175
Views
28
CrossRef citations to date
0
Altmetric
Review

Immunoprophylaxis and immunotherapy of Staphylococcus epidermidis infections: challenges and prospects

, , &
Pages 319-334 | Published online: 09 Jan 2014

References

  • Iwase T, Uehara Y, Shinji H et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465, 346–349 (2010).
  • Khashu M, Osiovich H, Henry D, Al Khotani A, Solimano A, Speert DP. Persistent bacteremia and severe thrombocytopenia caused by coagulase-negative Staphylococcus in a neonatal intensive care unit. Pediatrics 117(2), 340–348 (2006).
  • Isenberg Y, Parada JP. Spontaneous vertebral osteomyelitis due to Staphylococcus epidermidis. J. Med. Microbiol. 59, 599–601 (2010).
  • Donlan RM, Costerton JM. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193 (2002).
  • Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108 (2004).
  • Lynch AS, Robertson GT. Bacterial and fungal biofilm infections. Annu. Rev. Med. 59, 415–428 (2008).
  • Huebner J, Goldmann DA. Coagulase-negative staphylococci: role as pathogens. Annu. Rev. Med. 50, 223–236 (1999).
  • Ziebuhr W, Hennig S, Eckart M, Kränzler H, Batzilla C, Kozitskaya S. Nosocomial infections by Staphylococcus epidermidis: how a commensal bacterium turns into a pathogen. Int. J. Antimicrob. Agents 28S, S14–S20 (2006).
  • Schoenfelder SMK, Lange C, Eckart M, Hennig S, Kozytska S, Ziebuhr W. Success through diversity – how Staphylococcus epidermidis establishes as a nosocomial pathogen. Int. J. Med. Microbiol. 300, 380–386 (2010).
  • Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H. Inferring a population structure of Staphylococcus epidermidis from multilocus sequence typing data. J. Bacteriol. 189, 2540–2552 (2007).
  • McCann MT, Gilmore BF, Gorman SP. Staphylococcus epidermidis device-related infections: pathogenesis and clinical management. J. Pharm. Pharmacol. 60, 1551–1571 (2008).
  • Piette A, Verschraegen G. Role of coagulase-negative staphylococci in human disease. Vet. Microbiol. 134, 45–54 (2009).
  • Rogers KL, Fey PD, Rupp ME. Coagulase-negative staphylococcal infections. Infect. Dis. Clin. N. Am. 23, 73–98 (2009).
  • Ziebandt AK, Kusch H, Degner M et al. Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation. Proteomics 10, 1634–1644 (2010).
  • Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322, 1843–1845 (2008).
  • Marraffini LA, Sontheimer EJ. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463, 568–572 (2010).
  • Kovitskaya S, Olson ME, Fey PD, Witte W, Ohlsen K, Ziebuhr W. Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J. Clin. Microbiol. 43, 4751–4757 (2005).
  • Mack D, Davies AP, Harris LG, Rohde H, Horstkotte MA, Knobloch JKM. Microbial interactions in Staphylococcus epidermidis biofilms. Anal. Bioanal. Chem. 387, 399–408 (2007).
  • O’Gara JP. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270, 179–188 (2007).
  • Otto M. Staphylococcal biofilms. Curr. Top. Microbiol. Immunol. 322, 207–228 (2008).
  • Mack D, Davies AP, Harris LG, Knobloch JKM, Rohde H. Staphylococcus epidermidis biofilms: functional molecules, relation to virulence and vaccine potential. Top. Curr. Chem. 288, 157–182 (2009).
  • Fey PD, Olson ME. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol. 5(6), 917–933 (2010).
  • Thoendel M, Kavanaugh JS, Flack CE, Horswill AR. Peptide signalling in the staphylococci. Chem. Rev. 111, 117–151 (2011).
  • Qin Z, Ou Y, Yang L et al. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153, 2083–2092 (2007).
  • Otto M. Staphylococcus epidermidis – the ‘accidental’ pathogen. Nat. Rev. Microbiol. 7, 555–567 (2009).
