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Adhesion Mechanisms of Staphylococci

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Bacterial Adhesion

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 715))

Abstract

Staphylococcal adherence to an either biotic or abiotic surface is the critical first event in the establishment of an infection with these serious pathogens. Especially Staphylococcus aureus harbours 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 human host cells, or intercellular adhesion, which is essential for biofilm accumulation. Proteinaceous adhesins may be classified in covalently surface-anchored proteins of the MSCRAMM (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 SERAM (secretable expanded repertoire adhesive molecules) family, or membrane-spanning proteins. Non-proteinaceous adhesins comprise the polysaccharide PIA (polysaccharide intercellular adhesin) and wall teichoic and lipoteichoic 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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References

  • Barbu EM, Ganesh VK, Gurusiddappa S, Mackenzie RC, Foster TJ, Sudhof TC, Höök M (2010) β-Neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog 6:e1000726

    Article  PubMed  Google Scholar 

  • Biswas R, Voggu L, Simon UK, Hentschel P, Thumm G, Götz F (2006) Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259:260–268

    Article  PubMed  CAS  Google Scholar 

  • Chavakis T, Wiechmann K, Preissner KT, Herrmann M (2005) Staphylococcus aureus interactions with the endothelium: the role of bacterial “secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems. Thromb Haemost 94:278–285

    PubMed  CAS  Google Scholar 

  • Christner M, Franke G, Schommer N, Wendt U, Wegert K, Pehle P, Kroll G, Schulze C, Buck F, Mack D, Aepfelbacher M, Rohde H (2010) The giant extracellular matrix binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol 75:187–207

    Article  PubMed  CAS  Google Scholar 

  • Clarke SR, Andre G, Walsh EJ, Dufrene YF, Foster TJ, Foster SJ (2009) Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect Immun 77:2408–2416

    Article  PubMed  CAS  Google Scholar 

  • Clarke SR, Foster SJ (2006) Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 51:187–224

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Corrigan RM, Rigby D, Handley P, Foster TJ (2007) The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153:2435–2446

    Article  PubMed  CAS  Google Scholar 

  • Cucarella C, Tormo MA, Knecht E, Amorena B, Lasa I, Foster TJ, Penadés JR (2002) Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infect Immun 70:3180–3186

    Article  PubMed  Google Scholar 

  • Deivanayagam CC, Wann ER, Chen W, Carson M, Rajashankar KR, Höök M, Narayana SV (2002) 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 21:6660–6672

    Article  PubMed  CAS  Google Scholar 

  • Downer R, Roche F, Park PW, Mecham RP, Foster TJ (2002) 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 277:243–250

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, Biswas R, Henseler K, Götz F, Zähringer U, Peschel A (2007) A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol Microbiol 65:1078–1091

    Article  PubMed  CAS  Google Scholar 

  • Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Höök M (2008) A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog 4:e1000226

    Article  PubMed  Google Scholar 

  • Geoghegan JA, Corrigan RM, Gruszka DT, Speziale P, O’Gara JP, Potts JR, Foster TJ (2010) The role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol 192:5663–5673

    Google Scholar 

  • Gomez MI, Lee A, Reddy B, Muir A, Soong G, Pitt A, Cheung A, Prince A (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10:842–848

    Article  PubMed  CAS  Google Scholar 

  • Götz F (2002) Staphylococcus and biofilms. Mol Microbiol 43:1367–1378

    Article  PubMed  Google Scholar 

  • Greene C, McDevitt D, Francois P, Vaudaux PE, Lew DP, Foster TJ (1995) Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol Microbiol 17:1143–1152

    Article  PubMed  CAS  Google Scholar 

  • Hartford OM, Wann ER, Höök M, Foster TJ (2001) Identification of residues in the Staphylococcus aureus fibrinogen-binding MSCRAMM clumping factor A (ClfA) that are important for ligand binding. J Biol Chem 276:2466–2473

    Article  PubMed  CAS  Google Scholar 

  • Heilmann C, Götz F (2010) Cell-cell communication and biofilm formation in gram-positive bacteria. In: Krämer R, Jung K (eds) Bacterial signaling. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 7–17

