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Staphylococcal Virulence Factors

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Biomaterials Associated Infection

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Abstract

The adherence of staphylococci to the unmodified or host factor-coated surface of a medical device is the first critical event in the establishment of a device-associated infection with these serious pathogens. Staphylococcus aureus in particular harbors a variety of proteinaceous and non-proteinaceous adhesins that mediate attachment to a multitude of host factors, such as extracellular matrix and plasma proteins and platelets, or intercellular adhesins, which are essential for biofilm accumulation. Proteinaceous adhesins may be classified in covalently surface-anchored proteins of the microbial surface components recognizing adhesive matrix molecules family or in proteins that are surface-associated by different means, such as ionic or hydrophobic interactions. Non-covalently surface-associated proteins include the autolysin/adhesins, proteins of the secretable expanded repertoire adhesive molecules family, or membrane-spanning proteins. Non-proteinaceous adhesins include the polysaccharide intercellular adhesin as well as lipoteichoic and wall teichoic acids. The features and functions of surface and surface-associated protein adhesins as well as of non-proteinaceous adhesins are discussed.

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Abbreviations

aa:

Amino acids

CHAP:

Cysteine, histidine-dependent amidohydrolase/peptidase

Clf:

Clumping factor

Cn:

Collagen

Eap:

Extracellular adherence protein

Ebh:

Extracellular matrix-binding protein homologue

ECM:

Extracellular matrix

eDNA:

Extracellular DNA

Efb:

Extracellular fibrinogen-binding protein

Emp:

Extracellular matrix protein-binding protein

Fg:

Fibrinogen

Fn:

Fibronectin

FnBP:

Fibronectin-binding protein

LTA:

Lipoteichoic acid

LysM:

Lysine motif

Map:

MHC class II analogous protein

MSCRAMM:

Microbial surface component recognizing adhesive matrix molecules

PIA:

Polysaccharide intercellular adhesin

PSM:

Phenol-soluble modulin

SERAM:

Secretable expanded repertoire adhesive molecules

TSP:

Thrombospondin

Vn:

Vitronectin

vWf:

Von Willebrand factor

vWbp:

Von Willebrand factor-binding protein

WTA:

Wall teichoic acid

References

  1. Karlowsky JA, Jones ME, Draghi DC, Thornsberry C, Sahm DF, Volturo GA. Prevalence and antimicrobial susceptibilities of bacteria isolated from blood cultures of hospitalized patients in the United States in 2002. Ann Clin Microbiol Antimicrob. 2004;3:7.

    Article  Google Scholar 

  2. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339(8):520–32.

    Article  CAS  Google Scholar 

  3. Ziebuhr W. Staphylococcus aureus and Staphylococcus epidermidis: emerging pathogens in nosocomial infections. Contrib Microbiol. 2001;8:102–7.

    Article  CAS  Google Scholar 

  4. Götz F, Peters G. Colonization of medical devices by coagulase-negative staphylococci. In: Waldvogel FA, Bisno AL, editors. Infections associated with indwelling medical devices. 3rd ed. Washington, DC: ASM; 2000. p. 55–88.

    Google Scholar 

  5. Lentino JR. Prosthetic joint infections: bane of orthopedists, challenge for infectious disease specialists. Clin Infect Dis. 2003;36(9):1157–61.

    Article  Google Scholar 

  6. Peters G, Locci R, Pulverer G. Microbial colonization of prosthetic devices. II. Scanning electron microscopy of naturally infected intravenous catheters. Zentralbl Bakteriol Mikrobiol Hyg B. 1981;173(5):293–9.

    CAS  Google Scholar 

  7. Baldassarri L, Donnelli G, Gelosia A, Voglino MC, Simpson AW, Christensen GD. Purification and characterization of the staphylococcal slime-associated antigen and its occurrence among Staphylococcus epidermidis clinical isolates. Infect Immun. 1996;64(8):3410–5.

    CAS  Google Scholar 

  8. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol. 1996;178(1):175–83.

    CAS  Google Scholar 

  9. Hussain M, Wilcox MH, White PJ. The slime of coagulase-negative staphylococci: biochemistry and relation to adherence. FEMS Microbiol Rev. 1993;10(3–4):191–207.

    CAS  Google Scholar 

  10. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, Smeltzer MS, et al. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A. 2007;104(19):8113–8.

