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PMID: 18453278 Published · ppublish English Journal Article Review

Staphylococcal biofilms.

Current topics in microbiology and immunology ·Vol. 322 ·2008-00-00 ·Pages 207-28

Otto M

Abstract

Staphylococcus epidermidis and Staphylococcus aureus are the most frequent causes of nosocomial infections and infections on indwelling medical devices, which characteristically involve biofilms. Recent advances in staphylococcal molecular biology have provided more detailed insight into the basis of biofilm formation in these opportunistic pathogens. A series of surface proteins mediate initial attachment to host matrix proteins, which is followed by the expression of a cationic glucosamine-based exopolysaccharide that aggregates the bacterial cells. In some cases, proteins may function as alternative aggregating substances. Furthermore, surfactant peptides have now been recognized as key factors involved in generating the three-dimensional structure of a staphylococcal biofilm by cell-cell disruptive forces, which eventually may lead to the detachment of entire cell clusters. Transcriptional profiling experiments have defined the specific physiology of staphylococcal biofilms and demonstrated that biofilm resistance to antimicrobials is due to gene-regulated processes. Finally, novel animal models of staphylococcal biofilm-associated infection have given us important information on which factors define biofilm formation in vivo. These recent advances constitute an important basis for the development of anti-staphylococcal drugs and vaccines.

MeSH Terms
Biofilms/growth & development Humans Staphylococcal Infections/microbiology Staphylococcus/physiology
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Otto M
Laboratory of Human Bacterial Pathogenesis, National Institute of Allergy and Infectious Diseases, The National Institutes of Health, Rocky Mountain Laboratories, Hamilton, MT, USA. motto@niaid.nih.gov
References (101)
101 references, click to expand
  1. The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides.
    Infect Immun. 2004 Feb;72(2):1210-5 PMID: 14742578
  2. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces.
    Infect Immun. 2001 May;69(5):3423-6 PMID: 11292767
  3. Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A.
    Infect Immun. 2005 May;73(5):3007-17 PMID: 15845508
  4. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis.
    Infect Immun. 2006 Jan;74(1):488-96 PMID: 16369005
  5. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus.
    J Infect Dis. 2000 Dec;182(6):1688-93 PMID: 11069241
  6. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system.
    Cell Microbiol. 2004 Mar;6(3):269-75 PMID: 14764110
  7. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model.
    Infect Immun. 2005 Mar;73(3):1811-9 PMID: 15731082
  8. 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 May;36(5):237-45 PMID: 15043859
  9. An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization.
    J Exp Med. 1999 Mar 15;189(6):907-18 PMID: 10075974
  10. Use of the quorum-sensing inhibitor RNAIII-inhibiting peptide to prevent biofilm formation in vivo by drug-resistant Staphylococcus epidermidis.
    J Infect Dis. 2003 Feb 15;187(4):625-30 PMID: 12599079
  11. Quorum sensing in Staphylococcus aureus biofilms.
    J Bacteriol. 2004 Mar;186(6):1838-50 PMID: 14996815
  12. Microbial biofilms.
    Annu Rev Microbiol. 1995;49:711-45 PMID: 8561477
  13. Ultrastructural organization and regulation of a biomaterial adhesin of Staphylococcus epidermidis.
    J Bacteriol. 1996 Jan;178(2):537-41 PMID: 8550477
  14. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms.
    Mol Microbiol. 2005 Sep;57(5):1210-23 PMID: 16101996
  15. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence.
    J Bacteriol. 2002 Mar;184(5):1430-7 PMID: 11844774
  16. Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis.
    Microbiology (Reading). 2005 May;151(Pt 5):1453-1464 PMID: 15870455
  17. Autoinduction and signal transduction in the regulation of staphylococcal virulence.
    Mol Microbiol. 2003 Jun;48(6):1429-49 PMID: 12791129
  18. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development.
