Staphylococcus epidermidis — the 'accidental' pathogen (original) (raw)
CDC. National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am. J. Infect. Control32, 470–485 (2004).
Uckay, I. et al. Foreign body infections due to Staphylococcus epidermidis. Ann. Med.41, 109–119 (2009). ArticleCASPubMed Google Scholar
Dimick, J. B. et al. Increased resource use associated with catheter-related bloodstream infection in the surgical intensive care unit. Arch. Surg.136, 229–234 (2001). ArticleCASPubMed Google Scholar
Rello, J. et al. Evaluation of outcome of intravenous catheter-related infections in critically ill patients. Am. J. Respir. Crit. Care Med.162, 1027–1030 (2000). ArticleCASPubMed Google Scholar
Rogers, K. L., Fey, P. D. & Rupp, M. E. Coagulase-negative staphylococcal infections. Infect. Dis. Clin. North Am.23, 73–98 (2009). This provides an excellent review on clinical aspects ofS. epidermidisinfections. ArticlePubMed Google Scholar
Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science284, 1318–1322 (1999). ArticleCASPubMed Google Scholar
Kloos, W. & Schleifer, K. H. in Bergey's Manual of Systematic Bacteriology (eds Sneath, P. H. A., Mair, N., Sharpe, M. E. & Holt, J. G.) 1013–1035 (Williams & Wilkins, Baltimore, 1986). Google Scholar
Kloos, W. E. & Musselwhite, M. S. Distribution and persistence of Staphylococcus and Micrococcus species and other aerobic bacteria on human skin. Appl. Microbiol.30, 381–385 (1975). CASPubMedPubMed Central Google Scholar
Gill, S. R. et al. 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 (2005). This article describes the sequencing and comparison of the genomes of biofilm-formingS. epidermidisandS. aureus. ArticleCASPubMedPubMed Central Google Scholar
Zhang, Y. Q. et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol.49, 1577–1593 (2003). ArticleCASPubMed Google Scholar
Wang, X. M. et al. Evaluation of a multilocus sequence typing system for Staphylococcus epidermidis. J. Med. Microbiol.52, 989–998 (2003). ArticleCASPubMed Google Scholar
Wisplinghoff, H. et al. Related clones containing SCC_mec_ type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob. Agents Chemother.47, 3574–3579 (2003). ArticleCASPubMedPubMed Central Google Scholar
Thomas, J. C. et al. Improved multilocus sequence typing scheme for Staphylococcus epidermidis. J. Clin. Microbiol.45, 616–619 (2007). ArticlePubMed Google Scholar
Miragaia, M., Thomas, J. C., Couto, I., Enright, M. C. & de Lencastre, H. Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data. J. Bacteriol.189, 2540–2552 (2007). This article details an investigation of the population structure ofS. epidermidis. ArticleCASPubMedPubMed Central Google Scholar
Li, M., Wang, X., Gao, Q. & Lu, Y. Molecular characterization of Staphylococcus epidermidis strains isolated from a teaching hospital in Shanghai, China. J. Med. Microbiol.58, 456–461 (2009). ArticleCASPubMed Google Scholar
Galdbart, J. O., Allignet, J., Tung, H. S., Ryden, C. & El Solh, N. Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J. Infect. Dis.182, 351–355 (2000). ArticleCASPubMed Google Scholar
Gu, J. et al. Bacterial insertion sequence IS_256_ as a potential molecular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis. J. Hosp. Infect.61, 342–348 (2005). ArticleCASPubMed Google Scholar
Kozitskaya, S. et al. The bacterial insertion sequence element IS_256_ occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides. Infect. Immun.72, 1210–1215 (2004). ArticleCASPubMedPubMed Central Google Scholar
Yao, Y. et al. Factors characterizing Staphylococcus epidermidis invasiveness determined by comparative genomics. Infect. Immun.73, 1856–1860 (2005). ArticleCASPubMedPubMed Central Google Scholar
Lina, G. et al. Bacterial competition for human nasal cavity colonization: role of staphylococcal agr alleles. Appl. Environ. Microbiol.69, 18–23 (2003). ArticleCASPubMedPubMed Central Google Scholar
