Biomolecular mechanisms of staphylococcal biofilm formation

Future Microbiology

Volumn 8, Issue 4, 2013, Pages 509-524

  Laverty, Garry ^a   Gorman, Sean P ^a   Gilmore, Brendan F ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

adhesins; adhesion; biomaterial; ica operon; quorum sensing

Indexed keywords

ADHESIN; RNA POLYMERASE; STAPHYLOCOCCUS PROTEIN A; TEICHOIC ACID; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE;

ACETYLATION; AMINO ACID SEQUENCE; ANTIBIOSIS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; BACTERIAL CAPSULE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BINDING SITE; BIOFILM; BIOMASS; BIOMASS PRODUCTION; BIOSYNTHESIS; CELL ADHESION; CELL COMMUNICATION; CELL SURFACE; COAGULASE NEGATIVE STAPHYLOCOCCUS; DEACETYLATION; ENVIRONMENTAL STRESS; EXTRACELLULAR MATRIX; GENE CLUSTER; HYDROPHOBICITY; NONHUMAN; OPERON; PHAGOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PURINE SYNTHESIS; QUORUM SENSING; REGULATORY MECHANISM; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STATIC ELECTRICITY; SURFACE CHARGE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BIOFILMS; HUMANS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

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

EID: 84875751532     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.13.7     Document Type: Review

References (130)

