The Staphylococcus aureus two-component regulatory system, grars, senses and confers resistance to selected cationic antimicrobial peptides

Infection and Immunity

Volumn 80, Issue 1, 2012, Pages 74-81

  Yang, Soo Jin ^a,b   Bayer, Arnold S ^a,b   Mishra, Nagendra N ^a   Meehl, Michael ^c   Ledala, Nagender ^c   Yeaman, Michael R ^a,b   Xiong, Yan Q ^a,b   Cheung, Ambrose L ^c  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALPHA DEFENSIN; CALCIUM; DAPTOMYCIN; GENTAMICIN; NEUTROPHIL PEPTIDE 1; PHOSPHATIDYLGLYCEROL; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; THROMBOCYTE FACTOR 4; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN; TRANSCRIPTION FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM MUTANT; CONTROLLED STUDY; DLT GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE LOCUS; GENE REGULATORY NETWORK; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; GRAR GENE; HOST RESISTANCE; INNATE IMMUNITY; MAMMAL CELL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MPRF GENE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; SURFACE CHARGE; THROMBOCYTE; VRAG GENE; DRUG EFFECT; GENE DELETION; GENETICS; METABOLISM; MICROBIAL VIABILITY; SIGNAL TRANSDUCTION;

ANTIMICROBIAL CATIONIC PEPTIDES; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL VIABILITY; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION FACTORS;

EID: 84863230616     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05669-11     Document Type: Article

References (57)

