Login Register Cart 0
Review Article

Current Understanding of Group A Streptococcal Biofilms

Author(s): Heema K.N. Vyas, Emma-Jayne Proctor, Jason McArthur, Jody Gorman and Martina Sanderson-Smith*

Volume 20, Issue 9, 2019

Page: [982 - 993] Pages: 12

DOI: 10.2174/1389450120666190405095712

Abstract

Background: It has been proposed that GAS may form biofilms. Biofilms are microbial communities that aggregate on a surface, and exist within a self-produced matrix of extracellular polymeric substances. Biofilms offer bacteria an increased survival advantage, in which bacteria persist, and resist host immunity and antimicrobial treatment. The biofilm phenotype has long been recognized as a virulence mechanism for many Gram-positive and Gram-negative bacteria, however very little is known about the role of biofilms in GAS pathogenesis.

Objective: This review provides an overview of the current knowledge of biofilms in GAS pathogenesis. This review assesses the evidence of GAS biofilm formation, the role of GAS virulence factors in GAS biofilm formation, modelling GAS biofilms, and discusses the polymicrobial nature of biofilms in the oropharynx in relation to GAS.

Conclusion: Further study is needed to improve the current understanding of GAS as both a monospecies biofilm, and as a member of a polymicrobial biofilm. Improved modelling of GAS biofilm formation in settings closely mimicking in vivo conditions will ensure that biofilms generated in the lab closely reflect those occurring during clinical infection.

Keywords: Streptococcus pyogenes, Group A Streptococcus, biofilms, biofilm formation, antibiotics, virulence factors, biofilm modelling, polymicrobial.

