DltABCD- and MprF-mediated cell envelope modifications of Staphylococcus aureus confer resistance to platelet microbicidal proteins and contribute to virulence in a rabbit endocarditis model

Infection and Immunity

Volumn 73, Issue 12, 2005, Pages 8033-8038

  Weidenmaier, Christopher ^a   Peschel, Andreas ^a   Kempf, Volkhard A J ^a   Lucindo, Natalie ^b,c   Yeaman, Michael R ^b,c,d   Bayer, Arnold S ^b,c,d  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b HARBOR UCLA MEDICAL CENTER   (United States)

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

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALPHA DEFENSIN; ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; CATIONIC ANTIMICROBIAL PEPTIDE; FIBRINOGEN; FIBRONECTIN; LYSINE; PHOSPHATIDYLGLYCEROL; PROTEIN DLTABCD; PROTEIN MPRF; TEICHOIC ACID; THROMBIN INDUCED PLATELET MICROBICIDAL PROTEIN 1; THROMBOCYTE FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CELL ADHESION; CELL STRAIN; CONTROLLED STUDY; ENDOCARDITIS; ENDOTHELIUM CELL; ENDOVASCULAR INFECTION; GENE MUTATION; HUMAN; HUMAN CELL; INFECTION RESISTANCE; KIDNEY INFECTION; MICROBIAL COLONIZATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN MODIFICATION; RABBIT; SPLEEN; STAPHYLOCOCCUS AUREUS; VASCULAR DISEASE;

ANIMALS; BACTERIAL PROTEINS; BLOOD PROTEINS; CELL ADHESION; CELL MEMBRANE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, BACTERIAL; ENDOCARDITIS, BACTERIAL; ENDOTHELIAL CELLS; FIBRINOGEN; FIBRONECTINS; GENE DELETION; MEMBRANE PROTEINS; MUTATION; RABBITS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS; VIRULENCE;

EID: 28444471602     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.12.8033-8038.2005     Document Type: Article

References (43)

