F., J. Thompson, and R.M. Bertina. 1994. Stimulation of monocyte tissue factor expression in an in vitro model of bacterial endocarditis. Infect. Immun. 62:5669-5672.
10. Azizi, N., C. Li, A.J. Shen, A.S. Bayer, and M.R Yeaman. 1996. Staphylococcus aureus elicits release of platelet microbicidal proteins in vitro. Abstract 866. 36th Interscience Conference on Antimicrobial Agents and Chemotherapy, New Orleans, LA.
11. Bayer, A.S., M.D. Ramos, B.E. Menzies, M.R. Yeaman, A. Shen, and A.L. Cheung. 1997. Hyperproduction of α-toxin by Staphylococcus aureus results in paradoxically-reduced virulence in experimental endocarditis: a host defense role for platelet microbicidal proteins. Infect. Immun. 65:4652-4660.
12. Koo, S.P., A.S. Bayer, H.G. Sahl, R.A. Proctor, and M.R. Yeaman. 1996. Staphylocidal action of thrombin-induced platelet microbicidal protein is not solely dependent on transmembrane potential. Infect. Immun. 64:1070-1074.
13. Koo, S.P., M.R. Yeaman, and A.S. Bayer. 1996. Staphylocidal action of thrombin-induced platelet microbicidal protein is influenced by microenvironment and target cell growth phase. Infect. Immun. 64:3758-3764.
14. Sullam, P.M., U. Frank, M.G. Tauber, M.R. Yeaman, A.S. Bayer, and H.F. Chambers. 1993. Effect of thrombocytopenia on the early course of streptococcal endocarditis. J. Infect. Dis. 168:910-914.
15. Dhawan, V.K., M.R. Yeaman, A.L. Cheung, E. Kim, P.M. Sullam, and A.S. Bayer. 1997. Phenotypic resistance to thrombin-induced platelet microbicidal protein in vitro is correlated with enhanced virulence in experimental endocarditis due to Staphylococcus aureus. Infect. Immun. 65:3292-3299.
16. Yeaman, M.R., S.S. Soldan, M.A. Ghannoum, J.E. Edwards, Jr., S.G. Filler, and A.S. Bayer. 1996. Resistance to platelet microbicidal protein (PMP) results in increased severity of experimental Candida albicans endocarditis. Infect. Immun. 64:1379-1384.
17. Wu, T.M., M.R. Yeaman, C. Nast, C. Itatani, and A.S. Bayer. 1996. Ultrastructural evidence that platelet microbicidal protein (PMP) targets the bacterial cell membrane. Abstract A72. 96th General Meeting of the American Society for Microbiology, New Orleans, LA.
18. Koo, S.P., M.R. Yeaman, and A.S. Bayer. 1997. Cell membrane is a principal target for the staphylocidal action of platelet microbicidal protein. Infect. Immun. 65:4795-4800.
19. Balwit, J.M., P. van Langevelde, J.M. Vann, and R.A. Proctor. 1994. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170:1033-1037.
20. Selsted, M.E. 1993. Investigational approaches for studying the structures and biologic functions of myeloid antimicrobial peptides. Gen. Engineering. 15:131-147.
21. Harwig, S.S.L., T. Ganz, and R.I. Lehrer. 1994. Neutrophil defensins: purification, characterization, and antimicrobial testing. Methods Enzymol. 236: 160-176.
22. Lehrer, R.I., A. Barton, and T. Ganz. 1988. Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple wavelength spectrometry. J. Immunol. Methods. 108:153-158.
23. Vaara, M., and T. Vaara. 1983. Polycations sensitize enteric bacteria to antibiotics. Antimicrob. Agents Chemother. 24:107-113.
24. Pratt, W.B., and R. Fekety. 1986. Bactericidal inhibitors of protein synthesis. In The Antimicrobial Drugs. Oxford University Press, New York. 153-183.
25. Shapiro, H.M. 1990. Cell membrane potential analysis. Methods Enzymol. 33:25-35.
26. Darzynkiewicz, Z., X. Li, and J. Gong. 1994. Assays of cell viability: discrimination of cells dying of apoptosis. Methods Cell Biol. 41:15-38.
27. Shimoda, M., K. Ohki, Y. Shimamoto, and O. Kohashi. 1995. Morphology of defensin-treated Staphylococcus aureus. Infect. Immun. 63:2886-2891.
28. Traganos, F., and Z. Darzynkiewicz. 1994. Lysosomal proton pump activity: supravital cell staining with acridine orange differentiates leukocytes subpopulations. Methods Cell Biol. 41:185-194.
29. Kagan, B.L., M.E. Selsted, T. Ganz, and R.I. Lehrer. 1990. Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc. Natl. Acad. Sci. USA. 87:210-214.
30. Ganz, T., M.E. Selsted, and R.I. Lehrer. 1990. Defensins. Eur. J. Haematol. 44:1-8.
31. Lehrer, R.I., T. Ganz, and M.E. Selsted. 1990. Defensins: natural peptide antibiotics from neutrophils. ASM News. 56:315-318.
32. Carroll, S.F., and R.F. Martinez. 1981. Antibacterial peptide from normal rabbit serum. III. Inhibition of microbial electron transport. Biochemistry. 20:5988-5994.
33. Davies, K.A., Y. Hatefi, F.R. Salemme, and M.D. Kamen. 1972. Enzymic redox reactions of cytochromes c. Biochem. Biophys. Res. Commun. 49: 1329-1335.
34. Person, P., H. Zipper, A.S. Fine, and P.T. Mora. 1964. Macroion interactions involving cytochrome system components. J. Biol. Chem. 239:4159-4162.
35. Smith, L., H.C. Davies, and M.E. Nava. 1976. Evidence for binding sites on cytochrome c for oxidases and reductases from studies of different cytochromes c of known structure. Biochemistry. 15:5827-5831.
36. Charp, P.A., W.G. Rice, R.L. Raynor, E. Reimund, J.M. Kinkade, T. Ganz, M.E. Selsled, R.I. Lehrer, and J.F. Kuo. 1988. Inhibition of protein kinase C by defensins, antibiotic peptides from human neutrophils. Biochem. Pharmacol. 37:951-956.
37. Kordel, M., R. Benz, and H.G. Sahl. 1988. Mode of action of the staphylococcin-like peptide Pep-5: voltage-dependent depolarization of bacterial and artificial membranes. J. Bacteriol. 170:84-88.
38. Ruhr, E., and H.G. Sahl. 1985. Mode of action of the peptide antibiotic nisin and influence on the membrane potential of whole cells and on cytoplasmic and artificial membrane vesicles. Antimicrob. Agents Chemother. 27:841-845.
39. Kempf, C., R. Klausner, J.N. Weinstein, J. van Renswoude, M. Pincus, and R. Blumenthal. 1982. Voltage-dependent transbilayer orientation of melittin. J. Biol. Chem. 257:2469-2476.
40. Konisky, J. 1982. Colicins and other bacteriocins with established modes of action. Annu. Rev. Microbiol. 36:125-144.
41. Yang, C.C., and J. Konisky. 1984. Colicin V-treated Escherichia coli does not generate membrane potential. J. Bacteriol. 158:757-759.
42. Ohta, M., H. Ito, K. Masuda, S. Tanaka, Y. Arakawa, R. Wacharotayankun, and N. Kato. 1992. Mechanisms of antibacterial action of tachyplesins and polyphemusins, a group of antimicrobial peptides isolated from horseshoe crab hemocytes. Antimicrob. Agents Chemother. 36:1460-1465.