1. Bixler GD, Bhushan B. Biofouling: lessons from nature. Philos. Transact. A Math. Phys. Eng. Sci. 370(1967), 2381-2417 (2012).
2. Resch A, Rosenstein R, Nerz C, Gotz F. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 71(5), 2663-2676 (2005).
3. Cogen AL, Nizet V, Gallo RL. Skin microbiota: a source of disease or defence? Br. J. Dermatol. 158(3), 442-455 (2008).
4. Harris LG, Richards RG. Staphylococci and implant surfaces: a review. Injury 37(Suppl. 2), S3-S14 (2006).
5. Pascual A, Fleer A, Westerdaal NA, Verhoef J. Modulation of adherence of coagulase-negative staphylococci to Teflon catheters in vitro. Eur. J. Clin. Microbiol. 5(5), 518-522 (1986).
6. Tojo M, Yamashita N, Goldmann DA, Pier GB. Isolation and characterization of a capsular polysaccharide adhesin from Staphylococcus epidermidis. J. Infect. Dis. 157(4), 713-722 (1988).
7. Maira-Litran T, Kropec A, Abeygunawardana C et al. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect. Immun. 70(8), 4433-4440 (2002).
8. Shiro H, Meluleni G, Groll A et al. The pathogenic role of Staphylococcus epidermidis capsular polysaccharide/adhesin in a low-inoculum rabbit model of prosthetic valve endocarditis. Circulation 92(9), 2715-2722 (1995).
9. Christensen GD, Barker LP, Mawhinney TP, Baddour LM, Simpson WA. Identification of an antigenic marker of slime production for Staphylococcus epidermidis. Infect. Immun. 58(9), 2906-2911 (1990).
10. 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. 64(8), 3410-3415 (1996).
11. von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect. Dis. 2(11), 677-685 (2002).
12. Maira-Litran T, Kropec A, Goldmann D, Pier GB. Biologic properties and vaccine potential of the staphylococcal poly-N-acetyl glucosamine surface polysaccharide. Vaccine 22(7), 872-879 (2004).
13. Sadovskaya I, Vinogradov E, Flahaut S, Kogan G, Jabbouri S. Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect. Immun. 73(5), 3007-3017 (2005).
14. McKenney D, Hubner J, Muller E, Wang Y, Goldmann DA, Pier GB. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect. Immun. 66(10), 4711-4720 (1998).
15. Heilmann C, Gerke C, Perdreau-Remington F, Gotz F. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun. 64(1), 277-282 (1996).
16. 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. 183(7), 1038-1042 (2001).
17. Heilmann C, Hussain M, Peters G, Gotz F. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol. 24(5), 1013-1024 (1997).
18. Heilmann C, Thumm G, Chhatwal GS, Hartleib J, Uekotter A, Peters G. Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 149(Pt 10), 2769-2778 (2003).
19. Mack D. Molecular mechanisms of Staphylococcus epidermidis biofilm formation. J. Hosp. Infect. 43(Suppl.), S113-S125 (1999).
20. Biswas R, Voggu L, Simon UK, Hentschel P, Thumm G, Gotz F. Activity of the major staphylococcal autolysin Atl. FEMS Microbiol. Lett. 259(2), 260-268 (2006).
21. Hirschhausen N, Schlesier T, Schmidt MA, Gotz F, Peters G, Heilmann C. A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell. Microbiol. 12(12), 1746-1764 (2010).
22. Qin Z, Ou Y, Yang L et al. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153(Pt 7), 2083-2092 (2007).
23. Bose JL, Lehman MK, Fey PD, Bayles KW. Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS ONE 7(7), e42244 (2012).
24. Rice KC, Mann EE, Endres JL et al. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl Acad. Sci. USA 104(19), 8113-8118 (2007).
25. Mann EE, Rice KC, Boles BR et al. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4(6), e5822 (2009).
26. Bowden MG, Visai L, Longshaw CM, Holland KT, Speziale P, Hook M. Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin? J. Biol. Chem. 277(45), 43017-43023 (2002)
27. Williams RJ, Henderson B, Sharp LJ, Nair SP. Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect. Immun. 70(12), 6805-6810 (2002).
28. Hartford O, O'Brien L, Schofield K, Wells J, Foster TJ. The Fbe (SdrG) protein of Staphylococcus epidermidis HB promotes bacterial adherence to fibrinogen. Microbiology 147(Pt 9), 2545-2552 (2001).
29. Josefsson E, McCrea KW, Ni Eidhin D et al. Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology 144(Pt 12), 3387-3395 (1998).
30. Pei L, Palma M, Nilsson M, Guss B, Flock JI. Functional studies of a fibrinogen binding protein from Staphylococcus epidermidis. Infect. Immun. 67(9), 4525-4530 (1999).
31. Nilsson M, Frykberg L, Flock JI, Pei L, Lindberg M, Guss B. A fibrinogen-binding protein of Staphylococcus epidermidis. Infect. Immun. 66(6), 2666-2673 (1998).
32. Risley AL, Loughman A, Cywes-Bentley C, Foster TJ, Lee JC. Capsular polysaccharide masks clumping factor A-mediated adherence of Staphylococcus aureus to fibrinogen and platelets. J. Infect. Dis. 196(6), 919-927 (2007).
33. Wertheim HF, Walsh E, Choudhurry R et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 5(1), e17 (2008).
34. Jefferson KK. What drives bacteria to produce a biofilm? FEMS Microbiol. Lett. 236(2), 163-173 (2004).