  • Holland L, Conlon B, O’Gara JP. Mutation of tagO reveals an essential role for wall teichoic acids in Staphylococcus epidermidis biofilm development. Microbiology 157(2), 408–418 (2011).
  • Heilmann C. Adhesion mechanisms of staphylococci. Adv. Exp. Med. Biol. 715, 105–123 (2011).
  • Vuong C, Kocianova S, Voyich JM et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 52, 54881–54886 (2004).
  • Rohde H, Frankenberger S, Zähringer U, Mack D. Structure, function and contribution of polysaccharide intercellular adhesin (PIA) to Staphylococcus epidermidis biofilm formation and pathogenesis of biomaterial-associated infections. Eur. J. Cell. Biol. 89, 103–111 (2010).
  • Macintosh RL, Brittan JL, Bhattacharya R et al. The terminal A domain of the fibrillar accumulation-associated protein (Aap) of Staphylococcus epidermidis mediates adhesion to human corneocytes. J. Bacteriol. 191, 7007–7016 (2009).
  • Bateman A, Holden MTG, Yeats C. The G5 domain: a potential N-acetylglucosamine recognition domain involved in biofilm formation. Bioinformatics 21, 1301–1303 (2005).
  • Conrady DG, Brescia CC, Horii K, Weiss AA, Hassett DJ, Herr AB. A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc. Natl Acad. Sci. USA 105(49), 19456–19461 (2008).
  • Rohde H, Burdelski C, Bartscht K et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol. 55(6), 1883–1895 (2005).
  • Rohde H, Burandt EC, Siemssen N 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. Biomaterials 28, 1722–1720 (2007).
  • Tormo MA, Knecht E, Götz F, Lasa I, Penadés JR. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology 151, 2465–2475 (2005).
  • Hennig S, Wai SN, Ziebuhr W. Spontaneous switch to PIA-independent biofilm formation in an ica-positive Staphylococcus epidermidis isolate. Int. J. Med. Microbiol. 297, 117–122 (2007).
  • Christner M, Franke GC, Schommer NN et al. The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol. Microbiol. 75(1), 187–207 (2010).
  • Izano EA, Amarante MA, Kher WB, Kaplan JB. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl. Environ. Microbiol. 74(2), 470–476 (2008).
  • Yao Y, Sturdevant DE, 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).
  • Wang R, Khan BA, Cheung GYC et al. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J. Clin. Invest. 121, 238–248 (2011).
  • Zhu T, Lou Q, Wu Y, Hu J, Yu F, Qu D. Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile. BMC Microbiol. 10, 287 (2010).
  • Rani SA, Pitts B, Beyenal H et al. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration with bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189(11), 4223–4233 (2007).
  • Boles BR, Horswill AR. Staphylococcal biofilm disassembly. Trends Microbiol. 19, 449–455 (2011).
  • Kong KF, Vuong C, Otto M. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296, 133–139 (2006).
  • Vuong C, Voyich JM, Fischer ER et al. Polysaccharide intercellular adhesion (PIA) protects Staphylococcus epidermidis against major components of human innate immune system. Cell. Microbiol. 6(3), 269–275 (2004).
  • Guenther F, Stroh P, Wagner C, Obst U, Hänsch GM. Phagocytosis of staphylococci biofilms by polymorphonuclear neutrophils: S. aureus and S. epidermidis differ with regard to their susceptibility towards the host defense. Int. J. Artif. Organs 32(9), 565–573 (2010).
  • Schommer NN, Christner M, Hentschke M, Ruckdeschel K, Aepfelbacher M, Rohde H. Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1. Infect. Immun. 79(6), 2267–2276 (2011).
  • Kocianova S, Vuong C, Yao Y et al. Key role of poly-γ-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J. Clin. Invest. 115(3), 688–694 (2005).
  • Otto M, O’Mahoney DS, Guina T, Klebanoff SJ. Activity of Staphylococcus epidermidis phenol-soluble modulin peptides expressed in Staphylococcus carnosus. J. Infect. Dis. 190, 748–755 (2004).