« Previous
Graphical Abstract

[1]
Manetti AG, Zingaretti C, Falugi F, et al. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 2007; 64(4): 968-83.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05704.x] [PMID: 17501921]
[2]
Walker MJ, Barnett TC, McArthur JD, et al. Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clin Microbiol Rev 2014; 27(2): 264-301.
[http://dx.doi.org/ 10.1128/CMR.00101-13] [PMID: 24696436]
[3]
Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis 2005; 5(11): 685-94.
[http://dx.doi.org/10.1016/S1473-3099(05)70267-X] [PMID: 16253886]
[4]
Baldassarri L, Creti R, Recchia S, et al. Therapeutic failures of antibiotics used to treat macrolide-susceptible Streptococcus pyogenes infections may be due to biofilm formation. J Clin Microbiol 2006; 44(8): 2721-7.
[http://dx.doi.org/10.1128/JCM.00512-06] [PMID: 16891483]
[5]
Conley J, Olson ME, Cook LS, Ceri H, Phan V, Davies HD. Biofilm formation by group a streptococci: is there a relationship with treatment failure? J Clin Microbiol 2003; 41(9): 4043-8.
[http://dx.doi.org/10.1128/JCM.41.9.4043-4048.2003] [PMID: 12958223]
[6]
Facinelli B, Spinaci C, Magi G, Giovanetti EE, Varaldo P. Association between erythromycin resistance and ability to enter human respiratory cells in group A streptococci. Lancet 2001; 358(9275): 30-3.
[http://dx.doi.org/10.1016/S0140-6736(00)05253-3] [PMID: 11454374]
[7]
Pichichero ME, Casey JR. Systematic review of factors contributing to penicillin treatment failure in Streptococcus pyogenes pharyngitis. Otolaryngol Head Neck Surg 2007; 137(6): 851-7.
[http://dx.doi.org/10.1016/j.otohns.2007.07.033] [PMID: 18036409]
[8]
Ogawa T, Terao Y, Okuni H, et al. Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microb Pathog 2011; 51(1-2): 58-68.
[http://dx.doi.org/10.1016/j.micpath. 2011.03.009] [PMID: 21443942]
[9]
Marks LR, Reddinger RM, Hakansson AP. Biofilm formation enhances fomite survival of Streptococcus pneumoniae and Streptococcus pyogenes. Infect Immun 2014; 82(3): 1141-6.
[http://dx.doi.org/10.1128/IAI.01310-13] [PMID: 24371220]
[10]
Speziale P, Geoghegan JA. Biofilm formation by staphylococci and streptococci: structural, functional, and regulatory aspects and implications for pathogenesis. Front Cell Infect Microbiol 2015; 5: 31.
[http://dx.doi.org/10.3389/fcimb.2015.00031] [PMID: 25905046]
[11]
Abee T, Kovács ÁT, Kuipers OP, van der Veen S. Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol 2011; 22(2): 172-9.
[http://dx.doi.org/10.1016/j.copbio.2010. 10.016] [PMID: 21109420]
[12]
Al-Wrafy F, Brzozowska E, Górska S, Gamian A. Pathogenic factors of Pseudomonas aeruginosa - the role of biofilm in pathogenicity and as a target for phage therapy. Postepy Hig Med Dosw 2017; 71(0): 78-91.
[http://dx.doi.org/10.5604/01.3001.0010.3792] [PMID: 28258668]
[13]
Kong C, Chee C-F, Richter K, Thomas N, Abd Rahman N, Nathan S. Suppression of Staphylococcus aureus biofilm formation and virulence by a benzimidazole derivative, UM-C162. Sci Rep 2018; 8(1): 2758.
[http://dx.doi.org/10.1038/s41598-018-21141-2] [PMID: 29426873]
[14]
Zalewska-Piatek BM, Wilkanowicz SI, Piatek RJ, Kur JW. Biofilm formation as a virulence determinant of uropathogenic Escherichia coli Dr+ strains. Pol J Microbiol 2009; 58(3): 223-9.
[PMID: 19899615]
[15]
Roberts AL, Connolly KL, Kirse DJ, et al. Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage. BMC Pediatr 2012; 12: 3.
[http://dx.doi.org/10.1186/1471-2431-12-3] [PMID: 22230361]
[16]
Siemens N, Chakrakodi B, Shambat SM, et al. Biofilm in group A streptococcal necrotizing soft tissue infections. JCI Insight 2016; 1(10): e87882.
[http://dx.doi.org/10.1172/jci.insight.87882] [PMID: 27699220]
