Biofilm Formation Mechanisms and Targets for Developing Antibiofilm Agents

References

• Henrici AT . Studies of freshwater bacteria: I. A direct microscopic technique. J. Bacteriol.25 (3), 277–287 (1933).
   PubMedGoogle Scholar
• Heukelekian H , HellerA. Relation between food concentration and surface for bacterial growth. J. Bacteriol.40 (4), 547–558 (1940).
   PubMedGoogle Scholar
• Hoiby N , FlensborgE, BeckB, FriisB, JacobsenS, JacobsenL. Pseudomonas aeruginosa infection in cystic fibrosis. Diagnostic and prognostic significance of Pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis. Scand. J. Respir. Dis.58 (2), 65–79 (1977).
   PubMedGoogle Scholar
• Costerton JW , GeeseyGG, ChengKJ. How bacteria stick. Sci. Am.238 (1), 86–95 (1978).
   PubMed Web of Science ®Google Scholar
• Deligianni E , PattisonS, BerrarDet al. Pseudomonas aeruginosa cystic fibrosis isolates of similar RAPD genotype exhibit diversity in biofilm forming ability in vitro. BMC Microbiol.10, 38 (2010).
   PubMed Web of Science ®Google Scholar
• Ludecke C , JandtKD, SiegismundDet al. Reproducible biofilm cultivation of chemostat-grown Escherichia coli and investigation of bacterial adhesion on biomaterials using a non-constant-depth film fermenter. PLoS One9 (1), e84837 (2014).
   PubMed Web of Science ®Google Scholar
• Thurlow LR , HankeML, FritzTet al. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol.186 (11), 6585–6596 (2011).
   PubMed Web of Science ®Google Scholar
• Pammi M , LiangR, HicksJM, BarrishJ, VersalovicJ. Farnesol decreases biofilms of Staphylococcus epidermidis and exhibits synergy with nafcillin and vancomycin. Pediatr. Res.70 (6), 578–583 (2011).
   PubMed Web of Science ®Google Scholar
• Annous BA , FratamicoPM, SmithJL. Scientific status summary. J. Food Sci.74 (1), R24–R37 (2009).
   PubMed Web of Science ®Google Scholar
• Metwalli KH , KhanSA, KromBP, Jabra-RizkMA. Streptococcus mutans candida albicans and the human mouth: a sticky situation. PLoS Pathog.9 (10), e1003616 (2013).
   PubMed Web of Science ®Google Scholar
• Flemming HC , NeuTR, WozniakDJ. The EPS matrix: the “house of biofilm cells”. J. Bacteriol.189 (22), 7945–7947 (2007).
   PubMed Web of Science ®Google Scholar
• Zhang X , BishopPL, KupferleMJ. Measurement of polysaccharides and proteins in biofilm extracellular polymers. Water Sci. Technol.37 (45), 345–348 (1998).
   Google Scholar
• Nwodo UU , GreenE, OkohAI. Bacterial exopolysaccharides: functionality and prospects. Int. J. Mol. Sci.13 (11), 14002–14015 (2012).
   PubMed Web of Science ®Google Scholar
• Dawson LF , ValienteE, Faulds-PainA, DonahueEH, WrenBW. Characterisation of clostridium difficile biofilm formation, a role for Spo0A. PLoS One7 (12), e50527 (2012).
   PubMed Web of Science ®Google Scholar
• Bales PM , RenkeEM, MaySL, ShenY, NelsonDC. Purification and characterization of biofilm-associated EPS exopolysaccharides from ESKAPE organisms and other pathogens. PLoS One8 (6), e67950 (2013).
   PubMed Web of Science ®Google Scholar
• Prigent-Combaret C , VidalO, DorelC, LejeuneP. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol.181 (19), 5993–6002 (1999).
   PubMed Web of Science ®Google Scholar
• Davies DG , GeeseyGG. Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl. Environ. Microbiol.61 (3), 860–867 (1995).
   PubMed Web of Science ®Google Scholar
• Grant WD , SutherlandIW, WilkinsonJF. Exopolysaccharide colanic acid and its occurrence in the Enterobacteriaceae. J. Bacteriol.100 (3), 1187–1193 (1969).
   PubMed Web of Science ®Google Scholar
• Stevenson G , AndrianopoulosK, HobbsM, ReevesPR. Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J. Bacteriol.178 (16), 4885–4893 (1996).
   PubMed Web of Science ®Google Scholar
• Reid AN , WhitfieldC. Functional analysis of conserved gene products involved in assembly of Escherichia coli capsules and exopolysaccharides: evidence for molecular recognition between Wza and Wzc for colanic acid biosynthesis. J. Bacteriol.187 (15), 5470–5481 (2005).