O'Grady, N. P. et al. Guidelines for the prevention of intravascular catheter-related infections. MMWR Recomm. Rep.51, 1–26 (2002). PubMed Google Scholar
Chu, V. H. et al. Coagulase-negative staphylococcal prosthetic valve endocarditis — a contemporary update based on the International Collaboration on Endocarditis: prospective cohort study. Heart95, 570–576 (2009). ArticleCASPubMed Google Scholar
Massey, R. C., Horsburgh, M. J., Lina, G., Hook, M. & Recker, M. The evolution and maintenance of virulence in Staphylococcus aureus: a role for host-to-host transmission? Nature Rev. Microbiol.4, 953–958 (2006). This article reviews the mathematical model that explains the evolution of lifestyle differences betweenS. epidermidisandS. aureus. ArticleCAS Google Scholar
Otto, M., Sussmuth, R., Vuong, C., Jung, G. & Gotz, F. Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives. FEBS Lett.450, 257–262 (1999). ArticleCASPubMed Google Scholar
Carmody, A. B. & Otto, M. Specificity grouping of the accessory gene regulator quorum-sensing system of Staphylococcus epidermidis is linked to infection. Arch. Microbiol.181, 250–253 (2004). ArticleCASPubMed Google Scholar
Harder, J. & Schroder, J. M. Antimicrobial peptides in human skin. Chem. Immunol. Allergy86, 22–41 (2005). ArticleCASPubMed Google Scholar
Faurschou, M. & Borregaard, N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect.5, 1317–1327 (2003). ArticleCASPubMed Google Scholar
Pourmand, M. R., Clarke, S. R., Schuman, R. F., Mond, J. J. & Foster, S. J. Identification of antigenic components of Staphylococcus epidermidis expressed during human infection. Infect. Immun.74, 4644–4654 (2006). ArticleCASPubMedPubMed Central Google Scholar
Yao, Y., Sturdevant, D. E. & Otto, M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis.191, 289–298 (2005). An investigation of genome-wide gene regulatory changes that occur inS. epidermidisbiofilms. ArticleCASPubMed Google Scholar
Khardori, N., Yassien, M. & Wilson, K. Tolerance of Staphylococcus epidermidis grown from indwelling vascular catheters to antimicrobial agents. J. Ind. Microbiol.15, 148–151 (1995). ArticleCASPubMed Google Scholar
Duguid, I. G., Evans, E., Brown, M. R. & Gilbert, P. Effect of biofilm culture upon the susceptibility of Staphylococcus epidermidis to tobramycin. J. Antimicrobiol. Chemother.30, 803–810 (1992). ArticleCAS Google Scholar
Duguid, I. G., Evans, E., Brown, M. R. & Gilbert, P. Growth-rate-independent killing by ciprofloxacin of biofilm-derived Staphylococcus epidermidis; evidence for cell-cycle dependency. J. Antimicrobiol. Chemother.30, 791–802 (1992). ArticleCAS Google Scholar
O'Toole, G., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol.54, 49–79 (2000). ArticleCASPubMed Google Scholar
Vacheethasanee, K. et al. Bacterial surface properties of clinically isolated Staphylococcus epidermidis strains determine adhesion on polyethylene. J. Biomed. Mater. Res.42, 425–432 (1998). ArticleCASPubMed Google Scholar
Heilmann, C., Hussain, M., Peters, G. & Gotz, F. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol.24, 1013–1024 (1997). ArticleCASPubMed Google Scholar
Tormo, M. A., Knecht, E., Gotz, F., Lasa, I. & Penades, J. R. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology151, 2465–2475 (2005). ArticleCASPubMed Google Scholar
Mazmanian, S. K., Liu, G., Ton-That, H. & Schneewind, O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science285, 760–763 (1999). ArticleCASPubMed Google Scholar
Navarre, W. W. & Schneewind, O. Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev.63, 174–229 (1999). CASPubMedPubMed Central Google Scholar
Arrecubieta, C., Lee, M. H., Macey, A., Foster, T. J. & Lowy, F. D. SdrF, a Staphylococcus epidermidis surface protein, binds type I collagen. J. Biol. Chem.282, 18767–18776 (2007). ArticleCASPubMed Google Scholar
Hartford, O., O'Brien, L., Schofield, K., Wells, J. & Foster, T. J. The Fbe (SdrG) protein of Staphylococcus epidermidis HB promotes bacterial adherence to fibrinogen. Microbiology147, 2545–2552 (2001). ArticleCASPubMed Google Scholar