    Article  CAS  Google Scholar 

  11. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22.

    Article  CAS  Google Scholar 

  12. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol. 2001;183(9):2888–96.

    Article  CAS  Google Scholar 

  13. 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. 2002;277(45):43017–23.

    Article  CAS  Google Scholar 

  14. Heilmann C, Hussain M, Peters G, Götz F. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol. 1997;24(5):1013–24.

    Article  CAS  Google Scholar 

  15. Gross M, Cramton SE, Götz F, Peschel A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun. 2001;69:3423–6.

    Article  CAS  Google Scholar 

  16. Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, Biswas R, et al. A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol Microbiol. 2007;65(4):1078–91.

    Article  CAS  Google Scholar 

  17. Herrmann M, Lai QJ, Albrecht RM, Mosher DF, Proctor RA. Adhesion of Staphylococcus aureus to surface-bound platelets: role of fibrinogen/fibrin and platelet integrins. J Infect Dis. 1993;167(2):312–22.

    Article  CAS  Google Scholar 

  18. Herrmann M, Hartleib J, Kehrel B, Montgomery RR, Sixma JJ, Peters G. Interaction of von Willebrand factor with Staphylococcus aureus. J Infect Dis. 1997;176(4):984–91.

    Article  CAS  Google Scholar 

  19. Patti JM, Allen BL, McGavin MJ, Höök M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol. 1994;48:585–617.

    Article  CAS  Google Scholar 

  20. Schneewind O, Mihaylova-Petkov D, Model P. Cell wall sorting signals in surface proteins of gram-positive bacteria. EMBO J. 1993;12(12):4803–11.

    CAS  Google Scholar 

  21. Ton-That H, Liu G, Mazmanian SK, Faull KF, Schneewind O. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc Natl Acad Sci U S A. 1999;96(22):12424–9.

    Article  CAS  Google Scholar 

  22. Mazmanian SK, Liu G, Ton-That H, Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science. 1999;285(5428):760–3.

    Article  CAS  Google Scholar 

  23. Marraffini LA, Schneewind O. Anchor structure of staphylococcal surface proteins. V. Anchor structure of the sortase B substrate IsdC. J Biol Chem. 2005;280(16):16263–71.

    Article  CAS  Google Scholar 

  24. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, 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. 2005;187(7):2426–38.

    Article  CAS  Google Scholar 

  25. Herrmann M, Vaudaux PE, Pittet D, Auckenthaler R, Lew PD, Schumacher-Perdreau F, et al. Fibronectin, fibrinogen, and laminin act as mediators of adherence of clinical staphylococcal isolates to foreign material. J Infect Dis. 1988;158(4):693–701.

    Article  CAS  Google Scholar 

  26. McDevitt D, Francois P, Vaudaux P, Foster TJ. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol. 1994;11(2):237–48.

    Article  CAS  Google Scholar 

  27. Ni Eidhin D, Perkins S, Francois P, Vaudaux P, Höök M, Foster TJ. Clumping factor B (ClfB), a new surface located fibrinogen binding adhesin of Staphylococcus aureus. Mol Microbiol. 1998;30(2):245–57.

    Article  CAS  Google Scholar 

  28. McDevitt D, Francois P, Vaudaux P, Foster TJ. Identification of the ligand-binding domain of the surface-located fibrinogen receptor (clumping factor) of Staphylococcus aureus. Mol Microbiol. 1995;16(5):895–907.

    Article  CAS  Google Scholar 

  29. Hartford OM, Wann ER, Höök M, Foster TJ. Identification of residues in the Staphylococcus aureus fibrinogen-binding MSCRAMM clumping factor A (ClfA) that are important for ligand binding. J Biol Chem. 2001;276(4):2466–73.

    Article  CAS  Google Scholar 

  30. McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, et al. Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem. 1997;247(1):416–24.

    Article  CAS  Google Scholar 

  31. Siboo IR, Cheung AL, Bayer AS, Sullam PM. Clumping factor a mediates binding of Staphylococcus aureus to human platelets. Infect Immun. 2001;69(5):3120–7.

    Article  CAS  Google Scholar 

  32. O’Brien L, Kerrigan SW, Kaw G, Hogan M, Penades J, Litt D, et al. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol. 2002;44(4):1033–44.