    Google Scholar 

  • Heilmann C, Hartleib J, Hussain M, Peters G (2005) The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun 73:4793–4802

    Article  PubMed  CAS  Google Scholar 

  • Hirschhausen N, Schlesier T, Schmidt MA, Götz F, Peters G, Heilmann C (2010) A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 12:1746–1764

    Article  PubMed  CAS  Google Scholar 

  • Huesca M, Peralta R, Sauder DN, Simor AE, McGavin MJ (2002) 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 185:1285–1296

    Article  PubMed  Google Scholar 

  • Hussain M, Heilmann C, Peters G, Herrmann M (2001) Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin. Microb Pathog 31:261–270

    Article  PubMed  CAS  Google Scholar 

  • Hussain M, Schafer D, Juuti KM, Peters G, Haslinger-Löffler B, Kuusela PI, Sinha B (2009) Expression of Pls (plasmin sensitive) in Staphylococcus aureus negative for pls reduces adherence and cellular invasion and acts by steric hindrance. J Infect Dis 200:107–117

    Article  PubMed  CAS  Google Scholar 

  • Jönsson K, Signas C, Müller HP, Lindberg M (1991) Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202:1041–1048

    Article  PubMed  Google Scholar 

  • Kristian SA, Golda T, Ferracin F, Cramton SE, Neumeister B, Peschel A, Götz F, Landmann R (2004) The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb Pathog 36:237–245

    Article  PubMed  CAS  Google Scholar 

  • Lentino JR (2003) Prosthetic joint infections: bane of orthopedists, challenge for infectious disease specialists. Clin Infect Dis 36:1157–1161

    Article  PubMed  Google Scholar 

  • Loughman A, Fitzgerald JR, Brennan MP, Higgins J, Downer R, Cox D, Foster TJ (2005) Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol 57:804–818

    Article  PubMed  CAS  Google Scholar 

  • Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM, Schneewind O (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–909

    Article  PubMed  CAS  Google Scholar 

  • McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, Foster T, Höök M (1997) Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem 247:416–424

    Article  PubMed  CAS  Google Scholar 

  • Merino N, Toledo-Arana A, Vergara-Irigaray M, Valle J, Solano C, Calvo E, Lopez JA, Foster TJ, Penadés JR, Lasa I (2009) Protein A-mediated multicellular behavior in Staphylococcus aureus. J Bacteriol 191:832–843

    Article  PubMed  CAS  Google Scholar 

  • Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ (2007) Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect Immun 75:3335–3343

    Article  PubMed  CAS  Google Scholar 

  • Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ (2010) Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156:920–928

    Article  PubMed  CAS  Google Scholar 

  • Nguyen T, Ghebrehiwet B, Peerschke EIB (2000) Staphylococcus aureus Protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect Immun 68:2061–2068

    Article  PubMed  CAS  Google Scholar 

  • Ni Eidhin D, Perkins S, Francois P, Vaudaux P, Höök M, Foster TJ (1998) Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol Microbiol 30:245–257

    Article  PubMed  CAS  Google Scholar 

  • O’Brien L, Kerrigan SW, Kaw G, Hogan M, Penadés J, Litt D, Fitzgerald DJ, Foster TJ, Cox D (2002a) 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 44:1033–1044

    Article  PubMed  Google Scholar 

  • O’Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ (2002b) Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol 4:759–770

    Article  PubMed  Google Scholar 

  • O’Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A, Foster TJ, O’Gara JP (2008) A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol 190:3835–3850

    Article  PubMed  Google Scholar 

  • Patti JM, House-Pompeo K, Boles JO, Garza N, Gurusiddappa S, Höök M (1995) Critical residues in the ligand-binding site of the Staphylococcus aureus collagen-binding adhesin (MSCRAMM. J Biol Chem 270:12005–12011

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rhem MN, Lech EM, Patti JM, McDevitt D, Höök M, Jones DB, Wilhelmus KR (2000) The collagen-binding adhesin is a virulence factor in Staphylococcus aureus keratitis. Infect Immun 68:3776–3779