   PubMed Web of Science ®Google Scholar
• Danese PN , PrattLA, KolterR. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol.182 (12), 3593–3596 (2000).
   PubMed Web of Science ®Google Scholar
• Friedman L , KolterR. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol.51 (3), 675–690 (2004).
   PubMed Web of Science ®Google Scholar
• Friedman L , KolterR. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol.186 (14), 4457–4465 (2004).
   PubMed Web of Science ®Google Scholar
• Jackson KD , StarkeyM, KremerS, ParsekMR, WozniakDJ. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol.186 (14), 4466–4475 (2004).
   PubMed Web of Science ®Google Scholar
• May TB , ShinabargerD, MaharajRet al. Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin. Microbiol. Rev.4 (2), 191–206 (1991).
   PubMed Web of Science ®Google Scholar
• Hodges NA , GordonCA. Protection of Pseudomonas aeruginosa against ciprofloxacin and beta-lactams by homologous alginate. Antimicrob. Agents Chemother.35 (11), 2450–2452 (1991).
   PubMed Web of Science ®Google Scholar
• Simpson JA , SmithSE, DeanRT. Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages. J. Gen. Microbiol.134 (1), 29–36 (1988).
   PubMedGoogle Scholar
• Ma L , WangJ, WangSet al. Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post-transcriptionally regulated. Environ. Microbiol.14 (8), 1995–2005 (2012).
   PubMed Web of Science ®Google Scholar
• Coyne MJ , RussellKS, CoyleCL, GoldbergJB. The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase, required for the synthesis of a complete lipopolysaccharide core. J. Bacteriol.176 (12), 3500–3507 (1994).
   PubMed Web of Science ®Google Scholar
• Colvin KM , IrieY, TartCSet al. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol.14 (8), 1913–1928 (2012).
   PubMed Web of Science ®Google Scholar
• Franklin MJ , NivensDE, WeadgeJT, HowellPL. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol.2, 167 (2011).
   PubMed Web of Science ®Google Scholar
• Gacesa P . Bacterial alginate biosynthesis – recent progress and future prospects. Microbiology144 (5), 1133–1143 (1998).
   PubMedGoogle Scholar
• Stokke BT , DragetKI, Smidsr⊘dO, YuguchiY, UrakawaH, KajiwaraK. Small-angle X-ray scattering and rheological characterization of alginate Gels. 1. Ca-Alginate Gels. Macromolecules33 (5), 1853–1863 (2000).
   Web of Science ®Google Scholar
• Mack D , FischerW, KrokotschAet al. 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 (1), 175–183 (1996).
   PubMed Web of Science ®Google Scholar
• Cue DR , LeiMG, LeeC. Genetic regulation of the intercellular adhesion locus in staphylococci. Front. Cell. Infect. Microbiol.2, 38 (2012).
   PubMed Web of Science ®Google Scholar
• Stanley NR , LazazzeraBA. Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-dl-glutamic acid production and biofilm formation. Mol. Microbiol.57 (4), 1143–1158 (2005).
   PubMed Web of Science ®Google Scholar
• Branda SS , ChuF, KearnsDB, LosickR, KolterR. A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol.59 (4), 1229–1238 (2006).
   PubMed Web of Science ®Google Scholar
• Fr⊘lund B , PalmgrenR, KeidingK, NielsenPH. Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res.30 (8), 1749–1758 (1996).
   Web of Science ®Google Scholar
• Lynch DJ , FountainTL, MazurkiewiczJE, BanasJA. Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol. Lett.268 (2), 158–165 (2007).
   PubMed Web of Science ®Google Scholar
• Dueholm MS , S⊘ndergaardMT, NilssonMet al. Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen2 (3), 365–382 (2013).
   PubMed Web of Science ®Google Scholar
• Romero D , AguilarC, LosickR, KolterR. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. USA107 (5), 2230–2234 (2010).
   PubMed Web of Science ®Google Scholar
• Cucarella C , SolanoC, ValleJ, AmorenaB, LasaI, PenadésJR. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol.183 (9), 2888–2896 (2001).
   PubMed Web of Science ®Google Scholar
• Toledo-Arana A , ValleJ, SolanoCet al. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol.67 (10), 4538–4545 (2001).
   PubMed Web of Science ®Google Scholar
• Lasa I , PenadésJR. Bap: a family of surface proteins involved in biofilm formation. Res. Microbiol.157 (2), 99–107 (2006).