    Article  Google Scholar 

  33. Loughman A, Fitzgerald JR, Brennan MP, Higgins J, Downer R, Cox D, et al. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol. 2005;57(3):804–18.

    Article  CAS  Google Scholar 

  34. Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ. Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect Immun. 2007;75(7):3335–43.

    Article  CAS  Google Scholar 

  35. O’Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol. 2002;4(11):759–70.

    Article  Google Scholar 

  36. O’Connell DP, Nanavaty T, McDevitt D, Gurusiddappa S, Höök M, Foster TJ. The fibrinogen-binding MSCRAMM (clumping factor) of Staphylococcus aureus has a Ca2+−dependent inhibitory site. J Biol Chem. 1998;273(12):6821–9.

    Article  Google Scholar 

  37. Deivanayagam CC, Wann ER, Chen W, Carson M, Rajashankar KR, Höök M, et al. A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J. 2002;21 (24):6660–72.

    Article  CAS  Google Scholar 

  38. Que YA, Francois P, Haefliger J-A, Entenza J-M, Vaudaux P, Moreillon P. Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect Immun. 2001;69(10):6296–302.

    Article  CAS  Google Scholar 

  39. Sullam PM, Bayer AS, Foss WM, Cheung AL. Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect Immun. 1996;64(12):4915–21.

    CAS  Google Scholar 

  40. Josefsson E, Hartford O, O’Brien L, Patti JM, Foster T. Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis. 2001;184(12):1572–80.

    Article  CAS  Google Scholar 

  41. Hall AE, Domanski PJ, Patel PR, Vernachio JH, Syribeys PJ, Gorovits EL, et al. Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect Immun. 2003;71(12):6864–70.

    Article  CAS  Google Scholar 

  42. Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, et al. A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog. 2008;4(11):e1000226.

    Article  CAS  Google Scholar 

  43. Josefsson E, McCrea KW, Ni Eidhin D, O’Connell D, Cox J, Hook M, et al. Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology. 1998;144(Pt 12):3387–95.

    Article  CAS  Google Scholar 

  44. Savolainen K, Paulin L, Westerlund-Wikstrom B, Foster TJ, Korhonen TK, Kuusela P. Expression of pls, a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus, prevents bacterial adhesion in vitro. Infect Immun. 2001;69(5):3013–20.

    Article  CAS  Google Scholar 

  45. Corrigan RM, Miajlovic H, Foster TJ. Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol. 2009;9:22.

    Article  CAS  Google Scholar 

  46. Barbu EM, Ganesh VK, Gurusiddappa S, Mackenzie RC, Foster TJ, Sudhof TC, et al. Beta-Neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog. 2010;6(1):e1000726.

    Article  CAS  Google Scholar 

  47. Huesca M, Peralta R, Sauder DN, Simor AE, McGavin MJ. Adhesion and virulence properties of epidemic Canadian methicillin-resistant Staphylococcus aureus strain 1: identification of novel adhesion functions associated with plasmin-sensitive surface protein. J Infect Dis. 2002;185(9):1285–96.

    Article  Google Scholar 

  48. Roche FM, Meehan M, Foster TJ. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology. 2003;149(Pt 10):2759–67.

    Article  CAS  Google Scholar 

  49. Hussain M, Schafer D, Juuti KM, Peters G, Haslinger-Löffler B, Kuusela PI, et al. Expression of Pls (plasmin sensitive) in Staphylococcus aureus negative for pls reduces adherence and cellular invasion and acts by steric hindrance. J Infect Dis. 2009;200(1):107–17.

    Article  CAS  Google Scholar 

  50. Josefsson E, Juuti K, Bokarewa M, Kuusela P. The surface protein Pls of methicillin-resistant Staphylococcus aureus is a virulence factor in septic arthritis. Infect Immun. 2005;73 (5):2812–7.

    Article  CAS  Google Scholar 

  51. Tung H, Guss B, Hellman U, Persson L, Rubin K, Ryden C. A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem J. 2000;345(Pt 3):611–9.

    Article  CAS  Google Scholar 

  52. McCrea KW, Hartford O, Davis S, Eidhin DN, Lina G, Speziale P, et al. The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis. Microbiology. 2000;46(Pt 7):1535–46.