  • Vuong C, Dürr M, Carmody AB, Peschel A, Klebanoff SJ, Otto M. 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(8), 753–759 (2004).
  • Stevens NT, Sadovskaya I, Jabbouri S et al. Staphylococcus epidermidis polysaccharide intercellular adhesin induces IL-8 expression in human astrocytes via a mechanism involving TLR2. Cell. Microbiol. 11(3), 421–432 (2009).
  • Hirschhausen N, Schlesier T, Schmidt MA, Götz F, Peters G, Heilmann C. A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol. 12(12), 1746–1764 (2010).
  • Li M, Lai Y, Villaruz AE, Cha DJ, Sturdevant DE, Otto M. Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl Acad. Sci. USA 104(22), 9469–9474 (2007).
  • Cogen AL, Yamasaki K, Sanchez KM et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident on the skin. J. Invest. Dermatol. 130, 192–200 (2010).
  • Cheung GYC, Rigby K, Wang R et al. Staphylococcus epidermidis strategies to avoid killing by human neutrophils. PLoS Pathog. 6(10), e1001133 (2010).
  • Cogen AL, Yamasaki K, Muto J et al. Staphylococcus epidermidis antimicrobial δ-toxin (phenol-soluble modulin-γ) cooperates with host antimicrobial peptides to kill group A Streptococcus. PLoS ONE 5(1), e8557 (2010).
  • von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect. Dis. 2, 677–685 (2002).
  • Vuong C, Otto M. Staphylococcus epidermidis infections. Microbes Infect. 4, 481–489 (2002).
  • Ekkelenkamp MB, Hanssen M, Hsu SD et al. Isolation and structural characterization of epilancin 15X, a novel lantibiotic from a clinical strain of Staphylococcus epidermidis. FEBS Lett. 579, 1917–1922 (2005).
  • Projan SJ, Nesin M, Dunman PM. Staphylococcal vaccines and immunotherapy: to dream the impossible dream? Curr. Opin. Pharmacol. 6, 473–479 (2006).
  • Middleton JR. Staphylococcus aureus antigens and challenges in vaccine development. Expert Rev. Vaccines 7(6), 805–815 (2008).
  • García-Lara J, Foster SJ. Anti-Staphylococcus aureus immunotherapy: current status and prospects. Curr. Opin. Pharmacol. 9, 552–557 (2009).
  • Otto M. Novel targeted immunotherapy approaches for staphylococcal infection. Expert Opin. Biol. Ther. 10(7), 1049–1059 (2010).
  • Ohlsen K, Lorenz U. Immunotherapeutic strategies to combat staphylococcal infections. Int. J. Med. Microbiol. 300, 402–410 (2010).
  • Zhang YQ, Ren SX, Li H-L et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49(6), 1577–1593 (2003).
  • Gill SR, Fouts DE, Archer GL et al. Insights on evolution of virulence and resistance from the complete genome analysis from an early methicillin-resistant Staphylococcus aureus strain and a biofim-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187(7), 2426–2438 (2005).
  • Bowden MG, Chen W, Singvall J et al. Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis. Microbiology 151, 1453–1464 (2005).
  • Mora M, Telford JL. Genome-based approaches to vaccine development. J. Mol. Med. 88, 143–147 (2010).
  • Bambini S, Rappuoli R. The use of genomics in microbial vaccine development. Drug Discov. Today 14(5–6), 252–260 (2009).
  • Sellman BR, Howell AP, Kelly-Boyd C, Baker SM. Identification of immunogenic and serum binding proteins of Staphylococcus epidermidis. Infect. Immun. 73(10), 6591–6600 (2005).
  • Meinke A, Henics T, Hanner M, Minh DB, Nagy E. Antigenome technology: a novel approach for the selection of bacterial vaccine candidate antigens. Vaccine 23, 2035–2041 (2005).
  • Pourmand MR, Clarke SR, Schuman RF, Mond JJ, Foster SJ. Identification of antigenic components of Staphylococcus epidermidis expressed during human infection. Infect. Immun. 74(8), 4644–4654 (2006).
