Staphylococcal biofilms

Current Topics in Microbiology and Immunology

Volumn 322, Issue , 2008, Pages 207-228

  Otto, M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE;

BIOFILM; CELL DEATH; ENVIRONMENTAL FACTOR; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; VACCINATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHYSIOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

BIOFILMS; HUMANS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS;

EID: 45549084273     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-540-75418-3_10     Document Type: Review

References (102)

1. Arber N, Pras E, Copperman Y et al (1994) Pacemaker endocarditis. Report of 44 cases and review of the literature. Medicine (Baltimore) 73:299-305
2. Arciola CR, An YH, Campoccia D, Donati ME, Montanaro L (2005) Etiology of implant orthopedic infections: a survey on 1027 clinical isolates. Int J Artif Organs 28:1091-1100
3. Arciola CR, Campoccia D, Baldassarri L et al (2006) 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 76:425-430
4. Balaban N, Giacometti A, Cirioni O et al (2003) Use of the quorum-sensing inhibitor RNAIII-inhibiting peptide to prevent biofilm formation in vivo by drug-resistant Staphylococcus epidermidis. J Infect Dis 187:625-630
5. Balaban N, Cirioni O, Giacometti A et al (2007) Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother 51:2226-2229
6. Banner MA, Cunniffe JG, Macintosh RL et al (2007) Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J Bacteriol 189:2793-2804
7. Beenken KE, Dunman PM, McAleese F et al (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186:4665-4684
8. Boles BR, Thoendel M, Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210-1223
9. Bowden MG, Visai L, Longshaw CM, Holland KT, Speziale P, Hook M (2002) Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin? J Biol Chem 277:43017-43023
10. Bowden MG, Chen W, Singvall J et al (2005) Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis. Microbiology 151:1453-1464
11. Conlon KM, Humphreys H, O'Gara JP (2002) icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J Bacteriol 184:4400-4408
12. Conlon KM, Humphreys H, O'Gara JP (2004) Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol 186:6208-6219
13. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711-745
14. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322
15. Cramton SE, Ulrich M, Gotz F, Doring G (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69:4079-4085
16. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888-2896
17. Cucarella C, Tormo MA, Ubeda C et al (2004) Role of biofilm-associated protein bap in the pathogenesis of bovine Staphylococcus aureus. Infect Immun 72:2177-2185
18. Darby C, Hsu JW, Ghori N, Falkow S (2002) Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature 417:243-244
19. Davey ME, Caiazza NC, O'Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027-1036
20. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298
21. Dunne WM Jr, Mason EO Jr, Kaplan SL (1993) Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm. Antimicrob Agents Chemother 37:2522-2526
22. Fluckiger U, Ulrich M, Steinhuber A et al (2005) Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 73:1811-1819
23. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Gotz F (1998) Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273:18586-18593
24. Giesbrecht P, Wecke J, Reinicke B (1976) On the morphogenesis of the cell wall of staphylococci. Int Rev Cytol 44:225-318
25. Gill SR, Fouts DE, Archer GL et al (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187:2426-2438
26. Gross M, Cramton SE, Gotz F, Peschel A (2001) Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 69:3423-3426
27. Gu J, Li H, Li M et al (2005) Bacterial insertion sequence IS256 as a potential molecular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis. J Hosp Infect 61:342-348
28. Heilmann C, Gotz F (1998) Further characterization of Staphylococcus epidermidis transposon mutants deficient in primary attachment or intercellular adhesion. Zentralbl Bakteriol 287:69-83
29. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083-1091
30. Heilmann C, Hussain M, Peters G, Gotz F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013-1024
31. Heilmann C, Thumm G, Chhatwal GS, Hartleib J, Uekotter A, Peters G (2003) Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 149:2769-2778
32. Hussain M, Hastings JG, White PJ (1992) Comparison of cell-wall teichoic acid with high-molecular-weight extracellular slime material from Staphylococcus epidermidis. J Med Microbiol 37:368-375