[17]
Percival SL, Hill KE, Williams DW, Hooper SJ, Thomas DW, Costerton JW. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen 2012; 20(5): 647-57.
[http://dx.doi.org/10.1111/j.1524-475X.2012.00836.x] [PMID: 22985037]
[18]
Bjarnsholt T, Kirketerp-Møller K, Jensen PØ, et al. Why chronic wounds will not heal: A novel hypothesis. Wound Repair Regen 2008; 16(1): 2-10.
[http://dx.doi.org/10.1111/j.1524-475X.2007. 00283.x] [PMID: 18211573]
[19]
McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 2011; 10(1): 39-50.
[http://dx.doi.org/10.1038/nrmicro2695] [PMID: 22120588]
[20]
Rollet C, Gal L, Guzzo J. Biofilm-detached cells, a transition from a sessile to a planktonic phenotype: a comparative study of adhesion and physiological characteristics in Pseudomonas aeruginosa. FEMS Microbiol Lett 2009; 290(2): 135-42.
[http://dx.doi.org/ 10.1111/j.1574-6968.2008.01415.x] [PMID: 19054076]
[21]
Kostakioti M, Hadjifrangiskou M, Hultgren SJ. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med 2013; 3(4): a010306.
[http://dx.doi.org/10.1101/cshperspect.a010306] [PMID: 23545571]
[22]
Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis 2002; 8(9): 881-90.
[http://dx.doi.org/10.3201/eid0809.020063] [PMID: 12194761]
[23]
Shunmugaperumal T. Biofilm Eradication and Prevention: A Pharmaceutical Approach to Medical Device Infections 2010.
[http://dx.doi.org/10.1002/9780470640463]
[24]
O’Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998; 30(2): 295-304.
[http://dx.doi.org/10.1046/j.1365-2958.1998.01062.x] [PMID: 9791175]
[25]
Caiazza NC, Merritt JH, Brothers KM, O’Toole GA. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 2007; 189(9): 3603-12.
[http://dx.doi.org/10.1128/JB.01685-06] [PMID: 17337585]
[26]
Gloag ES, Turnbull L, Huang A, et al. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 2013; 110(28): 11541-6.
[http://dx.doi.org/10.1073/pnas.1218898110] [PMID: 23798445]
[27]
Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2012; 2(11): a012427.
[http://dx.doi.org/10.1101/cshperspect.a012427] [PMID: 23125205]
[28]
Wolcott RD, Rhoads DD, Dowd SE. Biofilms and chronic wound inflammation. J Wound Care 2008; 17(8): 333-41.
[http://dx.doi.org/10.12968/jowc.2008.17.8.30796] [PMID: 18754194]
[29]
Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker-Nielsen T. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 2005; 7(6): 894-906.
[http://dx.doi.org/10.1111/j.1462-2920.2005.00775.x] [PMID: 15892708]
[30]
Vickery K, Hu H, Jacombs AS, Bradshaw DA, Deva AK. A review of bacterial biofilms and their role in device-associated infection. Healthc Infect 2013; 18(2): 61-6.
[http://dx.doi.org/10.1071/HI12059]
[31]
Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2003; 2(2): 114-22.
[http://dx.doi.org/ 10.1038/nrd1008] [PMID: 12563302]
[32]
Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 1985; 27(4): 619-24.
[http://dx.doi.org/10.1128/AAC.27.4.619] [PMID: 3923925]
[33]
Prosser BL, Taylor D, Dix BA, Cleeland R. Method of evaluating effects of antibiotics on bacterial biofilm. Antimicrob Agents Chemother 1987; 31(10): 1502-6.
[http://dx.doi.org/10.1128/AAC. 31.10.1502] [PMID: 3435100]
[34]
Brown ML, Aldrich HC, Gauthier JJ. Relationship between glycocalyx and povidone-iodine resistance in Pseudomonas aeruginosa (ATCC 27853) biofilms. Appl Environ Microbiol 1995; 61(1): 187-93.
[PMID: 7887601]
[35]
Cowan T. Biofilms and their management: implications for the future of wound care. J Wound Care 2010; 19(3): 117-20.
[http://dx.doi.org/10.12968/jowc.2010.19.3.47281] [PMID: 20559189]
[36]
de la Fuente-Núñez C, Reffuveille F, Fernández L, Hancock REW. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 2013; 16(5): 580-9.