Heilmann, C. et al. Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology149, 2769–2778 (2003). ArticleCASPubMed Google Scholar
McCrea, K. W. et al. The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis. Microbiology146, 1535–1546 (2000). ArticleCASPubMed Google Scholar
Nilsson, M. et al. A fibrinogen-binding protein of Staphylococcus epidermidis. Infect. Immun.66, 2666–2673 (1998). CASPubMedPubMed Central Google Scholar
Guo, B., Zhao, X., Shi, Y., Zhu, D. & Zhang, Y. Pathogenic implication of a fibrinogen-binding protein of Staphylococcus epidermidis in a rat model of intravascular-catheter-associated infection. Infect. Immun.75, 2991–2995 (2007). ArticleCASPubMedPubMed Central Google Scholar
Ponnuraj, K. et al. A “dock, lock, and latch” structural model for a staphylococcal adhesin binding to fibrinogen. Cell115, 217–228 (2003). This work elucidated the mechanism by which SdrG binds to fibrinogen. ArticleCASPubMed Google Scholar
Sellman, B. R. et al. Expression of Staphylococcus epidermidis SdrG increases following exposure to an in vivo environment. Infect. Immun.76, 2950–2957 (2008). ArticleCASPubMedPubMed Central Google Scholar
Arrecubieta, C. et al. SdrF, a Staphylococcus epidermidis surface protein, contributes to the initiation of ventricular assist device driveline-related infections. PLoS Pathog.5, e1000411 (2009). ArticleCASPubMedPubMed Central Google Scholar
Bowden, M. G. et al. Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis. Microbiology151, 1453–1464 (2005). ArticleCASPubMed Google Scholar
Gross, M., Cramton, S. E., Gotz, F. & Peschel, A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun.69, 3423–3426 (2001). ArticleCASPubMedPubMed Central Google Scholar
Sadovskaya, I., Vinogradov, E., Flahaut, S., Kogan, G. & Jabbouri, S. Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect. Immun.73, 3007–3017 (2005). ArticleCASPubMedPubMed Central Google Scholar
Rice, K. C. et al. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl Acad. Sci. USA104, 8113–8118 (2007). ArticleCASPubMedPubMed Central Google Scholar
Mack, D. et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol.178, 175–183 (1996). This article details the structural characterization of the exopolysaccharide PNAG. ArticleCASPubMedPubMed Central Google Scholar
Darby, C., Hsu, J. W., Ghori, N. & Falkow, S. Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature417, 243–244 (2002). ArticleCASPubMed Google Scholar
Wang, X., Preston, J. F. I. & Romeo, T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol.186, 2724–2734 (2004). ArticleCASPubMedPubMed Central Google Scholar
Heilmann, C., Gerke, C., Perdreau-Remington, F. & Gotz, F. Characterization of Tn_917_ insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun.64, 277–282 (1996). CASPubMedPubMed Central Google Scholar
Heilmann, C. et al. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol.20, 1083–1091 (1996). This work identified the genetic locus that governs PNAG biosynthesis. ArticleCASPubMed Google Scholar
Francois, P. et al. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol. Med. Microbiol.35, 135–140 (2003). ArticleCASPubMed Google Scholar
Rupp, M. E., Ulphani, J. S., Fey, P. D., Bartscht, K. & Mack, D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect. Immun.67, 2627–2632 (1999). This was the firstin vivoanalysis of anS. epidermidisvirulence determinant (PNAG) using an isogenic mutant. CASPubMedPubMed Central Google Scholar
Rupp, M. E., Ulphani, J. S., Fey, P. D. & Mack, D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect. Immun.67, 2656–2659 (1999). CASPubMedPubMed Central Google Scholar
Chokr, A., Leterme, D., Watier, D. & Jabbouri, S. Neither the presence of ica locus, nor _in vitro_-biofilm formation ability is a crucial parameter for some Staphylococcus epidermidis strains to maintain an infection in a guinea pig tissue cage model. Microb. Pathog.42, 94–97 (2007). ArticleCASPubMed Google Scholar