1. Aricha B, et al. 2004. Differences in membrane fluidity and fatty acid composition between phenotypic variants of Streptococcus pneumoniae. J. Bacteriol. 186:4638-4644.
2. Arnaud M, Chastanet A, Debarbouille M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891.
3. Bader MW, et al. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
4. Bayer AS, et al. 2000. In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect. Immun. 68:3548-3553.
5. Bertsche U, et al. 2011. Correlation of daptomycin resistance in a clinical Staphylococcus aureus strain with increased cell wall teichoic acid production and D-alanylation. Antimicrob. Agents Chemother. 55:3922-3928.
6. Brogden KA. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250.
7. Climo MW, Patron RL, Archer GL. 1999. Combinations of vancomycin and _-lactams are synergistic against staphylococci with reduced susceptibilities to vancomycin. Antimicrob. Agents Chemother. 43:1747-1753.
8. Cui L, Murakami H, Kuwahara-Arai K, Hanaki H, Hiramatsu K. 2000. Contribution of a thickened cell wall and its glutamine nonamidated component to the vancomycin resistance expressed by Staphylococcus aureus Mu50. Antimicrob. Agents Chemother. 44:2276-2285.
9. Cui L, Tominaga E, Neoh H-M, Hiramatsu K. 2006. Correlation between reduced daptomycin susceptibility and vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob. Agents Chemother. 50:1079-1082.
10. De Lencastre H, et al. 1999. Antibiotic resistance as a stress response: complete sequencing of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb. Drug Resist. 5:163-175.
11. Dubrac S, Bisicchia P, Devine KM, Msadek T. 2008. A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol. Microbiol. 70:1307-1322.
12. Ernst C, et al. 2009. The bacterial defensin resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog. 5:e1000660.
13. Falord M, Mader U, Hiron A, Debarbouille M, Msadek T. 2011. Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. PLoS One 6:e21323.
14. Ganz T, Selsted ME, Lehrer RI. 1990. Defensins. Eur. J. Haematol. 44:1-8.
15. Gill SR, et al. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:2426-2438.
16. Hancock REW, Diamond G. 2000. The role of cationic antimicrobial peptides in innate host defenses. Trends Microbiol. 8:402-410.
17. Herbert S, et al. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102.
18. Howden BP, et al. 2008. Genomic analysis reveals a point mutation in the two-component sensor gene graS that leads to intermediate vancomycin resistance in clinical Staphylococcus aureus. Antimicrob. Agents Chemother. 52:3755-3762.
19. Jin T, et al. 2004. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172:1169-1176.
20. Jones T, et al. 2008. Failures in clinical treatment of Staphylococcus aureus infection with daptomycin are associated with alterations in surface charge, membrane phospholipid asymmetry, and drug binding. Antimicrob. Agents Chemother. 52:269-278.
21. Kilelee E, Pokorny A, Yeaman MR, Bayer AS. 2010. Lysylphosphatidylglycerol attenuates membrane perturbation rather than surface association of the cationic antimicrobial peptide 6W-RP-1 in a model membrane system: implications for daptomycin resistance. Antimicrob. Agents Chemother. 54:4476-4479.
22. Kuroda M, et al. 2001. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
23. Li M, et al. 2007. The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol. Microbiol. 66:1136-1147.
24. Li M, et al. 2007. Gram-positive three-component antimicrobial peptidesensing system. Proc. Natl. Acad. Sci. U. S. A. 104:9469-9474.
25. Matsuo M, Oogai Y, Kato F, Sugai M, Komatsuzawa H. 2011. Growthphase dependence of susceptibility to antimicrobial peptides in Staphylococcus aureus. Microbiology 157:1786-1797.
26. Meehl M, Herbert S, Gotz F, Cheung A. 2007. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 51:2679-2689.
27. Mezzano S, et al. 1992. Glomerular localization of platelet factor 4 in streptococcal nephritis. Nephron 61:58-63.
28. Mishra NN, et al. 2011. Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob. Agents Chemother. 55:526-531.
29. Mishra NN, et al. 2009. Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus (MRSA). Antimicrob. Agents Chemother. 53:2312-2318.
30. Mukhopadhyay K, et al. 2007. In vitro susceptibility of Staphylococcus aureus to thrombin-induced platelet microbicidal protein-1 (tPMP-1) is influenced by cell membrane phospholipid composition and asymmetry. Microbiology 153:1187-1197.
31. Nishi H, Komatsuzawa H, Fujiwara T, McCallum N, Sugai M. 2004. Reduced content of lysyl-phosphatidylglycerol in the cytoplasmic membrane affects susceptibility to moenomycin, as well as vancomycin, gentamicin, and antimicrobial peptides, in Staphylococcus aureus. Antimicrob. Agents Chemother. 48:4800-4807.
32. Ohki R, et al. 2003. The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol. Microbiol. 49:1135-1144.
33. Oku Y, Kurokawa K, Ichihashi N, Sekimizu K. 2004. Characterization of the Staphylococcus aureus mprF gene, involved in lysinylation of phosphatidylglycerol. Microbiology 150:45-51.
34. Pelegrini P, et al. 2009. A novel antimicrobial peptide from Crotalaria pallida seeds with activity against human and phytopathogens. Curr. Microbiol. 59:400-404.
35. Peschel A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179-186.
36. Peschel A, et al. 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.
37. Peschel A, et al. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410.
38. Peschel A, Sahl H-G. 2006. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4:529-536.
39. Rice KC, et al. 2003. The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J. Bacteriol. 185:2635-2643.
40. Sass P, Bierbaum G. 2009. Native graS mutation supports the susceptibility of Staphylococcus aureus strain SG511 to antimicrobial peptides. Int. J. Med. Microbiol. 299:313-322.
41. Shinitzky M, Barenholz Y. 1978. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta 515:367-394.
42. Sieprawska-Lupa M, et al. 2004. Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob. Agents Chemother. 48:4673-4679.
43. Soong LB, Ganz T, Ellison A, Caughey GH. 1997. Purification and characterization of defensins from cystic fibrosis sputum. Inflamm. Res. 46:98-102.
44. Staubitz P, Neumann H, Schneider T, Wiedemann I, Peschel A. 2004. MprF-mediated biosynthesis of lysylphosphatidylglycerol, an important determinant in staphylococcal defensin resistance. FEMS Microbiol. Lett. 231:67.
45. Utaida S, Pfeltz RF, Jayaswal RK, Wilkinson BJ. 2006. Autolytic properties of glycopeptide-intermediate Staphylococcus aureus Mu50. Antimicrob. Agents Chemother. 50:1541-1545.
46. Weidenmaier C, et al. 2005. 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. Infect. Immun. 73:8033-8038.
47. Welling MM, et al. 1998. Antibacterial activity of human neutrophil defensins in experimental infections in mice is accompanied by increased leukocyte accumulation. J. Clin. Invest. 102:1583-1590.
48. West AH, Stock AM. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369.
49. Xiong YQ, Bayer AS, Elazegui L, Yeaman MR. 2006. A synthetic congener modeled on a microbicidal domain of thrombin-induced platelet microbicidal protein-1 recapitulates staphylocidal mechanisms of the native molecule. Antimicrob. Agents Chemother. 50:3786-3792.
50. Xiong YQ, Mukhopadhyay K, Yeaman MR, Adler-Moore J, Bayer AS. 2005. Functional interrelationships between cell membrane and cell wall in antimicrobial peptide-mediated killing of Staphylococcus aureus. Antimicrob. Agents Chemother. 49:3114-3121.
51. Yang S-J, et al. 2010. Cell wall thickening is not a universal accompaniment of the daptomycin nonsusceptibility phenotype in Staphylococcus aureus: evidence for multiple resistance mechanisms. Antimicrob. Agents Chemother. 54:3079-3085.
52. Yang S-J, et al. 2005. A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon. J. Bacteriol. 187:5893-5900.
53. Yang SJ, et al. 2009. Enhanced expression of dltABCD is associated with development of daptomycin nonsusceptibility in a clinical endocarditis isolate of Staphylococcus aureus. J. Infect. Dis. 200:1916-1920.
54. Yang SJ, et al. 2009. Regulation of mprF in daptomycin-nonsusceptible Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2636-2637.
55. Yeaman MR, Bayer AS, Koo S-P, Foss W, Sullam PM. 1998. Platelet microbicidal proteins and neutrophil defensin disrupt the Staphylococcus aureus cytoplasmic membrane by distinct mechanisms of action. J. Clin. Invest. 101:178-187.
56. Yeaman MR, Gank KD, Bayer AS, Brass EP. 2002. Synthetic peptides that exert antimicrobial activities in whole blood and blood-derived matrices. Antimicrob. Agents Chemother. 46:3883-3891.
57. Yeaman MR, Puentes SM, Norman DC, Bayer AS. 1992. Partial characterization and staphylocidal activity of thrombin-induced platelet microbicidal protein. Infect. Immun. 60:1202-1209.