[http://dx.doi.org/10.1016/j.mib.2013.06.013] [PMID: 23880136]
[37]
Akiyama H, Morizane S, Yamasaki O, Oono T, Iwatsuki K. Assessment of Streptococcus pyogenes microcolony formation in infected skin by confocal laser scanning microscopy. J Dermatol Sci 2003; 32(3): 193-9.
[http://dx.doi.org/10.1016/S0923-1811(03) 00096-3] [PMID: 14507444]
[38]
Fiedler T, Riani C, Koczan D, Standar K, Kreikemeyer B, Podbielski A. Protective mechanisms of respiratory tract Streptococci against Streptococcus pyogenes biofilm formation and epithelial cell infection. Appl Environ Microbiol 2013; 79(4): 1265-76.
[http://dx.doi.org/10.1128/AEM.03350-12] [PMID: 23241973]
[39]
Lembke C, Podbielski A, Hidalgo-Grass C, Jonas L, Hanski E, Kreikemeyer B. Characterization of biofilm formation by clinically relevant serotypes of group A streptococci. Appl Environ Microbiol 2006; 72(4): 2864-75.
[http://dx.doi.org/10.1128/AEM.72.4. 2864-2875.2006] [PMID: 16597993]
[40]
Fiedler T, Köller T, Kreikemeyer B. Streptococcus pyogenes biofilms-formation, biology, and clinical relevance. Front Cell Infect Microbiol 2015; 5: 15.
[http://dx.doi.org/10.3389/fcimb.2015.00015] [PMID: 25717441]
[41]
Caparon MG, Stephens DS, Olsén A, Scott JR. Role of M protein in adherence of group A streptococci. Infect Immun 1991; 59(5): 1811-7.
[PMID: 2019444]
[42]
Ellen RP, Gibbons RJ. M protein-associated adherence of Streptococcus pyogenes to epithelial surfaces: prerequisite for virulence. Infect Immun 1972; 5(5): 826-30.
[PMID: 4564883]
[43]
Tylewska SK, Fischetti VA, Gibbons RJ. Binding selectivity of Streptococcus pyogenes and M-protein to epithelial cells differs from that of lipoteichoic acid. Curr Microbiol 1988; 16(4): 209-16.
[http://dx.doi.org/10.1007/BF01568531]
[44]
Cho KH, Caparon MG. Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Mol Microbiol 2005; 57(6): 1545-56.
[http://dx.doi.org/ 10.1111/j.1365-2958.2005.04786.x] [PMID: 16135223]
[45]
Courtney HS, Ofek I, Penfound T, et al. Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes. PLoS One 2009; 4(1): e4166.
[http://dx.doi.org/10.1371/journal. pone.0004166] [PMID: 19132104]
[46]
Podbielski A, Flosdorff A, Weber-Heynemann J. The group A streptococcal virR49 gene controls expression of four structural vir regulon genes. Infect Immun 1995; 63(1): 9-20.
[PMID: 7806389]
[47]
Kimura KR, Nakata M, Sumitomo T, et al. Involvement of T6 pili in biofilm formation by serotype M6 Streptococcus pyogenes. J Bacteriol 2012; 194(4): 804-12.
[http://dx.doi.org/10.1128/JB.06283-11] [PMID: 22155780]
[48]
Becherelli M, Manetti AG, Buccato S, et al. The ancillary protein 1 of Streptococcus pyogenes FCT-1 pili mediates cell adhesion and biofilm formation through heterophilic as well as homophilic interactions. Mol Microbiol 2012; 83(5): 1035-47.
[http://dx.doi.org/ 10.1111/j.1365-2958.2012.07987.x] [PMID: 22320452]
[49]
Oliver-Kozup HA, Elliott M, Bachert BA, et al. The streptococcal collagen-like protein-1 (Scl1) is a significant determinant for biofilm formation by group A Streptococcus. BMC Microbiol 2011; 11(1): 262.
[http://dx.doi.org/10.1186/1471-2180-11-262] [PMID: 22168784]
[50]
Bachert BA, Choi SJ, LaSala PR, et al. Unique Footprint in the scl1.3 Locus Affects Adhesion and Biofilm Formation of the Invasive M3-Type Group A Streptococcus. Front Cell Infect Microbiol 2016; 6: 90.
[http://dx.doi.org/10.3389/fcimb.2016.00090] [PMID: 27630827]
[51]
Sugareva V, Arlt R, Fiedler T, Riani C, Podbielski A, Kreikemeyer B. Serotype- and strain- dependent contribution of the sensor kinase CovS of the CovRS two-component system to Streptococcus pyogenes pathogenesis. BMC Microbiol 2010; 10(1): 34.