1. Bayer, A. S., D. Cheng, M. R. Yeaman, G. R. Corey, R. S. McClelland, L. J. Barrel, and V. G. Fowler, Jr. 1998. In vitro resistance to thrombin-induced platelet microbicidal protein among clinical bacteremic isolates of Staphylococcus aureus correlates with an endovascular infectious source. Antimicrob. Agents Chemother. 42:3169-3172.
2. + antiporter operon is associated with resistance to the microbicidal activity of thrombin-induced platelet microbicidal protein-1 in Staphylococcus aureus, abstr. 2482. Abstr. 103rd Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, D.C.
3. Bayer, A. S., R. Prasad, J. Chandra, A. Koul, M. Smriti, A. Varma, R. A. Skurray, N. Firth, M. H. Brown, S.-P. Koo, and M. R. Yeaman. 2000. In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal proteins is associated with alterations in cytoplasmic membrane fluidity. Infect. Immun. 68:3548-3553.
4. Cole, A. M., T. Ganz, A. M. Liese, M. D. Burdick, L. Liu, and R. M. Strieter. 2001. Cutting edge: IFN-inducible ELR-CXC chemokines display defensin-like antimicrobial activity. J. Immunol. 167:623-627.
5. Collins, L. V., S. A. Kristian, C. Weidenmaier, M. Faigle, K. P. Van Kessel, J. A. Van Strijp, F. Götz, B. Neumeister, and A. Peschel. 2002. Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J. Infect. Dis. 186:214-219.
6. De Haas, C. J., K. E. Veldkamp, A. Peschel, F. Weerkamp, W. J. van Wamel, E. C. Heezius, M. J. Poppelier, K. P. Van Kessel, and J. A. Van Strijp. 2004. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J. Exp. Med. 199:687-695.
7. Dhawan, V. K., A. S. Bayer, and M. R. Yeaman. 1998. In vitro resistance to thrombin-induced platelet microbicidal protein is associated with enhanced progression and hematogenous dissemination in experimental Staphylococcus aureus infective endocarditis. Infect. Immun. 66:3476-3479.
8. 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. 65:3293-3299.
9. Dürr, M., and A. Peschel. 2002. Chemokines meet defensins-the merging concepts of chemoattractants and antimicrobial peptides in host defense. Infect. Immun. 70:6515-6517.
10. Fedtke, I., F. Götz, and A. Peschel. 2004. Bacterial evasion of innate host defenses-the Staphylococcus aureus lesson. Int. J. Med. Microbiol. 294:189-194.
11. Fowler, V. G., Jr., G. Sakoulas, L. M. McIntyre, V. G. Meka, R. D. Arbeit, C. H. Cabell, M. E. Stryjewski, G. M. Eliopoulos, L. B. Reller, G. R. Corey, T. Jones, N. Lucindo, M. R. Yeaman, and A. S. Bayer. 2004. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J. Infect. Dis. 190:1140-1149.
12. Greene, C., D. McDevitt, P. Francois, P. E. Vaudaux, D. P. Lew, and T. J. Foster. 1995. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol. Microbiol. 17:1143-1152.
13. Hussain, M., C. Heilmann, G. Peters, and M. Herrmann. 2001. Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin. Microb. Pathog. 31:261-270.
14. Ing, M. B., L. M. Baddour, and A. S. Bayer. 1997. Bacteremia and infective endocarditis: pathogenesis, diagnosis, and complications, p. 331-354. In K. B. Crossley and G. L. Archer (ed.), The staphylococci in human disease. Churchill Livingstone, New York, N.Y.
15. Iordanescu, S., and M. Surdeanu. 1976. Two restriction and modification systems in Staphylococcus aureus NCTC8325. J. Gen. Microbiol. 96:277-281.
16. Koprivnjak, T., A. Peschel, M. H. Gelb, N. S. Liang, and J. P. Weiss. 2002. Role of charge properties of bacterial envelope in bactericidal action of human group HA phospholipase A2 against Staphylococcus aureus. J. Biol. Chem. 277:47636-47644.
17. Krygsveld, J., S. A. J. Zaat, J. Meeldijk, P. A. van Veelen, G. Fang, B. Poolman, E. Brandt, J. E. Ehlert, A. J. Kuijpers, G. H. M. Engbers, J. Feijen, and J. Dankert. 2000. Thrombocidins, microbicidal proteins from human blood platelets, are C-terminal deletion products of CXC chemokines. J. Biol. Chem. 275:20374-20381.
18. Kristian, S. A., M. Dürr, J. A. Van Strijp, B. Neumeister, and A. Peschel. 2003. MprF-mediated lysinylation of phospholipids in Staphylococcus aureus leads to protection against oxygen-independent neutrophil killing. Infect. Immun. 71:546-549.
19. Kristian, S. A., X. Lauth, V. Nizet, F. Götz, B. Neumeister, A. Peschel, and R. Landmann. 2003. Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model. J. Infect. Dis. 188:414-423.
20. Kupferwasser, L. I., R. A. Skurray, M. H. Brown, N. Firth, M. R. Yeaman, and A. S. Bayer. 1999. Plasmid-mediated resistance to thrombin-induced platelet microbicidal protein in staphylococci: role of the qacA locus. Antimicrob. Agents Chemother. 43:2395-2399.