Fluckiger, U. et al. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect. Immun.73, 1811–1819 (2005). ArticleCASPubMedPubMed Central Google Scholar
Gerke, C., Kraft, A., Sussmuth, R., Schweitzer, O. & Gotz, F. Characterization of the _N_-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J. Biol. Chem.273, 18586–18593 (1998). This article describes the identification of the biochemical function of the IcaA and IcaD proteins. ArticleCASPubMed Google Scholar
Vuong, C. et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem.279, 54881–54886 (2004). This study identified the biochemical function of the IcaB PNAG de-acetylase and showed its rolein vitroandin vivo. ArticleCASPubMed Google Scholar
O'Gara, J. P. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett.270, 179–188 (2007). ArticleCASPubMed Google Scholar
Ziebuhr, W. et al. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS_256_. Mol. Microbiol.32, 345–356 (1999). ArticleCASPubMed Google Scholar
Knobloch, J. K. et al. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J. Bacteriol.183, 2624–2633 (2001). ArticleCASPubMedPubMed Central Google Scholar
Mack, D. et al. Identification of three essential regulatory gene loci governing expression of Staphylococcus epidermidis polysaccharide intercellular adhesin and biofilm formation. Infect. Immun.68, 3799–3807 (2000). ArticleCASPubMedPubMed Central Google Scholar
Tormo, M. A. et al. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J. Bacteriol.187, 2348–2356 (2005). ArticleCASPubMedPubMed Central Google Scholar
Handke, L. D. et al. σB and SarA independently regulate polysaccharide intercellular adhesin production in Staphylococcus epidermidis. Can. J. Microbiol.53, 82–91 (2007). ArticleCASPubMed Google Scholar
Al Laham, N. et al. Augmented expression of polysaccharide intercellular adhesin in a defined Staphylococcus epidermidis mutant with the small-colony-variant phenotype. J. Bacteriol.189, 4494–4501 (2007). ArticleCASPubMedPubMed Central Google Scholar
Xu, L. et al. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect. Immun.74, 488–496 (2006). ArticleCASPubMedPubMed Central Google Scholar
Vuong, C., Gerke, C., Somerville, G. A., Fischer, E. R. & Otto, M. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J. Infect. Dis.188, 706–718 (2003). ArticleCASPubMed Google Scholar
Kogan, G., Sadovskaya, I., Chaignon, P., Chokr, A. & Jabbouri, S. Biofilms of clinical strains of Staphylococcus that do not contain polysaccharide intercellular adhesin. FEMS Microbiol. Lett.255, 11–16 (2006). ArticleCASPubMed Google Scholar
Rohde, H. et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials28, 1711–1720 (2007). This article gives an exceptionally balanced view of the roles of proteins versus exopolysaccharide inS. epidermisbiofilm formation, in contrast to several reports that point to the importance of protein-mediated biofilm formation. ArticleCASPubMed Google Scholar
Hussain, M., Herrmann, M., von Eiff, C., Perdreau-Remington, F. & Peters, G. A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces. Infect. Immun.65, 519–524 (1997). CASPubMedPubMed Central Google Scholar
Rohde, H. et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol.55, 1883–1895 (2005). ArticleCASPubMed Google Scholar
Conrady, D. G. et al. A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc. Natl Acad. Sci. USA105, 19456–19461 (2008). This work shed light on the mechanism of Aap self-aggregation. ArticleCASPubMedPubMed Central Google Scholar
Banner, M. A. et al. Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J. Bacteriol.189, 2793–2804 (2007). ArticleCASPubMedPubMed Central Google Scholar
Bateman, A., Holden, M. T. & Yeats, C. The G5 domain: a potential _N_-acetylglucosamine recognition domain involved in biofilm formation. Bioinformatics21, 1301–1303 (2005). ArticleCASPubMed Google Scholar