    Google Scholar 

  53. Ponnuraj K, Bowden MG, Davis S, Gurusiddappa S, Moore D, Choe D, et al. A “dock, lock, and latch” structural model for a staphylococcal adhesin binding to fibrinogen. Cell. 2003;115(2):217–28.

    Article  CAS  Google Scholar 

  54. Signas C, Raucci G, Jönsson K, Lindgren PE, Anantharamaiah GM, Höök M, et al. Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci U S A. 1989;86(2):699–703.

    Article  CAS  Google Scholar 

  55. Jönsson K, Signas C, Müller HP, Lindberg M. Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem. 1991;202(3):1041–8.

    Article  Google Scholar 

  56. Greene C, McDevitt D, Francois P, Vaudaux PE, Lew DP, Foster TJ. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol Microbiol. 1995;17(6):1143–52.

    Article  CAS  Google Scholar 

  57. Wann ER, Gurusiddappa S, Höök M. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem. 2000;275(18):13863–71.

    Article  CAS  Google Scholar 

  58. Roche FM, Downer R, Keane F, Speziale P, Park PW, Foster TJ. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J Biol Chem. 2004;279(37):38433–40.

    Article  CAS  Google Scholar 

  59. Keane FM, Loughman A, Valtulina V, Brennan M, Speziale P, Foster TJ. Fibrinogen and elastin bind to the same region within the A domain of fibronectin binding protein A, an MSCRAMM of Staphylococcus aureus. Mol Microbiol. 2007;63(3):711–23.

    Article  CAS  Google Scholar 

  60. Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, et al. Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature. 2003;423:177–81.

    Article  CAS  Google Scholar 

  61. Pilka ES, Werner JM, Schwarz-Linek U, Pickford AR, Meenan NA, Campbell ID, et al. Structural insight into binding of Staphylococcus aureus to human fibronectin. FEBS Lett. 2006;580(1):273–7.

    Article  CAS  Google Scholar 

  62. Peacock SJ, Day NP, Thomas MG, Berendt AR, Foster TJ. Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J Infect. 2000;41(1):23–31.

    Article  CAS  Google Scholar 

  63. Frees D, Chastanet A, Qazi S, Sorensen K, Hill P, Msadek T, et al. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol. 2004;54(5):1445–62.

    Article  CAS  Google Scholar 

  64. Sinha B, Francois PP, Nüsse O, Foti M, Hartford OM, Vaudaux P, et al. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol. 1999;1(2):101–17.

    Article  CAS  Google Scholar 

  65. Dziewanowska K, Patti JM, Deobald CF, Bayles KW, Trumble WR, Bohach GA. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect Immun. 1999;67(9):4673–8.

    CAS  Google Scholar 

  66. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, Höök M. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol. 2000;79(10):672–9.

    Article  CAS  Google Scholar 

  67. Dziewanowska K, Carson AR, Patti JM, Deobald CF, Bayles KW, Bohach GA. Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells. Infect Immun. 2000;68(11):6321–8.

    Article  CAS  Google Scholar 

  68. Grundmeier M, Hussain M, Becker P, Heilmann C, Peters G, Sinha B. Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect Immun. 2004;72(12):7155–63.

    Article  CAS  Google Scholar 

  69. Flock JI, Hienz SA, Heimdahl A, Schennings T. Reconsideration of the role of fibronectin binding in endocarditis caused by Staphylococcus aureus. Infect Immun. 1996;64(5):1876–8.

    CAS  Google Scholar 

  70. Palmqvist N, Foster T, Fitzgerald JR, Josefsson E, Tarkowski A. Fibronectin-binding proteins and fibrinogen-binding clumping factors play distinct roles in staphylococcal arthritis and systemic inflammation. J Infect Dis. 2005;191(5):791–8.

    Article  CAS  Google Scholar 

  71. McElroy MC, Cain DJ, Tyrrell C, Foster TJ, Haslett C. Increased virulence of a fibronectin-binding protein mutant of Staphylococcus aureus in a rat model of pneumonia. Infect Immun. 2002;70(7):3865–73.

    Article  CAS  Google Scholar 

  72. Kerdudou S, Laschke MW, Sinha B, Preissner KT, Menger MD, Herrmann M. Fibronectin binding proteins contribute to the adherence of Staphylococcus aureus to intact endothelium in vivo. Thromb Haemost. 2006;96(2):183–9.