21. Kupferwasser, L. I., R. A. Skurray, N. Firth, N. H. Brown, M. R. Yeaman, R. Prasad, M. Smriti, and A. S. Bayer. 2001. Staphylococcus aureus resistance to thrombin-induced platelet microbicidal protein-1 mediated by the qacA gene is specific and independent of multidrug efflux pump activity, abstr. 2288. Abstr. 101st Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, D.C.
22. Kupferwasser, L. I., M. R. Yeaman, S. M. Shapiro, C. C. Nast, and A. S. Bayer. 2002. In vitro susceptibility to thrombin-induced platelet microbicidal protein is associated with reduced disease progression and complication rates in experimental Staphylococcus aureus endocarditis: microbiological, histopathologic, and echocardiographic analyses. Circulation 105:746-752.
23. Midorikawa, K., K. Ouhara, H. Komatsuzawa, T. Kawai, S. Yamada, T. Fujiwara, K. Yamazaki, K. Sayama, M. A. Taubman, H. Kurihara, K. Hashimoto, and M. Sugai. 2003. Staphylococcus aureus susceptibility to innate antimicrobial peptides, beta-defensins and CAP18, expressed by human keratinocytes. Infect. Immun. 71:3730-3739.
24. Moreillon, P., Y. A. Que, and A. S. Bayer. 2002. Pathogenesis of streptococcal and staphylococcal endocarditis. Infect. Dis. Clin. N. Am. 16:297-318.
25. Nizet, V., T. Ohtake, X. Lauth, J. Trowbridge, J. Rudisill, R. A. Dorschner, V. Pestonjamasp, J. Piraino, K. Huttner, and R. L. Gallo. 2001. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414:454-457.
26. Peschel, A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179-186.
27. Peschel, A., R. W. Jack, M. Otto, L. V. Collins, P. Staubitz, G. Nicholson, H. Kalbacher, W. F. Nieuwenhuizen, G. Jung, A. Tarkowski, K. P. Van Kessel, and J. A. Van Strijp. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with L-lysine. J. Exp. Med. 193:1067-1076.
28. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J. Biol. Chem. 274: 8405-8410.
29. Proctor, R. A., P. van Langevelde, M. Kristjansson, J. N. Maslow, and R. D. Arbeit. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20:95-102.
30. Sullam, P. M., A. S. Bayer, W. M. Foss, and A. L. Cheung. 1996. Diminished platelet binding in vitro by Staphylococus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect. Immun. 64:4915-4921.
31. Tang, Y.-Q., M. R. Yeaman, and M. E. Selsted. 2002. Antimicrobial peptides from human platelets. Infect. Immun. 70:6524-6533.
32. Weidenmaier, C., J. F. Kokai-Kun, S. A. Kristian, T. Chanturyia, H. Kalbacber, M. Gross, G. Nicholson, B. Neumeister, J. J. Mond, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-245.
33. Weidenmaier, C., S. A. Kristian, and A. Peschel. 2003. Bacterial resistance to antimicrobial host defenses-an emerging target for novel antiinfective strategies? Curr. Drug Targets 4:643-649.
34. Weidenmaier, C., A. Peschel, Y. Q. Xiong, S. A. Kristian, K. Dietz, M. R. Yeaman, and A. S. Bayer. 2005. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J. Infect. Dis. 191:1771-1777.
35. Wolz, C., D. McDevitt, T. J. Foster, and A. L. Cheung. 1996. Influence of agr on fibrinogen binding in Staphylococcus aureus Newman. Infect. Immun. 64:3142-3147.
36. Wu, T., M. R. Yeaman, and A. S. Bayer. 1994. In vitro resistance to platelet microbicidal protein correlates with endocarditis source among bacteremic staphylococcal and streptococcal isolates. Antimicrob. Agents Chemother. 38:729-732.
37. Yeaman, M. R., and A. S. Bayer. 2000. Staphylococcus aureus, platelets, and the heart. Curr. Infect. Dis. Rep. 2:281-298.
38. Yeaman, M. R., A. S. Bayer, S.-P. Koo, W. Foss, and P. M. Sullam. 1998. Platelet microbicidal proteins and neutrophil defensin disrupt the Staphylococcus aureus cytoplasmic membrane by distinct mechanisms of action. J. Clin. Investig. 101:178-187.
39. Yeaman, M. R., J. C. Lee, and A. S. Bayer. 1999. Experimental Candida endocarditis, p. 1709-1720. In M. A. Sande and O. Zak (ed.), Handbook of animal model infections. Academic Press, San Diego, Calif.
40. Reference deleted.
41. 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.
42. Yeaman, M. R., and N. Y. Yount. 2005. Code among chaos: the immunorelativity and the AEGIS model of antimicrobial peptides. ASM News 71:21-27.
43. Yount, N. Y., K. D. Gank, Y. Q. Xiong, A. S. Bayer, T. Pender, W. H. Welch, and M. R. Yeaman. 2004. Platelet microbicidal protein 1: structural themes of a multifunctional antimicrobial peptide. Antimicrob. Agents Chemother. 48:4395-4404.