[http://dx.doi.org/10.1186/1471-2180-10-34] [PMID: 20113532]
[52]
Maddocks SE, Wright CJ, Nobbs AH, et al. Streptococcus pyogenes antigen I/II-family polypeptide AspA shows differential ligand-binding properties and mediates biofilm formation. Mol Microbiol 2011; 81(4): 1034-49.
[http://dx.doi.org/10.1111/j.1365-2958.2011.07749.x] [PMID: 21736640]
[53]
Doern CD, Holder RC, Reid SD. Point mutations within the streptococcal regulator of virulence (Srv) alter protein-DNA interactions and Srv function. Microbiology 2008; 154(Pt 7): 1998-2007.
[http://dx.doi.org/10.1099/mic.0.2007/013466-0] [PMID: 18599828]
[54]
Oliver-Kozup H, Martin KH, Schwegler-Berry D, et al. The group A streptococcal collagen-like protein-1, Scl1, mediates biofilm formation by targeting the extra domain A-containing variant of cellular fibronectin expressed in wounded tissue. Mol Microbiol 2013; 87(3): 672-89.
[http://dx.doi.org/10.1111/mmi.12125] [PMID: 23217101]
[55]
Aggarwal C, Jimenez JC, Nanavati D, Federle MJ. Multiple length peptide-pheromone variants produced by Streptococcus pyogenes directly bind Rgg proteins to confer transcriptional regulation. J Biol Chem 2014; 289(32): 22427-36.
[http://dx.doi.org/ 10.1074/jbc.M114.583989] [PMID: 24958729]
[56]
Jimenez JC, Federle MJ. Quorum sensing in group A Streptococcus. Front Cell Infect Microbiol 2014; 4: 127.
[http://dx.doi.org/10.3389/fcimb.2014.00127] [PMID: 25309879]
[57]
Thenmozhi R, Balaji K, Kumar R, Rao TS, Pandian SK. Characterization of biofilms in different clinical M serotypes of Streptococcus pyogenes. J Basic Microbiol 2011; 51(2): 196-204.
[http://dx.doi.org/10.1002/jobm.201000006] [PMID: 21298675]
[58]
Nakata M, Kimura KR, Sumitomo T, et al. Assembly mechanism of FCT region type 1 pili in serotype M6 Streptococcus pyogenes. J Biol Chem 2011; 286(43): 37566-77.
[http://dx.doi.org/ 10.1074/jbc.M111.239780] [PMID: 21880740]
[59]
Young C, Holder RC, Dubois L, Reid SD. Streptococcus pyogenes Biofilm 2016.
[60]
Köller T, Manetti AGO, Kreikemeyer B, et al. Typing of the pilus-protein-encoding FCT region and biofilm formation as novel parameters in epidemiological investigations of Streptococcus pyogenes isolates from various infection sites. J Med Microbiol 2010; 59(Pt 4): 442-52.
[http://dx.doi.org/10.1099/jmm.0.013581-0] [PMID: 20007764]
[61]
Falugi F, Zingaretti C, Pinto V, et al. Sequence variation in group A Streptococcus pili and association of pilus backbone types with lancefield T serotypes. J Infect Dis 2008; 198(12): 1834-41.
[http://dx.doi.org/10.1086/593176] [PMID: 18928376]
[62]
Kratovac Z, Manoharan A, Luo F, Lizano S, Bessen DE. Population genetics and linkage analysis of loci within the FCT region of Streptococcus pyogenes. J Bacteriol 2007; 189(4): 1299-310.
[http://dx.doi.org/10.1128/JB.01301-06] [PMID: 17028269]
[63]
Abbot EL, Smith WD, Siou GP, et al. Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol 2007; 9(7): 1822-33.
[http://dx.doi.org/10.1111/j.1462-5822.2007.00918.x] [PMID: 17359232]
[64]
Crotty Alexander LE, Maisey HC, Timmer AM, et al. M1T1 group A streptococcal pili promote epithelial colonization but diminish systemic virulence through neutrophil extracellular entrapment. J Mol Med (Berl) 2010; 88(4): 371-81.
[http://dx.doi.org/ 10.1007/s00109-009-0566-9] [PMID: 19960175]
[65]
Smith WD, Pointon JA, Abbot E, et al. Roles of minor pilin subunits Spy0125 and Spy0130 in the serotype M1 Streptococcus pyogenes strain SF370. J Bacteriol 2010; 192(18): 4651-9.
[http://dx.doi.org/10.1128/JB.00071-10] [PMID: 20639332]
[66]
Manetti AGO, Köller T, Becherelli M, et al. Environmental acidification drives S. pyogenes pilus expression and microcolony formation on epithelial cells in a FCT-dependent manner. PLoS One 2010; 5(11): e13864.