Sun, D., Accavitti, M. A. & Bryers, J. D. Inhibition of biofilm formation by monoclonal antibodies against Staphylococcus epidermidis RP62A accumulation-associated protein. Clin. Diagn. Lab. Immunol.12, 93–100 (2005). CASPubMedPubMed Central Google Scholar
Conlon, K. M., Humphreys, H. & O'Gara, J. P. Inactivations of rsbU and sarA by IS_256_ represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J. Bacteriol.186, 6208–6219 (2004). ArticleCASPubMedPubMed Central Google Scholar
Chaignon, P. et al. Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl. Microbiol. Biotechnol.75, 125–132 (2007). ArticleCASPubMed Google Scholar
Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B. & Otto, M. Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J. Infect. Dis.190, 1498–1505 (2004). This manuscript shows the role of theS. epidermidis agrquorum sensing regulatorin vivo. ArticlePubMed Google Scholar
Yarwood, J. M., Bartels, D. J., Volper, E. M. & Greenberg, E. P. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol.186, 1838–1850 (2004). ArticleCASPubMedPubMed Central Google Scholar
Teufel, P. & Gotz, F. Characterization of an extracellular metalloprotease with elastase activity from Staphylococcus epidermidis. J. Bacteriol.175, 4218–4224 (1993). ArticleCASPubMedPubMed Central Google Scholar
Dubin, G. et al. Molecular cloning and biochemical characterisation of proteases from Staphylococcus epidermidis. Biol. Chem.382, 1575–1582 (2001). ArticleCASPubMed Google Scholar
Ohara-Nemoto, Y. et al. Characterization and molecular cloning of a glutamyl endopeptidase from Staphylococcus epidermidis. Microb. Pathog.33, 33–41 (2002). ArticleCASPubMed Google Scholar
Kaplan, J. B. et al. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol.186, 8213–8220 (2004). ArticleCASPubMedPubMed Central Google Scholar
Kaplan, J. B., Ragunath, C., Ramasubbu, N. & Fine, D. H. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β-hexosaminidase activity. J. Bacteriol.185, 4693–4698 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kong, K. F., Vuong, C. & Otto, M. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol.296, 133–139 (2006). ArticleCASPubMed Google Scholar
Vuong, C. et al. Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epidermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modulins. Cell. Microbiol.6, 753–759 (2004). ArticleCASPubMed Google Scholar
Yao, Y. et al. Characterization of the Staphylococcus epidermidis accessory-gene regulator response: quorum-sensing regulation of resistance to human innate host defence. J. Infect. Dis.193, 841–848 (2006). ArticlePubMed Google Scholar
Kocianova, S. et al. Key role of poly-γ-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J. Clin. Invest.115, 688–694 (2005). This article investigates the role of poly-γ-DL-glutamic acid inS. epidermidis. ArticleCASPubMedPubMed Central Google Scholar
Little, S. F. & Ivins, B. E. Molecular pathogenesis of Bacillus anthracis infection. Microbes Infect.1, 131–139 (1999). ArticleCASPubMed Google Scholar
Oppermann-Sanio, F. B. & Steinbuchel, A. Occurrence, functions and biosynthesis of polyamides in microorganisms and biotechnological production. Naturwissenschaften89, 11–22 (2002). ArticlePubMed Google Scholar
Kristian, S. A. et al. Biofilm formation induces C3a release and protects Staphylococcus epidermidis from IgG and complement deposition and from neutrophil-dependent killing. J. Infect. Dis.197, 1028–1035 (2008). ArticlePubMed Google Scholar
Vuong, C. et al. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell. Microbiol.6, 269–275 (2004). This study shows the important role of PNAG in immune evasion. ArticleCASPubMed Google Scholar
Begun, J. et al. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defences. PLoS Pathog.3, e57 (2007). ArticleCASPubMedPubMed Central Google Scholar
Mah, T. F. et al. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature426, 306–310 (2003). ArticleCASPubMed Google Scholar