    Article  PubMed  CAS  Google Scholar 

  • Roche FM, Downer R, Keane F, Speziale P, Park PW, Foster TJ (2004) The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J Biol Chem 279:38433–38440

    Article  PubMed  CAS  Google Scholar 

  • Roche FM, Massey R, Peacock SJ, Day NP, Visai L, Speziale P, Lam A, Pallen M, Foster TJ (2003a) Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 149:643–654

    Article  PubMed  CAS  Google Scholar 

  • Roche FM, Meehan M, Foster TJ (2003b) The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149:2759–2767

    Article  PubMed  CAS  Google Scholar 

  • Schneewind O, Mihaylova-Petkov D, Model P (1993) Cell wall sorting signals in surface proteins of gram-positive bacteria. EMBO J 12:4803–4811

    PubMed  CAS  Google Scholar 

  • Schroeder K, Jularic M, Horsburgh SM, Hirschhausen N, Neumann C, Bertling A, Schulte A, Foster S, Kehrel BE, Peters G, Heilmann C (2009) Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation. PLoS One 4:e7567

    Article  PubMed  Google Scholar 

  • Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Höök M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem β-zipper. Nature 423:177–181

    Article  PubMed  CAS  Google Scholar 

  • Siboo IR, Chaffin DO, Rubens CE, Sullam PM (2008) Characterization of the accessory Sec system of Staphylococcus aureus. J Bacteriol 190:6188–6196

    Article  PubMed  CAS  Google Scholar 

  • Siboo IR, Cheung AL, Bayer AS, Sullam PM (2001) Clumping Factor A Mediates Binding of Staphylococcus aureus to Human Platelets. Infect Immun 69:3120–3127

    Article  PubMed  CAS  Google Scholar 

  • Signas C, Raucci G, Jönsson K, Lindgren PE, Anantharamaiah GM, Höök M, Lindberg M (1989) 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 USA 86:699–703

    Article  PubMed  CAS  Google Scholar 

  • Sobke AC, Selimovic D, Orlova V, Hassan M, Chavakis T, Athanasopoulos AN, Schubert U, Hussain M, Thiel G, Preissner KT, Herrmann M (2006) The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J 20:2621–2623

    Article  PubMed  CAS  Google Scholar 

  • Tung H, Guss B, Hellman U, Persson L, Rubin K, Ryden C (2000) A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem J 345(Pt 3):611–619

    Article  PubMed  CAS  Google Scholar 

  • Vergara-Irigaray M, Valle J, Merino N, Latasa C, García B, Ruiz De LosMozos I, Solano C, Toledo-Arana A, Penadés JR, Lasa I (2009) Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 77:3978–3991

    Article  PubMed  CAS  Google Scholar 

  • Wann ER, Gurusiddappa S, Höök M (2000) The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 275:13863–13871

    Article  PubMed  CAS  Google Scholar 

  • Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, Yeaman MR, Bayer AS (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191:1771–1777

    Article  PubMed  CAS  Google Scholar 

  • Williams RJ, Henderson B, Sharp LJ, Nair SP (2002) Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect Immun 70:6805–6810

    Article  PubMed  CAS  Google Scholar 

  • Ziebuhr W (2001) Staphylococcus aureus and Staphylococcus epidermidis: emerging pathogens in nosocomial infections. Contrib Microbiol 8:102–107

    Article  PubMed  CAS  Google Scholar 

  • Ziebuhr W, Heilmann C, Götz F, Meyer P, Wilms K, Straube E, Hacker J (1997) Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 65:890–896

    PubMed  CAS  Google Scholar 

  • Zong Y, Xu Y, Liang X, Keene DR, Höök A, Gurusiddappa S, Höök M, Narayana SV (2005) A ‘Collagen Hug’ model for Staphylococcus aureus CNA binding to collagen. EMBO J 24:4224–4236

    Article  PubMed  CAS  Google Scholar 

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Heilmann, C. (2011). Adhesion Mechanisms of Staphylococci. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_7

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