    CAS  Google Scholar 

  73. Heilmann C, Niemann S, Sinha B, Herrmann M, Kehrel BE, Peters G. Staphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB. J Infect Dis. 2004;190(2):321–9.

    Article  CAS  Google Scholar 

  74. Fitzgerald JR, Loughman A, Keane F, Brennan M, Knobel M, Higgins J, et al. Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgammaRIIa receptor. Mol Microbiol. 2006;59(1):212–30.

    Article  CAS  Google Scholar 

  75. Edwards AM, Potts JR, Josefsson E, Massey RC. Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog. 2010;6(6):e1000964.

    Article  CAS  Google Scholar 

  76. Patti JM, House-Pompeo K, Boles JO, Garza N, Gurusiddappa S, Höök M. Critical residues in the ligand-binding site of the Staphylococcus aureus collagen-binding adhesin (MSCRAMM). J Biol Chem. 1995;270(20):12005–11.

    Article  CAS  Google Scholar 

  77. Zong Y, Xu Y, Liang X, Keene DR, Höök A, Gurusiddappa S, et al. A ‘Collagen Hug’ model for Staphylococcus aureus CNA binding to collagen. EMBO J. 2005;24(24):4224–36.

    Article  CAS  Google Scholar 

  78. Rhem MN, Lech EM, Patti JM, McDevitt D, Höök M, Jones DB, et al. The collagen-binding adhesin is a virulence factor in Staphylococcus aureus keratitis. Infect Immun. 2000; 68(6):3776–9.

    Article  CAS  Google Scholar 

  79. Siboo IR, Chambers HF, Sullam PM. Role of SraP, a Serine-Rich Surface Protein of Staphylococcus aureus, in binding to human platelets. Infect Immun. 2005;73(4): 2273–80.

    Article  CAS  Google Scholar 

  80. Siboo IR, Chaffin DO, Rubens CE, Sullam PM. Characterization of the accessory Sec system of Staphylococcus aureus. J Bacteriol. 2008;190(18):6188–96.

    Article  CAS  Google Scholar 

  81. Uhlen M, Guss B, Nilsson B, Gatenbeck S, Philipson L, Lindberg M. Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. J Biol Chem. 1984;259(3):1695–702.

    CAS  Google Scholar 

  82. Deisenhofer J. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-A resolution. Biochemistry. 1981;20(9):2361–70.

    Article  CAS  Google Scholar 

  83. Gouda H, Shiraishi M, Takahashi H, Kato K, Torigoe H, Arata Y, et al. NMR study of the interaction between the B domain of staphylococcal protein A and the Fc portion of immunoglobulin G. Biochemistry. 1998;37(1):129–36.

    Article  CAS  Google Scholar 

  84. Hartleib J, Kohler N, Dickinson RB, Chhatwal GS, Sixma JJ, Hartford OM, et al. Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood. 2000;96(6):2149–56.

    CAS  Google Scholar 

  85. Nguyen T, Ghebrehiwet B, Peerschke EIB. Staphylococcus aureus Protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect Immun. 2000;68:2061–8.

    Article  CAS  Google Scholar 

  86. Gomez MI, Lee A, Reddy B, Muir A, Soong G, Pitt A, et al. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med. 2004;10(8):842–8.

    Article  CAS  Google Scholar 

  87. Dryla A, Gelbmann D, von Gabain A, Nagy E. Identification of a novel iron regulated staphylococcal surface protein with haptoglobin-haemoglobin binding activity. Mol Microbiol. 2003;49(1):37–53.

    Article  CAS  Google Scholar 

  88. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, et al. Passage of heme-iron across the envelope of Staphylococcus aureus. Science. 2003;99(5608):906–9.

    Article  CAS  Google Scholar 

  89. Clarke SR, Wiltshire MD, Foster SJ. IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol. 2004;51(5):1509–19.

    Article  CAS  Google Scholar 

  90. Clarke SR, Andre G, Walsh EJ, Dufrene YF, Foster TJ, Foster SJ. Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect Immun. 2009;77(6):2408–16.

    Article  CAS  Google Scholar 

  91. Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, et al. Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis. 2006;193(8):1098–108.

    Article  CAS  Google Scholar 

  92. Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ. Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology. 2010;156(Pt 3):920–8.

    Article  CAS  Google Scholar 

  93. Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, et al. A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun. 2006;74(4):2215–23.