Heine, H. & Ulmer, A. J. Recognition of bacterial products by Toll-like receptors. Chem. Immunol. Allergy86, 99–119 (2005). ArticleCASPubMed Google Scholar
Stevens, N. T. et al. Staphylococcus epidermidis polysaccharide intercellular adhesin induces IL-8 expression in human astrocytes via a mechanism involving TLR2. Cell. Microbiol.11, 421–432 (2008). ArticleCASPubMed Google Scholar
Henneke, P. et al. Lipoproteins are critical TLR2 activating toxins in group B streptococcal sepsis. J. Immunol.180, 6149–6158 (2008). ArticleCASPubMed Google Scholar
Li, H., Nooh, M. M., Kotb, M. & Re, F. Commercial peptidoglycan preparations are contaminated with superantigen-like activity that stimulates IL-17 production. J. Leukoc. Biol.83, 409–418 (2008). ArticleCASPubMed Google Scholar
Hashimoto, M. et al. Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J. Immunol.177, 3162–3169 (2006). ArticleCASPubMed Google Scholar
Mehlin, C., Headley, C. M. & Klebanoff, S. J. An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J. Exp. Med.189, 907–918 (1999). This article describes the identification and pro-inflammatory properties of the mainS. epidermidisPSMs. ArticleCASPubMedPubMed Central Google Scholar
Wang, R. et al. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nature Med.13, 1510–1514 (2007). ArticleCASPubMed Google Scholar
Hajjar, A. M. et al. Cutting edge: functional interactions between Toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol.166, 15–19 (2001). ArticleCASPubMed Google Scholar
Lambert, P. A., Worthington, T., Tebbs, S. E. & Elliott, T. S. Lipid S, a novel Staphylococcus epidermidis exocellular antigen with potential for the serodiagnosis of infections. FEMS Immunol. Med. Microbiol.29, 195–202 (2000). ArticleCASPubMed Google Scholar
Li, M. et al. Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl Acad. Sci. USA104, 9469–9474 (2007). This work identified and characterized the first Gram-positive AMP sensor inS. epidermidis. ArticleCASPubMedPubMed Central Google Scholar
Peschel, A. et al. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem.274, 8405–8410 (1999). ArticleCASPubMed Google Scholar
Peschel, A. et al. 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 (2001). ArticleCASPubMedPubMed Central Google Scholar
Li, M. et al. The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol. Microbiol.66, 1136–1147 (2007). ArticleCASPubMed Google Scholar
Bader, M. W. et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell122, 461–472 (2005). ArticleCASPubMed Google Scholar
Marin, M. E., de la Rosa, M. C. & Cornejo, I. Enterotoxigenicity of Staphylococcus strains isolated from Spanish dry-cured hams. Appl. Environ. Microbiol.58, 1067–1069 (1992). CASPubMedPubMed Central Google Scholar
Bautista, L., Gaya, P., Medina, M. & Nunez, M. A quantitative study of enterotoxin production by sheep milk staphylococci. Appl. Environ. Microbiol.54, 566–569 (1988). CASPubMedPubMed Central Google Scholar
Klingenberg, C. et al. Persistent strains of coagulase-negative staphylococci in a neonatal intensive care unit: virulence factors and invasiveness. Clin. Microbiol. Infect.13, 1100–1111 (2007). ArticleCASPubMed Google Scholar
Scheifele, D. W., Bjornson, G. L., Dyer, R. A. & Dimmick, J. E. Delta-like toxin produced by coagulase-negative staphylococci is associated with neonatal necrotizing enterocolitis. Infect. Immun.55, 2268–2273 (1987). CASPubMedPubMed Central Google Scholar
Rohde, H. et al. Detection of virulence-associated genes not useful for discriminating between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J. Clin. Microbiol.42, 5614–5619 (2004). ArticleCASPubMedPubMed Central Google Scholar
Ziebuhr, W. et al. Modulation of the polysaccharide intercellular adhesin (PIA) expression in biofilm forming Staphylococcus epidermidis. Analysis of genetic mechanisms. Adv. Exp. Med. Biol.485, 151–157 (2000). ArticleCASPubMed Google Scholar