35. Pei L, Flock JI. Lack of fbe, the gene for a fibrinogen-binding protein from Staphylococcus epidermidis, reduces its adherence to fibrinogen coated surfaces. Microb. Pathog. 31(4), 185-193 (2001).
36. Houston P, Rowe SE, Pozzi C, Waters EM, O'Gara JP. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect. Immun. 79(3), 1153-1165 (2011).
37. O'Neill E, Pozzi C, Houston P et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol. 190(11), 3835-3850 (2008).
38. Shanks RM, Meehl MA, Brothers KM et al. Genetic evidence for an alternative citrate-dependent biofilm formation pathway in Staphylococcus aureus that is dependent on fibronectin binding proteins and the GraRS two-component regulatory system. Infect. Immun. 76(6), 2469-2477 (2008).
39. Vergara-Irigaray M, Valle J, Merino N et al. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect. Immun. 77(9), 3978-3991 (2009).
40. Mazmanian SK, Ton-That H, Schneewind O. Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol. Microbiol. 40(5), 1049-1057 (2001).
41. Schneewind O, Mihaylova-Petkov D, Model P. Cell wall sorting signals in surface proteins of Gram-positive bacteria. EMBO J. 12(12), 4803-4811 (1993).
42. Marraffini LA, Dedent AC, Schneewind O. Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70(1), 192-221 (2006).
43. Review focusing on the mechanisms of surface protein anchoring to the cell wall envelope by sortases and their role in bacterial pathogenesis. Weidenmaier C, Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6(4), 276-287 (2008).
44. Sadovskaya I, Vinogradov E, Li J, Jabbouri S. Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr. Res. 339(8), 1467-1473 (2004).
45. Gross M, Cramton SE, Gotz F, Peschel A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69(5), 3423-3426 (2001).
46. Vergara-Irigaray M, Maira-Litran T, Merino N, Pier GB, Penades JR, Lasa I. Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology 154(Pt 3), 865-877 (2008).
47. Gotz F. Staphylococcus and biofilms. Mol. Microbiol. 43(6), 1367-1378 (2002).
48. nn Explores the genetic and molecular basis of biofilm formation in staphylococci, including the roles of the ica operon, AtlE and teichoic acids. Peschel A, Collins LV. Staphylococcal resistance to antimicrobial peptides of mammalian and bacterial origin. Peptides 22(10), 1651-1659 (2001).
49. Ziebuhr W, Heilmann C, Gotz F et al. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect. Immun. 65(3), 890-896 (1997).
50. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20(5), 1083-1091 (1996).
51. Mack D, Fischer W, Krokotsch A et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear b-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178(1), 175-183 (1996).
52. Vuong C, Kocianova S, Voyich JM et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 279(52), 54881-54886 (2004).
53. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Gotz F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J. Biol. Chem. 273(29), 18586-18593 (1998).
54. Jefferson KK, Cramton SE, Gotz F, Pier GB. Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol. Microbiol. 48(4), 889-899 (2003).
55. Begun J, Gaiani JM, Rohde H et al. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3(4), e57 (2007).
56. Li H, Xu L, Wang J et al. Conversion of Staphylococcus epidermidis strains from commensal to invasive by expression of the ica locus encoding production of biofilm exopolysaccharide. Infect. Immun. 73(5), 3188-3191 (2005).
57. Knobloch JK, Jager S, Horstkotte MA, Rohde H, Mack D. RsbU-dependent regulation of Staphylococcus epidermidis biofilm formation is mediated via the alternative s factor sB by repression of the negative regulator gene icaR. Infect. Immun. 72(7), 3838-3848 (2004).
58. Valle J, Toledo-Arana A, Berasain C et al. SarA and not sB is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48(4), 1075-1087 (2003).
59. Lauderdale KJ, Boles BR, Cheung AL, Horswill AR. Interconnections between sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect. Immun. 77(4), 1623-1635 (2009).
60. Jager S, Mack D, Rohde H, Horstkotte MA, Knobloch JK. Disintegration of Staphylococcus epidermidis biofilms under glucose-limiting conditions depends on the activity of the alternative s factor sB. Appl. Environ. Microbiol. 71(9), 5577-5581 (2005).
61. Conlon KM, Humphreys H, O'Gara JP. Regulation of icaR gene expression in Staphylococcus epidermidis. FEMS Microbiol. Lett. 216(2), 171-177 (2002).
62. Conlon KM, Humphreys H, O'Gara JP. Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J. Bacteriol. 186(18), 6208-6219 (2004).
63. Kullik I, Giachino P, Fuchs T. Deletion of the alternative s factor sB in Staphylococcus aureus reveals its function as a global regulator of virulence genes. J. Bacteriol. 180(18), 4814-4820 (1998).
64. Rachid S, Ohlsen K, Wallner U, Hacker J, Hecker M, Ziebuhr W. Alternative transcription factor sB is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J. Bacteriol. 182(23), 6824-6826 (2000).