[http://dx.doi.org/10.1371/journal.pone. 0013864] [PMID: 21079780]
[67]
Lukomski S, Nakashima K, Abdi I, et al. Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect Immun 2000; 68(12): 6542-53.
[http://dx.doi.org/ 10.1128/IAI.68.12.6542-6553.2000] [PMID: 11083763]
[68]
Xu Y, Keene DR, Bujnicki JM, Höök M, Lukomski S. Streptococcal Scl1 and Scl2 proteins form collagen-like triple helices. J Biol Chem 2002; 277(30): 27312-8.
[http://dx.doi.org/10.1074/jbc.M201163200] [PMID: 11976327]
[69]
Flores AR, Jewell BE, Versalovic EM, et al. Natural variant of collagen-like protein a in serotype M3 group a Streptococcus increases adherence and decreases invasive potential. Infect Immun 2015; 83(3): 1122-9.
[http://dx.doi.org/10.1128/IAI.02860-14] [PMID: 25561712]
[70]
Stoolmiller AC, Dorfman A. The biosynthesis of hyaluronic acid by Streptococcus. J Biol Chem 1969; 244(2): 236-46.
[PMID: 5773295]
[71]
Cywes C, Stamenkovic I, Wessels MR. CD44 as a receptor for colonization of the pharynx by group A Streptococcus. J Clin Invest 2000; 106(8): 995-1002.
[http://dx.doi.org/10.1172/JCI10195] [PMID: 11032859]
[72]
Schrager HM, Albertí S, Cywes C, Dougherty GJ, Wessels MR. Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of group A Streptococcus to CD44 on human keratinocytes. J Clin Invest 1998; 101(8): 1708-16.
[http://dx.doi.org/10.1172/JCI2121] [PMID: 9541502]
[73]
Bartelt MA, Duncan JL. Adherence of group A streptococci to human epithelial cells. Infect Immun 1978; 20(1): 200-8.
[PMID: 352928]
[74]
Henningham A, Yamaguchi M, Aziz RK, et al. Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus. J Biol Chem 2014; 289(46): 32303-15.
[http://dx.doi.org/ 10.1074/jbc.M114.602847] [PMID: 25266727]
[75]
Connolly KL, Roberts AL, Holder RC, Reid SD. Dispersal of Group A streptococcal biofilms by the cysteine protease SpeB leads to increased disease severity in a murine model. PLoS One 2011; 6(4): e18984.
[http://dx.doi.org/10.1371/journal.pone.0018984] [PMID: 21547075]
[76]
Doern CD, Roberts AL, Hong W, et al. Biofilm formation by group A Streptococcus: a role for the streptococcal regulator of virulence (Srv) and streptococcal cysteine protease (SpeB). Microbiology 2009; 155(Pt 1): 46-52.
[http://dx.doi.org/10.1099/mic.0.021048-0] [PMID: 19118345]
[77]
Reid SD, Chaussee MS, Doern CD, et al. Inactivation of the group A Streptococcus regulator srv results in chromosome wide reduction of transcript levels, and changes in extracellular levels of Sic and SpeB. FEMS Immunol Med Microbiol 2006; 48(2): 283-92.
[http://dx.doi.org/10.1111/j.1574-695X.2006.00150.x] [PMID: 16999824]
[78]
Belotserkovsky I, Baruch M, Peer A, et al. Functional analysis of the quorum-sensing streptococcal invasion locus (sil). PLoS Pathog 2009; 5(11): e1000651.
[http://dx.doi.org/10.1371/journal.ppat. 1000651] [PMID: 19893632]
[79]
Lembke C, Podbielski A, Hidalgo-Grass C, Jonas L, Hanski E, Kreikemeyer B. Characterization of biofilm formation by clinically relevant serotypes of group A streptococci. Appl Environ Microbiol 2006; 72(4): 2864-75.
[http://dx.doi.org/10.1128/AEM.72.4. 2864-2875.2006] [PMID: 16597993]
[80]
Chang JC, LaSarre B, Jimenez JC, Aggarwal C, Federle MJ. Two group A streptococcal peptide pheromones act through opposing Rgg regulators to control biofilm development. PLoS Pathog 2011; 7(8): e1002190.
[http://dx.doi.org/10.1371/journal.ppat.1002190] [PMID: 21829369]
[81]
Cook LC, LaSarre B, Federle MJ. Interspecies communication among commensal and pathogenic streptococci. MBio 2013; 4(4): e00382-13.
[http://dx.doi.org/10.1128/mBio.00382-13] [PMID: 23882015]
[82]