  • De Groot AS. Immunomics: discovering new targets for vaccines and therapeutics. Drug Discov. Today 11(5–6), 203–209 (2006).
  • McCrea KW, Hartford O, Davis S. The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis. Microbiology 146, 1535–1546 (2000).
  • Brennan MP, Loughman A, Devocelle M et al. Elucidating the role of Staphylococcus epidermidis serine-aspartate protein G in platelet activation. J. Thromb. Haemost. 7, 1364–1372 (2008).
  • Rennermalm A, Nilsson M, Flock JI. The fibrinogen binding protein of Staphylococcus epidermidis is a target for opsonic antibodies. Infect. Immun. 72, 3081–3083 (2004).
  • Guo B, Zhao X, Shi Y, Zhu D, Zhang Y. Pathogenic implications of a fibrinogen-binding protein of Staphylococcus epidermidis in a rat model of intravascular-catheter-associated infection. Infect. Immun. 75(6), 2991–2995 (2007).
  • Arciola CR, Campoccia D, Gamberini S, Donati ME, Montanaro L. Presence of fibrinogen-binding adhesin gene in Staphylococcus epidermidis isolates from central venous catheters-associated and orthopaedic implant-associated infections. Biomaterials 25, 4825–4829 (2004).
  • Nilsson M, Frykberg L, Flock JI, Pei L, Lindberg M, Guss B. A fibrinogen-binding protein of Staphylococcus epidermidis. Infect. Immun. 66(6), 2666–2673 (1998).
  • Sellman BR, Timofeyeva Y, Nanra J et al. Expression of Staphylococcus epidermidis SdrG increases following exposure to an in vivo environment. Infect. Immun. 76(6), 2950–2957 (2008).
  • Vernachio JH, Bayer AS, Ames B et al. Human immunoglobulin G recognizing fibrinogen-binding surface proteins is protective against both Staphylococcus aureus and Staphylococcus epidermidis infections in vivo. Antimicrob. Agents Chemother. 50(2), 511–518 (2006).
  • Bloom BT. INH-A21: a donor-selected Staphylococcal human immune globulin for the prevention of late-onset neonatal Staphylococcal infection. Expert Opin. Investig. Drugs 15(6), 703–707 (2006).
  • DeJonge M, Burchfield D, Bloom B et al. Clinical trial of safety and efficacy of INH-A21 for the prevention of nosocomial staphylococcal bloodstream infection in premature infants. J. Pediatr. 151, 261–265 (2007).
  • de la Morena MT. Specific immune globulin therapy for prevention of nosocomial staphylococcal bloodstream infection in premature infants: not what we hoped. J. Pediatr. 151, 232–234 (2007).
  • Arrecubieta C, Toba FA, von Bayern M et al. SdrF, a Staphylococcus epidermidis surface protein, contributes to the initation of ventricular assist device driveline-related infections. PLoS Pathog. 5(5), e1000411 (2009).
  • Shahrooei M. Identification of potential targets for vaccination against Staphylococcus epidermidis biofilms. PhD thesis, Medical Sciences, Katholieke Universiteit Leuven, Belgium, 140 (2010).
  • Bowden MG, Visai L, Longshaw CM, Holland KT, Speziale P, Höök M. Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin? J. Biol. Chem. 277(45), 43017–43023 (2002).
  • Rohde H, Kalitzky M, Kröger N et al. Detection of virulence-associated genes not useful for discrimination between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J. Clin. Microbiol. 42(12), 5614–5619 (2004).
  • Frebourg NB, Lefebvre S, Baert S, Lemeland JF. PCR-based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J. Clin. Microbiol. 38(2), 877–880 (2000).
  • Shahrooei M, Hira V, Merckx R, Stijlmans B, Hermans PWM, Van Eldere J. Inhibition of Staphylococcus epidermidis biofilm formation by rabbit polyclonal antibodies against SesC protein. Infect. Immun. 77(9), 3670–3678 (2009).
  • Yao Y, Sturdevant DE, Villaruz A, Xu L, Gao Q, Otto M. Factors characterizing Staphylococcus epidermidis invasiveness determined by comparative genomics. Infect. Immun. 73(3), 1856–1860 (2005).