65. Knobloch JK, Horstkotte MA, Rohde H, Kaulfers PM, Mack D. Alcoholic ingredients in skin disinfectants increase biofilm expression of Staphylococcus epidermidis. J. Antimicrob. Chemother. 49(4), 683-687 (2002).
66. Knobloch JK, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med. Microbiol. Immunol. 191(2), 101-106 (2002).
67. Baldassarri L, Bertuccini L, Ammendolia MG, Arciola CR, Montanaro L. Effect of iron limitation on slime production by Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 20(5), 343-345 (2001).
68. Valle J, Vergara-Irigaray M, Merino N, Penades JR, Lasa I. sB regulates IS256- mediated Staphylococcus aureus biofilm phenotypic variation. J. Bacteriol. 189(7), 2886-2896 (2007).
69. Fluckiger U, Wolz C, Cheung AL. Characterization of a sar homolog of Staphylococcus epidermidis. Infect. Immun. 66(6), 2871-2878 (1998).
70. Tormo MA, Marti M, Valle J et al. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J. Bacteriol. 187(7), 2348-2356 (2005).
71. Beenken KE, Blevins JS, Smeltzer MS. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71(7), 4206-4211 (2003).
72. Beenken KE, Mrak LN, Griffin LM et al. Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLoS ONE 5(5), e10790 (2010).
73. Mrak LN, Zielinska AK, Beenken KE et al. saeRS and sarA act synergistically to repress protease production and promote biofilm formation in Staphylococcus aureus. PLoS ONE 7(6), e38453 (2012).
74. Trotonda MP, Manna AC, Cheung AL, Lasa I, Penades Jr. SarA positively controls bap-dependent biofilm formation in Staphylococcus aureus. J. Bacteriol. 187(16), 5790-5798 (2005).
75. Mack D, Davies AP, Harris LG, Rohde H, Horstkotte MA, Knobloch JK. Microbial interactions in Staphylococcus epidermidis biofilms. Anal. Bioanal. Chem. 387(2), 399-408 (2007).
76. nn Elucidation of the factors involved and progress made in determining the pathogenesis of S. epidermidis biofilms in a medical device setting. 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. 255(1), 11-16 (2006).
77. Chokr A, Watier D, Eleaume H et al. Correlation between biofilm formation and production of polysaccharide intercellular adhesin in clinical isolates of coagulase-negative staphylococci. Int. J. Med. Microbiol. 296(6), 381-388 (2006).
78. 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. 65(2), 519-524 (1997).
79. Corrigan RM, Rigby D, Handley P, Foster TJ. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153(Pt 8), 2435-2446 (2007).
80. Rohde H, Burdelski C, Bartscht K et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol. 55(6), 1883-1895 (2005).
81. Bateman A, Holden MT, Yeats C. The G5 domain: a potential N-acetylglucosamine recognition domain involved in biofilm formation. Bioinformatics 21(8), 1301-1303 (2005).
82. Lindsay JA, Foster SJ. Interactive regulatory pathways control virulence determinant production and stability in response to environmental conditions in Staphylococcus aureus. Mol. Gen. Genet. 262(2), 323-331 (1999).
83. Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48(6), 1429-1449 (2003).
84. Xu L, Li H, Vuong C et al. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect. Immun. 74(1), 488-496 (2006).
85. Doherty N, Holden MT, Qazi SN, Williams P, Winzer K. Functional analysis of luxS in Staphylococcus aureus reveals a role in metabolism but not quorum sensing. J. Bacteriol. 188(8), 2885-2897 (2006).
86. Li YH, Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel) 12(3), 2519-2538 (2012).
87. Morfeldt E, Taylor D, von Gabain A, Arvidson S. Activation of a-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14(18), 4569-4577 (1995).
88. Novick RP, Projan SJ, Kornblum J et al. The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol. Gen. Genet. 248(4), 446-458 (1995).
89. Zhang L, Lin J, Ji G. Membrane anchoring of the AgrD N-terminal amphipathic region is required for its processing to produce a quorum-sensing pheromone in Staphylococcus aureus. J. Biol. Chem. 279(19), 19448-19456 (2004).
90. Kavanaugh JS, Thoendel M, Horswill AR. A role for type I signal peptidase in Staphylococcus aureus quorum sensing. Mol. Microbiol. 65(3), 780-798 (2007).
91. Kong KF, Vuong C, Otto M. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296(2-3), 133-139 (2006).
92. Vuong C, Saenz HL, Gotz F, Otto M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182(6), 1688-1693 (2000).
93. Ji G, Beavis R, Novick RP. Bacterial interference caused by autoinducing peptide variants. Science 276(5321), 2027-2030 (1997).
94. Dunman PM, Murphy E, Haney S et al. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183(24), 7341-7353 (2001).
95. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186(6), 1838-1850 (2004).
96. Yao Y, Sturdevant DE, Otto M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis. 191(2), 289-298 (2005).
97. Vuong C, Durr M, Carmody AB, Peschel A, Klebanoff SJ, Otto M. Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epidermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modulins. Cell. Microbiol. 6(8), 753-759 (2004).