    Article  CAS  Google Scholar 

  94. Hell W, Meyer HG, Gatermann SG. Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol Microbiol. 1998;29(3):871–81.

    Article  CAS  Google Scholar 

  95. Rupp ME, Fey PD, 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. 2001;183(7):1038–42.

    Article  CAS  Google Scholar 

  96. Biswas R, Voggu L, Simon UK, Hentschel P, Thumm G, Götz F. Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett. 2006;259(2):260–8.

    Article  CAS  Google Scholar 

  97. 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. 2010;12:1746–64.

    Article  CAS  Google Scholar 

  98. Zoll S, Patzold B, Schlag M, Götz F, Kalbacher H, Stehle T. Structural basis of cell wall cleavage by a staphylococcal autolysin. PLoS Pathog. 2010;6(3):e1000807.

    Article  CAS  Google Scholar 

  99. Braun L, Ohayon H, Cossart P. The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol. 1998;27(5):1077–87.

    Article  CAS  Google Scholar 

  100. Milohanic E, Jonquieres R, Cossart P, Berche P, Gaillard J-L. The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol Microbiol. 2001;39:1212–24.

    Article  CAS  Google Scholar 

  101. Multhoff G. Heat shock protein 70 (Hsp70): membrane location, export and immunological relevance. Methods. 2007;43(3):229–37.

    Article  CAS  Google Scholar 

  102. Allignet J, Aubert S, Dyke KG, El Solh N. Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect Immun. 2001;69(2):712–8.

    Article  CAS  Google Scholar 

  103. Meyer HG, Wengler-Becker U, Gatermann SG. The hemagglutinin of Staphylococcus saprophyticus is a major adhesin for uroepithelial cells. Infect Immun. 1996;64(9):3893–6.

    CAS  Google Scholar 

  104. Heilmann C, Hartleib J, Hussain M, Peters G. The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun. 2005;73(8):4793–802.

    Article  CAS  Google Scholar 

  105. Heilmann C, Thumm G, Chhatwal GS, Hartleib J, Uekötter A, Peters G. Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology. 2003;149:2769–78.

    Article  CAS  Google Scholar 

  106. Bateman A, Rawlings ND. The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci. 2003;28(5):234–7.

    Article  CAS  Google Scholar 

  107. Buist G, Steen A, Kok J, Kuipers OP. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol. 2008;68(4):838–47.

    Article  CAS  Google Scholar 

  108. Chavakis T, Wiechmann K, Preissner KT, Herrmann M. Staphylococcus aureus interactions with the endothelium: the role of bacterial “secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems. Thromb Haemost. 2005;94(2):278–85.

    CAS  Google Scholar 

  109. Hussain M, Becker K, von Eiff C, Schrenzel J, Peters G, Herrmann M. Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J Bacteriol. 2001;183(23):6778–86.

    Article  CAS  Google Scholar 

  110. McGavin MH, Krajewska-Pietrasik D, Ryden C, Höök M. Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect Immun. 1993;61(6):2479–85.

    CAS  Google Scholar 

  111. Jönsson K, McDevitt D, McGavin MH, Patti JM, Höök M. Staphylococcus aureus expresses a major histocompatibility complex class II analog. J Biol Chem. 1995;270(37):21457–60.

    Article  Google Scholar 

  112. Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, Flock JI, et al. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med. 2002;8(7):687–93.

    Article  CAS  Google Scholar 

  113. Sobke AC, Selimovic D, Orlova V, Hassan M, Chavakis T, Athanasopoulos AN, et al. The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J. 2006;20(14):2621–3.

    Article  CAS  Google Scholar 

  114. Hussain M, von Eiff C, Sinha B, Joost I, Herrmann M, Peters G, et al. eap Gene as novel target for specific identification of Staphylococcus aureus. J Clin Microbiol. 2008;46(2):470–6.

    Article  CAS  Google Scholar 

  115. Clarke SR, Harris LG, Richards RG, Foster SJ. Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect Immun. 2002; 70(12):6680–7.

    Article  CAS  Google Scholar 

  116. Williams RJ, Henderson B, Sharp LJ, Nair SP. Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect Immun. 2002;70(12):6805–10.