    J Bacteriol. 2005 Apr;187(7):2348-56 PMID: 15774878
  19. Enzymatic detachment of Staphylococcus epidermidis biofilms.
    Antimicrob Agents Chemother. 2004 Jul;48(7):2633-6 PMID: 15215120
  20. Global gene expression in Staphylococcus aureus biofilms.
    J Bacteriol. 2004 Jul;186(14):4665-84 PMID: 15231800
  21. Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing.
    J Clin Microbiol. 2005 Sep;43(9):4751-7 PMID: 16145137
  22. Key role of poly-gamma-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis.
    J Clin Invest. 2005 Mar;115(3):688-94 PMID: 15696197
  23. Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo.
    J Infect Dis. 2004 Oct 15;190(8):1498-505 PMID: 15378444
  24. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases.
    Mol Microbiol. 2005 Mar;55(6):1883-95 PMID: 15752207
  25. Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein.
    J Bacteriol. 2007 Apr;189(7):2793-804 PMID: 17277069
  26. Mutation of traP in Staphylococcus aureus has no impact on expression of agr or biofilm formation.
    Infect Immun. 2007 Sep;75(9):4528-33 PMID: 17548479
  27. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling.
    Proteomics. 2006 Mar;6(6):1867-77 PMID: 16470655
  28. Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis.
    Mol Microbiol. 2006 Apr;60(2):458-68 PMID: 16573694
  29. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis.
    Mol Microbiol. 2005 Dec;58(5):1322-39 PMID: 16313619
  30. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):174-229 PMID: 10066836
  31. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis.
    Mol Microbiol. 1996 Jun;20(5):1083-91 PMID: 8809760
  32. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall.
    Science. 1999 Jul 30;285(5428):760-3 PMID: 10427003
  33. Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm.
    Antimicrob Agents Chemother. 1993 Dec;37(12):2522-6 PMID: 8109913
  34. Bacterial evasion of antimicrobial peptides by biofilm formation.
    Curr Top Microbiol Immunol. 2006;306:251-8 PMID: 16909925
  35. 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 Mar;28(9):1711-20 PMID: 17187854
  36. Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP.
    Antimicrob Agents Chemother. 2007 Jun;51(6):2226-9 PMID: 17371825
  37. Characterization of the opsonic and protective activity against Staphylococcus aureus of fully human monoclonal antibodies specific for the bacterial surface polysaccharide poly-N-acetylglucosamine.
    Infect Immun. 2006 May;74(5):2742-50 PMID: 16622211
  38. Dynamics of bacterial colonisation in the respiratory tract of patients with cystic fibrosis.
    Infect Genet Evol. 2001 Jul;1(1):29-39 PMID: 12798048
  39. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis.
    Infect Immun. 2001 Jun;69(6):4079-85 PMID: 11349079
  40. Staphylococcus epidermidis infections.
    Microbes Infect. 2002 Apr;4(4):481-9 PMID: 11932199
  41. 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 Apr;187(7):2426-38 PMID: 15774886
  42. Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin.
    Microb Pathog. 2001 Dec;31(6):261-70 PMID: 11747374
  43. RsbU-dependent regulation of Staphylococcus epidermidis biofilm formation is mediated via the alternative sigma factor sigmaB by repression of the negative regulator gene icaR.
    Infect Immun. 2004 Jul;72(7):3838-48 PMID: 15213125
  44. 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 May;67(5):2627-32 PMID: 10225932
  45. Conversion of Staphylococcus epidermidis strains from commensal to invasive by expression of the ica locus encoding production of biofilm exopolysaccharide.
    Infect Immun. 2005 May;73(5):3188-91 PMID: 15845531
  46. 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 Apr 1;183(7):1038-42 PMID: 11237828
  47. MSCRAMM-mediated adherence of microorganisms to host tissues.
    Annu Rev Microbiol. 1994;48:585-617 PMID: 7826020
  48. Death's toolbox: examining the molecular components of bacterial programmed cell death.
    Mol Microbiol. 2003 Nov;50(3):729-38 PMID: 14617136
  49. On the morphogenesis of the cell wall of staphylococci.
    Int Rev Cytol. 1976;44:225-318 PMID: 770370
  50. Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat.