Rogers, K. L., Rupp, M. E. & Fey, P. D. The presence of icaADBC is detrimental to the colonization of human skin by Staphylococcus epidermidis. Appl. Environ. Microbiol.74, 6155–6157 (2008). ArticleCASPubMedPubMed Central Google Scholar
Lai, Y. et al. The human anionic antimicrobial peptide dermcidin induces proteolytic defence mechanisms in staphylococci. Mol. Microbiol.63, 497–506 (2007). ArticleCASPubMed Google Scholar
Diekema, D. J. et al. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin. Infect. Dis.32, S114–S132 (2001). ArticleCASPubMed Google Scholar
Vos, M. C., Ott, A. & Verbrugh, H. A. Successful search-and-destroy policy for methicillin-resistant Staphylococcus aureus in The Netherlands. J. Clin. Microbiol.43, 2034; author reply 2034–2035 (2005). ArticlePubMedPubMed Central Google Scholar
van Pelt, C. et al. Strict infection control measures do not prevent clonal spread of coagulase negative staphylococci colonizing central venous catheters in neutropenic hemato-oncologic patients. FEMS Immunol. Med. Microbiol.38, 153–158 (2003). ArticleCASPubMed Google Scholar
Chambers, H. F., Hartman, B. J. & Tomasz, A. Increased amounts of a novel penicillin-binding protein in a strain of methicillin-resistant Staphylococcus aureus exposed to nafcillin. J. Clin. Invest.76, 325–331 (1985). ArticleCASPubMedPubMed Central Google Scholar
Ma, X. X. et al. Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob. Agents Chemother.46, 1147–1152 (2002). ArticleCASPubMedPubMed Central Google Scholar
Miragaia, M., Couto, I. & de Lencastre, H. Genetic diversity among methicillin-resistant Staphylococcus epidermidis (MRSE). Microb. Drug Resist.11, 83–93 (2005). ArticleCASPubMed Google Scholar
Diep, B. A. et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J. Infect. Dis.197, 1523–1530 (2008). ArticleCASPubMed Google Scholar
Miragaia, M. et al. Molecular characterization of methicillin-resistant Staphylococcus epidermidis clones: evidence of geographic dissemination. J. Clin. Microbiol.40, 430–438 (2002). ArticleCASPubMedPubMed Central Google Scholar
Raad, I., Hanna, H. & Maki, D. Intravascular catheter-related infections: advances in diagnosis, prevention, and management. Lancet Infect. Dis.7, 645–657 (2007). ArticlePubMed Google Scholar
Schwalbe, R. S., Stapleton, J. T. & Gilligan, P. H. Emergence of vancomycin resistance in coagulase-negative staphylococci. N. Engl. J. Med.316, 927–931 (1987). ArticleCASPubMed Google Scholar
Gagnon, R. F., Richards, G. K. & Subang, R. Vancomycin therapy of experimental peritoneal catheter-associated infection (Staphylococcus epidermidis) in a mouse model. Perit. Dial. Int.13 (Suppl. 2), 310–312 (1993). Google Scholar
Richards, G. K., Prentis, J. & Gagnon, R. F. Antibiotic activity against Staphylococcus epidermidis biofilms in dialysis fluids. Adv. Perit. Dial.5, 133–137 (1989). CASPubMed Google Scholar
Raad, I. et al. Comparative activities of daptomycin, linezolid, and tigecycline against catheter-related methicillin-resistant Staphylococcus bacteremic isolates embedded in biofilm. Antimicrob. Agents Chemother.51, 1656–1660 (2007). ArticleCASPubMedPubMed Central Google Scholar
Hanssen, A. M., Kjeldsen, G. & Sollid, J. U. Local variants of staphylococcal cassette chromosome mec in sporadic methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci: evidence of horizontal gene transfer? Antimicrob. Agents Chemother.48, 285–296 (2004). ArticleCASPubMedPubMed Central Google Scholar
Diep, B. A. et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet367, 731–739 (2006). ArticleCASPubMed Google Scholar
Otto, M. Targeted immunotherapy for staphylococcal infections: focus on anti-MSCRAMM antibodies. BioDrugs22, 27–36 (2008). ArticleCASPubMed Google Scholar
Marraffini, L. A. & Sontheimer, E. J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science322, 1843–1845 (2008). This article describes the functional characterization of CRISPR sequences inS. epidermidis. ArticleCASPubMedPubMed Central Google Scholar