Beema Shafreen RM, Selvaraj C, Singh SK, Karutha Pandian S. In silico and in vitro studies of cinnamaldehyde and their derivatives against LuxS in Streptococcus pyogenes: effects on biofilm and virulence genes. J Mol Recognit 2014; 27(2): 106-16.
[http://dx.doi.org/10.1002/jmr.2339] [PMID: 24436128]
[83]
Lyon WR, Madden JC, Levin JC, Stein JL, Caparon MG. Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 2001; 42(1): 145-57.
[http://dx.doi.org/10.1046/j.1365-2958.2001.02616.x] [PMID: 11679074]
[84]
Marouni MJ, Sela S. The luxS gene of Streptococcus pyogenes regulates expression of genes that affect internalization by epithelial cells. Infect Immun 2003; 71(10): 5633-9.
[http://dx.doi.org/ 10.1128/IAI.71.10.5633-5639.2003] [PMID: 14500483]
[85]
Siller M, Janapatla RP, Pirzada ZA, Hassler C, Zinkl D, Charpentier E. Functional analysis of the group A streptococcal luxS/AI-2 system in metabolism, adaptation to stress and interaction with host cells. BMC Microbiol 2008; 8: 188.
[http://dx.doi.org/10.1186/1471-2180-8-188] [PMID: 18973658]
[86]
Zobell CE. The Effect of Solid Surfaces upon Bacterial Activity. J Bacteriol 1943; 46(1): 39-56.
[PMID: 16560677]
[87]
Håkansson A, Bentley CC, Shakhnovic EA, Wessels MR. Cytolysin-dependent evasion of lysosomal killing. Proc Natl Acad Sci USA 2005; 102(14): 5192-7.
[http://dx.doi.org/10.1073/pnas.0408721102] [PMID: 15795386]
[88]
Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol 2010; 192(19): 5002-17.
[http://dx.doi.org/10.1128/JB.00542-10] [PMID: 20656903]
[89]
Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. MBio 2010; 1(3): e00129-10.
[http://dx.doi.org/10.1128/mBio.00129-10] [PMID: 20802827]
[90]
Gao Z, Kang Y, Yu J, Ren L. Human pharyngeal microbiome may play a protective role in respiratory tract infections. Genomics Proteomics Bioinformatics 2014; 12(3): 144-50.
[http://dx.doi.org/ 10.1016/j.gpb.2014.06.001] [PMID: 24953866]
[91]
Anderson DJ, Richet H, Chen LF, et al. Seasonal variation in Klebsiella pneumoniae bloodstream infection on 4 continents. J Infect Dis 2008; 197(5): 752-6.
[http://dx.doi.org/10.1086/527486] [PMID: 18260762]
[92]
Mertz D, Frei R, Jaussi B, et al. Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis 2007; 45(4): 475-7.
[http://dx.doi.org/10.1086/520016] [PMID: 17638197]
[93]
Widmer AF, Mertz D, Frei R. Necessity of screening of both the nose and the throat to detect methicillin-resistant Staphylococcus aureus colonization in patients upon admission to an intensive care unit. J Clin Microbiol 2008; 46(2): 835.
[http://dx.doi.org/10.1128/JCM.02276-07] [PMID: 18252860]
[94]
Lafontaine ER, Wall D, Vanlerberg SL, Donabedian H, Sledjeski DD. Moraxella catarrhalis coaggregates with Streptococcus pyogenes and modulates interactions of S. pyogenes with human epithelial cells. Infect Immun 2004; 72(11): 6689-93.
[http://dx.doi.org/10.1128/IAI.72.11.6689-6693.2004] [PMID: 15501804]
[95]
Federle MJ, Bassler BL. Interspecies communication in bacteria. J Clin Invest 2003; 112(9): 1291-9.
[http://dx.doi.org/10.1172/JCI20195] [PMID: 14597753]
[96]
Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol 2002; 56: 187-209.
[http://dx.doi.org/10.1146/annurev.micro.56.012302.160705] [PMID: 12142477]
[97]
Suntharalingam P, Cvitkovitch DG. Quorum sensing in streptococcal biofilm formation. Trends Microbiol 2005; 13(1): 3-6.
[http://dx.doi.org/10.1016/j.tim.2004.11.009] [PMID: 15639624]
[98]
Wolcott R, Costerton JW, Raoult D, Cutler SJ. The polymicrobial nature of biofilm infection. Clin Microbiol Infect 2013; 19(2): 107-12.
[http://dx.doi.org/10.1111/j.1469-0691.2012.04001.x] [PMID: 22925473]

Rights & Permissions Print Cite
Article Metrics
54
10
© 2024 Bentham Science Publishers | Privacy Policy