98. Schwartz K, Syed AK, Stephenson RE, Rickard AH, Boles BR. Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8(6), e1002744 (2012).
99. Periasamy S, Joo HS, Duong AC et al. How Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl Acad. Sci. USA 109(4), 1281-1286 (2012).
100. Boles BR, Horswill AR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4(4), e1000052 (2008).
101. Dubin G. Extracellular proteases of Staphylococcus spp. Biol. Chem. 383(7-8), 1075-1086 (2002).
102. Lopez D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harb. Perspect. Biol. 2(7), a000398 (2010).
103. Cirioni O, Giacometti A, Ghiselli R et al. RNAIII-inhibiting peptide significantly reduces bacterial load and enhances the effect of antibiotics in the treatment of central venous catheter-associated Staphylococcus aureus infections. J. Infect. Dis. 193(2), 180-186 (2006).
104. Kiran MD, Giacometti A, Cirioni O, Balaban N. Suppression of biofilm related, device-associated infections by staphylococcal quorum sensing inhibitors. Int. J. Artif. Organs 31(9), 761-770 (2008).
105. Dell'Acqua G, Giacometti A, Cirioni O et al. Suppression of drug-resistant staphylococcal infections by the quorum-sensing inhibitor RNAIII-inhibiting peptide. J. Infect. Dis. 190(2), 318-320 (2004).
106. Balaban N, Goldkorn T, Gov Y et al. Regulation of Staphylococcus aureus pathogenesis via target of RNAIII-activating protein (TRAP). J. Biol. Chem. 276(4), 2658-2667 (2001).
107. Giacometti A, Cirioni O, Gov Y et al. RNA III inhibiting peptide inhibits in vivo biofilm formation by drug-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47(6), 1979-1983 (2003).
108. Gov Y, Bitler A, Dell'Acqua G, Torres JV, Balaban N. RNAIII inhibiting peptide (RIP), a global inhibitor of Staphylococcus aureus pathogenesis: structure and function analysis. Peptides 22(10), 1609-1620 (2001).
109. Adhikari RP, Arvidson S, Novick RP. A nonsense mutation in agrA accounts for the defect in agr expression and the avirulence of Staphylococcus aureus 8325-4 traP::kan. Infect. Immun. 75(9), 4534-4540 (2007).
110. Shaw LN, Jonsson IM, Singh VK, Tarkowski A, Stewart GC. Inactivation of traP has no effect on the agr quorum-sensing system or virulence of Staphylococcus aureus. Infect. Immun. 75(9), 4519-4527 (2007).
111. Tsang LH, Daily ST, Weiss EC, Smeltzer MS. Mutation of traP in Staphylococcus aureus has no impact on expression of agr or biofilm formation. Infect. Immun. 75(9), 4528-4533 (2007).
112. O'Gara JP. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270(2), 179-188 (2007).
113. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199 (2001).
114. Xavier KB, Bassler BL. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6(2), 191-197 (2003).
115. Federle MJ. Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling. Contrib. Microbiol. 16, 18-32 (2009).
116. Vendeville A, Winzer K, Heurlier K, Tang CM, Hardie KR. Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3(5), 383-396 (2005).
117. Schauder S, Shokat K, Surette MG, Bassler BL. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41(2), 463-476 (2001).
118. Dalton HM, March PE. Molecular genetics of bacterial attachment and biofouling. Curr. Opin. Biotechnol. 9(3), 252-255 (1998).
119. Rimondini L, Fini M, Giardino R. The microbial infection of biomaterials: a challenge for clinicians and researchers. A short review. J. Appl. Biomater. Biomech. 3(1), 1-10 (2005).
120. Vuong C, Gerke C, Somerville GA, Fischer ER, Otto M. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J. Infect. Dis. 188(5), 706-718 (2003).
121. de Kievit TR. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11(2), 279-288 (2009).
122. Stranger-Jones YK, Bae T, Schneewind O. Vaccine assembly from surface proteins of Staphylococcus aureus. Proc. Natl Acad. Sci. USA 103(45), 16942-16947 (2006).
123. Scott CJ, McDowell A, Martin SL, Lynas JF, Vandenbroeck K, Walker B. Irreversible inhibition of the bacterial cysteine protease-transpeptidase sortase (SrtA) by substrate-derived affinity labels. Biochem. J. 366(Pt 3), 953-958 (2002).
124. Maresso AW, Schneewind O. Sortase as a target of anti-infective therapy. Pharmacol. Rev. 60(1), 128-141 (2008).
125. Laverty G, Gorman SP, Gilmore BF. The potential of antimicrobial peptides as biocides. Int. J. Mol. Sci. 12(10), 6566-6596 (2011).
126. Carson L, Chau PKW, Earle MJ et al. Antibiofilm activities of 1-alkyl-3- methylimidazolium chloride ionic liquids. Green Chem. 11, 492-497 (2009).
127. Fey PD, Olson ME. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol. 5(6), 917-933 (2010).
128. Montanaro L, Speziale P, Campoccia D et al. Scenery of Staphylococcus implant infections in orthopedics. Future Microbiol. 6(11), 1329-1349 (2011).
129. Veiga AS, Sinthuvanich C, Gaspar D, Franquelim HG, Castanho MA, Schneider JP. Arginine-rich self-assembling peptides as potent antibacterial gels. Biomaterials 33(35), 8907-8916 (2012).
130. Zelzer M, Todd SJ, Hirst AR, McDonald TO, Ulijn RV. Enzyme responsive materials: design strategies and future developments. Biomater. Sci. 1, 11-39 (2013).