33. Hussain M, Wilcox MH, White PJ (1993) The slime of coagulase-negative staphylococci: biochemistry and relation to adherence. FEMS Microbiol Rev 10:191-207
34. Hussain M, Herrmann M, von Eiff C, Perdreau-Remington F, Peters G (1997) A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces. Infect Immun 65:519-524
35. Hussain M, Heilmann C, Peters G, Herrmann M (2001) Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin. Microb Pathog 31:261-270
36. Ji G, Beavis R, Novick RP (1997) Bacterial interference caused by autoinducing peptide variants. Science 276:2027-2030
37. Jones SM, Morgan M, Humphrey TJ, Lappin-Scott H (2001) Effect of vancomycin and rifampicin on methicillin-resistant Staphylococcus aureus biofilms. Lancet 357:40-41
38. Kaplan JB, Ragunath C, Ramasubbu N, Fine DH (2003) Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J Bacteriol 185:4693-4698
39. Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N (2004a) Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48:2633-2636
40. Kaplan JB, Velliyagounder K, Ragunath C et al (2004b) Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol 186:8213-8220
41. Kelly-Quintos C, Cavacini LA, Posner MR, Goldmann D, Pier GB (2006) 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 74:2742-2750
42. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K (2004) Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230:13-18
43. Kloos W, Schleifer KH (1986) Staphylococcus. In: Sneath PHA, Mair S, Sharpe ME, Holt JG (eds) Bergey's manual of systematic bacteriology. Williams and Wilkins, Baltimore
44. Knobloch JK, Bartscht K, Sabottke A, Rohde H, Feucht HH, Mack D (2001) Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J Bacteriol 183:2624-2633
45. Knobloch JK, Jager S, Horstkotte MA, Rohde H, Mack D (2004) 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 72:3838-3848
46. Kocianova S, Vuong C, Yao Y et al (2005) Key role of poly-gamma-DL- glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J Clin Invest 115:688-694
47. Kozitskaya S, Cho SH, Dietrich K, Marre R, Naber K, Ziebuhr W (2004) The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides. Infect Immun 72:1210-1215
48. Kozitskaya S, Olson ME, Fey PD, Witte W, Ohlsen K, Ziebuhr W (2005) Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J Clin Microbiol 43:4751-4757
49. Kristian SA, Golda T, Ferracin F et al (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
50. Lasa I, Penades JR (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:99-107
51. Latasa C, Roux A, Toledo-Arana A et al (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58:1322-1339
52. Li H, Xu L, Wang J et al (2005) Conversion of Staphylococcus epidermidis strains from commensal to invasive by expression of the ica locus encoding production of biofilm exopolysaccharide. Infect Immun 73:3188-3191
53. Lim Y, Jana M, Luong TT, Lee CY (2004) Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus. J Bacteriol 186:722-729
54. Mack D, Fischer W, Krokotsch A et al (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178:175-183
55. Marraffini LA, Dedent AC, Schneewind O (2006) Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol Mol Biol Rev 70:192-221
56. Mazmanian SK, Liu G, Ton-That H, Schneewind O (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760-763
57. McCrea KW, Hartford O, Davis S et al (2000) The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis . Microbiology 146:1535-1546
58. Mehlin C, Headley CM, Klebanoff SJ (1999) An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J Exp Med 189:907-918
59. Navarre WW, Schneewind O (1999) Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174-229
60. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48:1429-1449
61. Otto M (2006) Bacterial evasion of antimicrobial peptides by biofilm formation. Curr Top Microbiol Immunol 306:251-258
62. Patti JM, Allen BL, McGavin MJ, Hook M (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585-617
63. Peschel A, Vuong C, Otto M, Gotz F (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44:2845-2847
64. Qazi S, Middleton B, Muharram SH et al (2006) N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910-919
65. Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W (2000) Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 44:3357-3363
66. Renders N, Verbrugh H, Van Belkum A (2001) Dynamics of bacterial colonisation in the respiratory tract of patients with cystic fibrosis. Infect Genet Evol 1:29-39
67. Rennermalm A, Li YH, Bohaufs L et al (2001) Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat. Vaccine 19:3376-3383