  • Söderquist B, Andersson M, Nilsson M et al. Staphylococcus epidermidis surface protein I (SesI): a marker of the invasive capacity of S. epidermidis? J. Med. Microbiol. 58, 1395–1397 (2009).
  • Rogers KL, Rupp ME, Fey PD. The presence of icaADBC is detrimental to the colonization of human skin by Staphylococcus epidermidis. Appl. Environ. Microbiol. 74(19), 6155–6157 (2008).
  • Maira-Litrán T, Kropec A, Goldmann DA, Pier GB. Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated staphylococcal poly-N-acetyl-β-(1–6)-glucosamine. Infect. Immun. 73(10), 6752–6762 (2005).
  • Pourmand MR, Abdossamadi Z, Salari MH, Hosseini M. Slime layer formation and the prevalence of mecA and aap genes in Staphylococcus epidermidis isolates. J. Infect. Dev. Ctries 5(1), 34–40 (2011).
  • Sun D, Accavitti MA, Bryers JD. Inhibition of biofilm formation by monoclonal antibodies against Staphylococcus epidermidis RP62A accumulation-associated protein. Clin. Diagn. Lab. Immunol. 12(1), 93–100 (2005).
  • Broekhuizen CAN, de Boer L, Schipper K et al. The influence of antibodies on Staphylococcus epidermidis adherence to polyvinylpyrrolidone-coated silicone elastomer in experimental biomaterial-associated infection in mice. Biomaterials 30, 6444–6450 (2009).
  • Hu J, Xu T, Zhu T et al. Monoclonal antibodies against accumulation-associated protein affect EPS biosynthesis and enhance bacterial accumulation of Staphylococcus epidermidis. PloS One 6(6), e20918 (2011).
  • Lasa I, Penadés JR. Bap: a family of surface proteins involved in biofilm formation. Res. Microbiol. 157, 99–107 (2006).
  • Weisman LE. Antibody for the prevention of neonatal nosocomial staphylococcal infection: a review of the literature. Arch. Pediatr. 14(Suppl. 1), S31–S34 (2007).
  • Weisman LE, Fischer GW, Thackray HM et al. Safety and pharmacokinetics of a chimerized anti-lipoteichoic monoclonal antibody in healthy adults. Int. Immunopharmacol. 9, 639–644 (2009).
  • Weisman LE, Thackray HM, Garcia-Prats JA et al. Phase 1/2 double-blind, placebo-controlled, dose escalation, safety, and pharmacokinetic study of pagibaximab (BSYX-A110), an antistaphylococcal monoclonal antibody for the prevention of staphylococcal bloodstream infections, in very-low-birthweight neonates. Antimicrob. Agents Chemother. 53(7), 2879–2886 (2009).
  • Weisman LE, Thackray HM, Steinhorn RH et al. A randomized study of a monoclonal antibody (pagibaximab) to prevent staphylococcal sepsis. Pediatrics 128(2), 271–279 (2011).
  • Joyce J, Cook J, Chabot D et al. Immunogenicity and protective efficacy of Bacillus anthracis poly-γ-D-glutamic acid capsule covalently coupled to a protein carrier using a novel triazine-based conjugation strategy. J. Biol. Chem. 281(8), 4831–4843 (2006).
  • Lee DY, Chun JH, Ha HJ et al. Poly-gamma-D-glutamic acid and protective antigen conjugate vaccines induce functional antibodies against the protective antigen and capsule of Bacillus anthracis in guinea-pigs and rabbits. FEMS Immunol. Med. Microbiol. 57(2), 165–172 (2009).
  • Skurnik D, Merighi M, Grout M et al. Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J. Clin. Invest. 120(9), 3220–3233 (2010).
  • Mohamed N, Jones SM, Casey LS, Pincus SE, Spitalny GL. Heteropolymers: a novel technology against blood-borne infections. Curr. Opin. Mol. Ther 7(2), 144–150 (2005).

Website

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.