    Article  CAS  Google Scholar 

  117. Kuroda M, Tanaka Y, Aoki R, Shu D, Tsumoto K, Ohta T. Staphylococcus aureus giant protein Ebh is involved in tolerance to transient hyperosmotic pressure. Biochem Biophys Res Commun. 2008;374(2):237–41.

    Article  CAS  Google Scholar 

  118. Downer R, Roche F, Park PW, Mecham RP, Foster TJ. The elastin-binding protein of Staphylococcus aureus (EbpS) is expressed at the cell surface as an integral membrane protein and not as a cell wall-associated protein. J Biol Chem. 2002;277(1):243–50.

    Article  CAS  Google Scholar 

  119. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med. 2004;10(3):243–5.

    Article  CAS  Google Scholar 

  120. Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, Yeaman MR, et al. 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. 2005;191(10):1771–7.

    Article  CAS  Google Scholar 

  121. Hussain M, Heilmann C, Peters G, Herrmann M. Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin. Microb Pathog. 2001;31(6):261–70.

    Article  CAS  Google Scholar 

  122. 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. 1997;65(2):519–24.

    CAS  Google Scholar 

  123. Corrigan RM, Rigby D, Handley P, Foster TJ. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology. 2007;153(Pt 8):2435–46.

    Article  CAS  Google Scholar 

  124. Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F, Horstkotte MA, et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol. 2005;55(6):1883–95.

    Article  CAS  Google Scholar 

  125. 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 U S A. 2008;105(49):19456–61.

    Article  CAS  Google Scholar 

  126. Sun D, Accavitti MA, Bryers JD. Inhibition of biofilm formation by monoclonal antibodies against Staphylococcus epidermidis RP62A accumulation-associated protein. Clin Diagn Lab Immunol. 2005;12(1):93–100.

    CAS  Google Scholar 

  127. Geoghegan JA, Corrigan RM, Gruszka DT, Speziale P, O’Gara JP, Potts JR, et al. Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol. 2010;192: 5663–73.

    Article  CAS  Google Scholar 

  128. Banner MA, Cunniffe JG, Macintosh RL, Foster TJ, Rohde H, Mack D, et al. Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J Bacteriol. 2007;189(7):2793–804.

    Article  CAS  Google Scholar 

  129. Cucarella C, Tormo MA, Knecht E, Amorena B, Lasa I, Foster TJ, et al. Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infect Immun. 2002;70(6):3180–6.

    Article  Google Scholar 

  130. Schroeder K, Jularic M, Horsburgh SM, Hirschhausen N, Neumann C, Bertling A, et al. Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation. PLoS One. 2009;4(10):e7567.

    Article  CAS  Google Scholar 

  131. Merino N, Toledo-Arana A, Vergara-Irigaray M, Valle J, Solano C, Calvo E, et al. Protein A-mediated multicellular behavior in Staphylococcus aureus. J Bacteriol. 2009;191(3):832–43.

    Article  CAS  Google Scholar 

  132. O’Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A, et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol. 2008;190(11):3835–50.

    Article  CAS  Google Scholar 

  133. Vergara-Irigaray M, Valle J, Merino N, Latasa C, Garcia B, de Ruiz Los Mozos I, et al. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun. 2009;77(9):3978–91.

    Article  CAS  Google Scholar 

  134. Christner M, Franke G, Schommer N, Wendt U, Wegert K, Pehle P, et al. The giant extracellular matrix binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol. 2010;75(1):187–207.

    Article  CAS  Google Scholar 

  135. Mack D, Nedelmann M, Krokotsch A, Schwarzkopf A, Heesemann J, Laufs R. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun. 1994;62(8):3244–53.

    CAS  Google Scholar 

  136. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol. 1996;20(5):1083–91.

    Article  CAS  Google Scholar 

  137. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 1999;67(10):5427–33.

    CAS  Google Scholar 

  138. Maira-Litran T, Kropec A, Abeygunawardana C, Joyce J, Mark G, Goldmann DA, et al. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun. 2002;70(8):4433–40.

    Article  CAS  Google Scholar 

  139. Kaplan JB, Velliyagounder K, Ragunath C, Rohde H, Mack D, Knobloch JK, et al. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol. 2004;186(24): 8213–20.

    Article  CAS  Google Scholar 

  140. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Götz F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem. 1998;273(29):18586–93.

    Article  CAS  Google Scholar 

  141. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem. 2004;279(52):54881–6.