Rupp, M. E., Fey, P. D., Heilmann, C. & Gotz, F. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J. Infect. Dis.183, 1038–1042 (2001). ArticleCASPubMed Google Scholar
Pintens, V. et al. The role of σB in persistence of Staphylococcus epidermidis foreign body infection. Microbiology154, 2827–2836 (2008). ArticleCASPubMed Google Scholar
Vandecasteele, S. J., Peetermans, W. E., Merckx, R. & Van Eldere, J. Expression of biofilm-associated genes in Staphylococcus epidermidis during in vitro and in vivo foreign body infections. J. Infect. Dis.188, 730–737 (2003). ArticleCASPubMed Google Scholar
Vuong, C., Kocianova, S., Yu, J., Kadurugamuwa, J. L. & Otto, M. Development of real-time in vivo imaging of device-related Staphylococcus epidermidis infection in mice and influence of animal immune status on susceptibility to infection. J. Infect. Dis.198, 258–261 (2008). ArticlePubMed Google Scholar
Novick, R. P. & Geisinger, E. Quorum sensing in staphylococci. Annu. Rev. Genet.42, 541–564 (2008). ArticleCASPubMed Google Scholar
Novick, R. P. et al. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J.12, 3967–3975 (1993). ArticleCASPubMedPubMed Central Google Scholar
Queck, S. Y. et al. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell32, 150–158 (2008). ArticleCASPubMedPubMed Central Google Scholar
Mayville, P. et al. Structure–activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl Acad. Sci. USA96, 1218–1223 (1999). ArticleCASPubMedPubMed Central Google Scholar
Otto, M., Sussmuth, R., Jung, G. & Gotz, F. Structure of the pheromone peptide of the Staphylococcus epidermidis agr system. FEBS Lett.424, 89–94 (1998). ArticleCASPubMed Google Scholar
Otto, M. Staphylococcus aureus and Staphylococcus epidermidis peptide pheromones produced by the accessory gene regulator agr system. Peptides22, 1603–1608 (2001). ArticleCASPubMed Google Scholar
Otto, M., Echner, H., Voelter, W. & Gotz, F. Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun.69, 1957–1960 (2001). ArticleCASPubMedPubMed Central Google Scholar
Vuong, C., Gotz, F. & Otto, M. Construction and characterization of an agr deletion mutant of Staphylococcus epidermidis. Infect. Immun.68, 1048–1053 (2000). ArticleCASPubMedPubMed Central Google Scholar
Simons, J. W. et al. Cloning, purification and characterisation of the lipase from Staphylococcus epidermidis — comparison of the substrate selectivity with those of other microbial lipases. Eur. J. Biochem.253, 675–683 (1998). ArticleCASPubMed Google Scholar
Farrell, A. M., Foster, T. J. & Holland, K. T. Molecular analysis and expression of the lipase of Staphylococcus epidermidis. J. Gen. Microbiol.139, 267–277 (1993). ArticleCASPubMed Google Scholar
Longshaw, C. M., Farrell, A. M., Wright, J. D. & Holland, K. T. Identification of a second lipase gene, gehD, in Staphylococcus epidermidis: comparison of sequence with those of other staphylococcal lipases. Microbiology146, 1419–1427 (2000). ArticleCASPubMed Google Scholar
Lindsay, J. A., Riley, T. V. & Mee, B. J. Production of siderophore by coagulase-negative staphylococci and its relation to virulence. Eur. J. Clin. Microbiol. Infect. Dis.13, 1063–1066 (1994). ArticleCASPubMed Google Scholar
Cotton, J. L., Tao, J. & Balibar, C. J. Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry48, 1025–1035 (2009). ArticleCASPubMed Google Scholar
Cockayne, A. et al. Molecular cloning of a 32-kilodalton lipoprotein component of a novel iron-regulated Staphylococcus epidermidis ABC transporter. Infect. Immun.66, 3767–3774 (1998). CASPubMedPubMed Central Google Scholar
Chamberlain, N. R. & Brueggemann, S. A. Characterisation and expression of fatty acid modifying enzyme produced by Staphylococcus epidermidis. J. Med. Microbiol.46, 693–697 (1997). ArticleCASPubMed Google Scholar
Park, P. W., Rosenbloom, J., Abrams, W. R., Rosenbloom, J. & Mecham, R. P. Molecular cloning and expression of the gene for elastin-binding protein (ebpS) in Staphylococcus aureus. J. Biol. Chem.271, 15803–15809 (1996). ArticleCASPubMed Google Scholar