    Vaccine. 2001 May 14;19(25-26):3376-83 PMID: 11348701
  51. 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. 2001 Apr;183(8):2624-33 PMID: 11274123
  52. Molecular genetics of Staphylococcus epidermidis biofilms on indwelling medical devices.
    Int J Artif Organs. 2005 Nov;28(11):1069-78 PMID: 16353113
  53. Detection of biofilm formation in Staphylococcus epidermidis from implant infections. Comparison of a PCR-method that recognizes the presence of ica genes with two classic phenotypic methods.
    J Biomed Mater Res A. 2006 Feb;76(2):425-30 PMID: 16270350
  54. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis.
    Antimicrob Agents Chemother. 2000 Dec;44(12):3357-63 PMID: 11083640
  55. 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 Jan;178(1):175-83 PMID: 8550413
  56. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin.
    Antimicrob Agents Chemother. 2003 Jan;47(1):317-23 PMID: 12499208
  57. The involvement of cell-to-cell signals in the development of a bacterial biofilm.
    Science. 1998 Apr 10;280(5361):295-8 PMID: 9535661
  58. Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria.
    Microbiol Mol Biol Rev. 2006 Mar;70(1):192-221 PMID: 16524923
  59. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis.
    J Infect Dis. 2003 Sep 1;188(5):706-18 PMID: 12934187
  60. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms.
    J Bacteriol. 2004 Dec;186(24):8213-20 PMID: 15576769
  61. Lysostaphin disrupts Staphylococcus aureus and Staphylococcus epidermidis biofilms on artificial surfaces.
    Antimicrob Agents Chemother. 2003 Nov;47(11):3407-14 PMID: 14576095
  62. Bacterial insertion sequence IS256 as a potential molecular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis.
    J Hosp Infect. 2005 Dec;61(4):342-8 PMID: 16242209
  63. Characterization of the Staphylococcus epidermidis accessory-gene regulator response: quorum-sensing regulation of resistance to human innate host defense.
    J Infect Dis. 2006 Mar 15;193(6):841-8 PMID: 16479519
  64. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin.
    J Biol Chem. 1998 Jul 17;273(29):18586-93 PMID: 9660830
  65. 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 Jan 15;191(2):289-98 PMID: 15609240
  66. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis.
    J Bacteriol. 2002 Aug;184(16):4400-8 PMID: 12142410
  67. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation.
    J Bacteriol. 2004 May;186(9):2724-34 PMID: 15090514
  68. Comparison of cell-wall teichoic acid with high-molecular-weight extracellular slime material from Staphylococcus epidermidis.
    J Med Microbiol. 1992 Dec;37(6):368-75 PMID: 1460655
  69. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence.
    J Biol Chem. 2004 Dec 24;279(52):54881-6 PMID: 15501828
  70. Bap: a family of surface proteins involved in biofilm formation.
    Res Microbiol. 2006 Mar;157(2):99-107 PMID: 16427771
  71. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions.
    Appl Environ Microbiol. 2005 May;71(5):2663-76 PMID: 15870358
  72. Etiology of implant orthopedic infections: a survey on 1027 clinical isolates.
    Int J Artif Organs. 2005 Nov;28(11):1091-100 PMID: 16353115
  73. Role of biofilm-associated protein bap in the pathogenesis of bovine Staphylococcus aureus.
    Infect Immun. 2004 Apr;72(4):2177-85 PMID: 15039341
  74. Inactivation of traP has no effect on the agr quorum-sensing system or virulence of Staphylococcus aureus.
    Infect Immun. 2007 Sep;75(9):4519-27 PMID: 17548478
  75. The slime of coagulase-negative staphylococci: biochemistry and relation to adherence.
    FEMS Microbiol Rev. 1993 Apr;10(3-4):191-207 PMID: 8318256
  76. Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus.