    Article  CAS  Google Scholar 

  142. Rupp ME, Ulphani JS, Fey PD, 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. 1999;67(5):2627–32.

    CAS  Google Scholar 

  143. Kristian SA, Golda T, Ferracin F, Cramton SE, Neumeister B, Peschel A, et al. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb Pathog. 2004;36(5):237–45.

    Article  CAS  Google Scholar 

  144. Ziebuhr W, Heilmann C, Götz F, Meyer P, Wilms K, Straube E, et al. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun. 1997;65(3):890–6.

    CAS  Google Scholar 

  145. Hall-Stoodley L, Nistico L, Sambanthamoorthy K, Dice B, Nguyen D, Mershon WJ, et al. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol. 2008;8:173.

    Article  CAS  Google Scholar 

  146. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, et al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol. 2006;59(4):1114–28.

    Article  CAS  Google Scholar 

  147. Thomas VC, Thurlow LR, Boyle D, Hancock LE. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol. 2008;190(16):5690–8.

    Article  CAS  Google Scholar 

  148. Itoh Y, Wang X, Hinnebusch BJ, Preston 3rd JF, Romeo T. Depolymerization of beta-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol. 2005; 187(1):382–7.

    Article  CAS  Google Scholar 

  149. 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. 2008;74(2):470–6.

    Article  CAS  Google Scholar 

  150. 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. 2006;255(1):11–6.

    Article  CAS  Google Scholar 

  151. Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster S, 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. 2007;28(9):1711–20.

    Article  CAS  Google Scholar 

  152. Chaignon P, Sadovskaya I, Ragunah C, Ramasubbu N, Kaplan JB, Jabbouri S. Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl Microbiol Biotechnol. 2007;75(1):125–32.

    Article  CAS  Google Scholar 

  153. Boles BR, Horswill AR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 2008;4(4):e1000052.

    Article  CAS  Google Scholar 

  154. Mehlin C, Headley CM, Klebanoff SJ. An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J Exp Med. 1999;189(6):907–18.

    Article  CAS  Google Scholar 

  155. Novick RP. Staphylococcal pathogenesis and pathogenicity factors: genetics and regulation. In: Fischetti VA, Ferretti JJ, Portnoy DA, Rood JI, Novick RP, editors. Gram-positive pathogens. 2nd ed. Washington: ASM Press; 2006. p. 496–516.

    Google Scholar 

  156. Vuong C, Saenz HL, Götz F, Otto M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J Infect Dis. 2000;182(6):1688–93.

    Article  CAS  Google Scholar 

  157. Otto M. Staphylococcal biofilms. Curr Top Microbiol Immunol. 2008;322:207–28.

    Article  CAS  Google Scholar 

  158. Otto M, O’Mahoney DS, Guina T, Klebanoff SJ. Activity of Staphylococcus epidermidis phenol-soluble modulin peptides expressed in Staphylococcus carnosus. J Infect Dis. 2004;190(4):748–55.

    Article  CAS  Google Scholar 

  159. 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. 2005;191(2):289–98.

    Article  CAS  Google Scholar 

  160. Patti JM, Jonsson H, Guss B, Switalski LM, Wiberg K, Lindberg M, et al. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesin. J Biol Chem. 1992;267(7):4766–72.

    CAS  Google Scholar 

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Authors and Affiliations

  1. The Interdisciplinary Center for Clinical Research (IZKF), Institute for Medical Microbiology, Münster University Hospital of Münster, Domagkstraße 10, Münster, 48149, Germany

    Christine Heilmann

  2. Department of Microbial Genetics, Faculty of Biology, University of Tübingen, Waldhäuser Straße 70/8, Tübingen, 72076, Germany

    Friedrich Götz

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    T. Fintan Moriarty

  2. , Medical Microbiology, Academic Medical Center, Meibergdreef 15, Amsterdam, 1105 AZ, Netherlands

    Sebastian A.J. Zaat

  3. University Medical Center Groningen, A. Deusinglaan 1, Groningen, 9713 AV, Netherlands

    Henk J. Busscher

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Heilmann, C., Götz, F. (2013). Staphylococcal Virulence Factors. In: Moriarty, T., Zaat, S., Busscher, H. (eds) Biomaterials Associated Infection. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1031-7_3

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