68. Resch A, Rosenstein R, Nerz C, Gotz F (2005) Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 71:2663-2676
69. Resch A, Leicht S, Saric M et al (2006) Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6:1867-1877
70. Rice KC, Bayles KW (2003) Death's toolbox: examining the molecular components of bacterial programmed cell death. Mol Microbiol 50:729-738
71. Rice KC, Mann EE, Endres JL et al (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 104:8113-8118
72. Rohde H, Burdelski C, Bartscht K et al (2005) Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 55:1883-1895
73. Rohde H, Burandt EC, Siemssen N et al (2007) Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 28:1711-1720
74. Rupp ME, Ulphani JS, Fey PD, Bartscht K, Mack D (1999a) Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 67:2627-2632
75. Rupp ME, Ulphani JS, Fey PD, Mack D (1999b) Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect Immun 67:2656-2659
76. Rupp ME, Fey PD, Heilmann C, Gotz F (2001) Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis 183:1038-1042
77. Sadovskaya I, Vinogradov E, Flahaut S, Kogan G, Jabbouri S (2005) Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect Immun 73:3007-3017
78. Shaw LN, Jonnson IM, Singh VK, Tarkowski A, Stewart GC (2007) Inactivation of traP has no effect on the Agr quorum sensing system or virulence of Staphylococcus aureus. Infect Immun 75:4521-4527
79. Somerville GA, Beres SB, Fitzgerald JR et al (2002) In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence. J Bacteriol 184:1430-1437
80. Tormo MA, Marti M, Valle J et al (2005) SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol 187:2348-2356
81. Tsang LH, Daily ST, Weiss EC, Smeltzer MS (2007) Mutation of traP in Staphylococcus aureus has no impact on expression of agr or biofilm formation. Infect Immun 75:4528-4533
82. Vadyvaloo V, Otto M (2005) Molecular genetics of Staphylococcus epidermidis biofilms on indwelling medical devices. Int J Artif Organs 28:1069-1078
83. Van Belkum A (2006) Staphylococcal colonization and infection: homeostasis versus disbalance of human (innate) immunity and bacterial virulence. Curr Opin Infect Dis 19:339-344
84. Veenstra GJ, Cremers FF, van Dijk H, Fleer A (1996) Ultrastructural organization and regulation of a biomaterial adhesin of Staphylococcus epidermidis. J Bacteriol 178:537-541
85. Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microbes Infect 4:481-489
86. Vuong C, Saenz HL, Gotz F, Otto M (2000) Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J Infect Dis 182:1688-1693
87. Vuong C, Gerke C, Somerville GA, Fischer ER, Otto M (2003) Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J Infect Dis 188:706-718
88. Vuong C, Kocianova S, Voyich JM et al (2004a) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279:54881-54886
89. Vuong C, Kocianova S, Yao Y, Carmody AB, Otto M (2004b) Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J Infect Dis 190:1498-1505
90. Vuong C, Voyich JM, Fischer ER et al (2004c) Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6:269-275
91. Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47:317-323
92. Wang X, Preston JFI, Romeo T (2004) The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724-2734
93. Wright JS 3rd, Jin R, Novick RP (2005) Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc Natl Acad Sci U S A 102:1691-1696
94. Wu JA, Kusuma C, Mond JJ, Kokai-Kun JF (2003) Lysostaphin disrupts Staphylococcus aureus and Staphylococcus epidermidis biofilms on artificial surfaces. Antimicrob Agents Chemother 47:3407-3414
95. Xu L, Li H, Vuong C et al (2006) Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect Immun 74:488-496
96. Yang SJ, Dunman PM, Projan SJ, Bayles KW (2006) Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis. Mol Microbiol 60:458-468
97. Yao Y, Sturdevant DE, Otto M (2005) 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
98. Yao Y, Vuong C, Kocianova S et al (2006) Characterization of the Staphylococcus epidermidis accessory-gene regulator response: quorum-sensing regulation of resistance to human innate host defense. J Infect Dis 193:841-848
99. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186:1838-1850
100. Zhang YQ, Ren SX, Li HL et al (2003) Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 49:1577-1593
101. Ziebuhr W, Krimmer V, Rachid S, Lossner I, Gotz F, Hacker J (1999) 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 32:345-356
102. Zimmerli W, Waldvogel FA, Vaudaux P, Nydegger UE (1982) Pathogenesis of foreign body infection: description and characteristics of an animal model. J Infect Dis 146:487-497