    J Bacteriol. 2004 Feb;186(3):722-9 PMID: 14729698
  77. Effect of vancomycin and rifampicin on meticillin-resistant Staphylococcus aureus biofilms.
    Lancet. 2001 Jan 6;357(9249):40-1 PMID: 11197363
  78. Transient interference with staphylococcal quorum sensing blocks abscess formation.
    Proc Natl Acad Sci U S A. 2005 Feb 1;102(5):1691-6 PMID: 15665088
  79. 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 IS256.
    Mol Microbiol. 1999 Apr;32(2):345-56 PMID: 10231490
  80. N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus.
    Infect Immun. 2006 Feb;74(2):910-9 PMID: 16428734
  81. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model.
    Infect Immun. 1999 May;67(5):2656-9 PMID: 10225938
  82. The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis.
    Microbiology (Reading). 2000 Jul;146 ( Pt 7):1535-1546 PMID: 10878118
  83. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228).
    Mol Microbiol. 2003 Sep;49(6):1577-93 PMID: 12950922
  84. Caenorhabditis elegans: plague bacteria biofilm blocks food intake.
    Nature. 2002 May 16;417(6886):243-4 PMID: 12015591
  85. Bacterial interference caused by autoinducing peptide variants.
    Science. 1997 Jun 27;276(5321):2027-30 PMID: 9197262
  86. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes.
    Antimicrob Agents Chemother. 2000 Oct;44(10):2845-7 PMID: 10991869
  87. Staphylococcal colonization and infection: homeostasis versus disbalance of human (innate) immunity and bacterial virulence.
    Curr Opin Infect Dis. 2006 Aug;19(4):339-44 PMID: 16804380
  88. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1.
    J Bacteriol. 2003 Feb;185(3):1027-36 PMID: 12533479
  89. Persister cells and tolerance to antimicrobials.
    FEMS Microbiol Lett. 2004 Jan 15;230(1):13-8 PMID: 14734160
  90. Further characterization of Staphylococcus epidermidis transposon mutants deficient in primary attachment or intercellular adhesion.
    Zentralbl Bakteriol. 1998 Jan;287(1-2):69-83 PMID: 9532266
  91. Pathogenesis of foreign body infection: description and characteristics of an animal model.
    J Infect Dis. 1982 Oct;146(4):487-97 PMID: 7119479
  92. Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin?
    J Biol Chem. 2002 Nov 8;277(45):43017-23 PMID: 12218064
  93. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):8113-8 PMID: 17452642
  94. Pacemaker endocarditis. Report of 44 cases and review of the literature.
    Medicine (Baltimore). 1994 Nov;73(6):299-305 PMID: 7984081
  95. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity.
    J Bacteriol. 2003 Aug;185(16):4693-8 PMID: 12896987
  96. Bap, a Staphylococcus aureus surface protein involved in biofilm formation.
    J Bacteriol. 2001 May;183(9):2888-96 PMID: 11292810
  97. Bacterial biofilms: a common cause of persistent infections.
    Science. 1999 May 21;284(5418):1318-22 PMID: 10334980
  98. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface.
    Mol Microbiol. 1997 Jun;24(5):1013-24 PMID: 9220008
  99. Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis.
    Microbiology (Reading). 2003 Oct;149(Pt 10):2769-2778 PMID: 14523110
  100. Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis.
    J Bacteriol. 2004 Sep;186(18):6208-19 PMID: 15342591
  101. A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces.
    Infect Immun. 1997 Feb;65(2):519-24 PMID: 9009307
Article Info
Journal
Current topics in microbiology and immunology
Abbr.
Curr Top Microbiol Immunol
ISSN
0070-217X
Published
2008-00-00
Pages
207-28
Language
English
Region
Germany
NLM ID
0110513
PMCID
PMC2777538
Subset
IM
Grants
Intramural NIH HHS · Z99 AI999999 · United States
Intramural NIH HHS · ZIA AI001080-02 · United States
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