   PubMed Web of Science ®Google Scholar
• Mora P , RosconiF, Franco FraguasL, Castro-Sowinski S. Azospirillum brasilense Sp7 produces an outer-membrane lectin that specifically binds to surface-exposed extracellular polysaccharide produced by the bacterium. Arch. Microbiol.189 (5), 519–524 (2008).
   PubMed Web of Science ®Google Scholar
• Diggle SP , StaceyRE, DoddC, CámaraM, WilliamsP, WinzerK. The galactophilic lectin, LecA, contributes to biofilm development in Pseudomonas aeruginosa. Environ. Microbiol.8 (6), 1095–1104 (2006).
   PubMed Web of Science ®Google Scholar
• Tielker D , HackerS, LorisRet al. Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology151 (5), 1313–1323 (2005).
   PubMedGoogle Scholar
• Zhang X , BishopPL. Biodegradability of biofilm extracellular polymeric substances. Chemosphere50 (1), 63–69 (2003).
   PubMed Web of Science ®Google Scholar
• Kaplan JB , VelliyagounderK, RagunathCet al. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol.186 (24), 8213–8220 (2004).
   PubMed Web of Science ®Google Scholar
• Whitchurch CB , Tolker-NielsenT, RagasPC, MattickJS. Extracellular DNA required for bacterial biofilm formation. Science295 (5559), 1487 (2002).
   PubMed Web of Science ®Google Scholar
• Hamilton HL , DomínguezNM, SchwartzKJ, HackettKT, DillardJP. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol.55 (6), 1704–1721 (2005).
   PubMed Web of Science ®Google Scholar
• Das T , SharmaPK, BusscherHJ, van der MeiHC, KromBP. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl. Environ. Microbiol.76 (10), 3405–3408 (2010).
   PubMed Web of Science ®Google Scholar
• Gloag ES , TurnbullL, HuangAet al. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc. Natl. Acad. Sci. USA110 (28), 11541–11546 (2013).
   PubMed Web of Science ®Google Scholar
• Lewenza S . Extracellular DNA-induced antimicrobial peptide resistance mechanisms in Pseudomonas aeruginosa. Front. Microbiol.4, 21 (2013).
   PubMed Web of Science ®Google Scholar
• Mulcahy H , Charron-MazenodL, LewenzaS. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog.4 (11), e1000213 (2008).
   PubMed Web of Science ®Google Scholar
• Johnson L , HorsmanSR, Charron-MazenodLet al. Extracellular DNA-induced antimicrobial peptide resistance in Salmonella enterica serovar Typhimurium. BMC Microbiol.13, 115 (2013).
   PubMed Web of Science ®Google Scholar
• Doroshenko N , TsengBS, HowlinRPet al. Extracellular DNA impedes the transport of vancomycin in Staphylococcus epidermidis biofilms pre-exposed to sub-inhibitory concentrations of vancomycin. Antimicrob. Agents Chemother.58 (12), 7273–7282 (2014).
   PubMed Web of Science ®Google Scholar
• Otto M . Staphylococcus epidermidis Pathogenesis. Methods Mol. Biol.1106, 17–31 (2014).
   PubMedGoogle Scholar
• Barnes AMT , BalleringKS, LeibmanRS, WellsCL, DunnyGM. Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. MBio.3 (4), e00193–12 (2012).
   PubMed Web of Science ®Google Scholar
• Jefferson KK . What drives bacteria to produce a biofilm?FEMS Microbiol. Lett.236 (2), 163–173 (2004).
   PubMed Web of Science ®Google Scholar
• Rasmussen TB , GivskovM. Quorum-sensing inhibitors as anti-pathogenic drugs. Int. J. Med. Microbiol.296 (23), 149–161 (2006).
   PubMedGoogle Scholar
• Hausner M , WuertzS. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol.65 (8), 3710–3713 (1999).
   PubMed Web of Science ®Google Scholar
• Palmer J , FlintS, BrooksJ. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biotechnol.34 (9), 577–588 (2007).
   PubMed Web of Science ®Google Scholar
• Renner LD , WeibelDB. Physicochemical regulation of biofilm formation. MRS Bull.36 (5), 347–355 (2011).
   Web of Science ®Google Scholar
• Sutherland I . Biofilm exopolysaccharides: a strong and sticky framework. Microbiology147 (1), 3–9 (2001).
   PubMed Web of Science ®Google Scholar
• O'Toole GA , KolterR. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol.30 (2), 295–304 (1998).
   PubMed Web of Science ®Google Scholar
• Otto M . Staphylococcal biofilms. Curr. Top. Microbiol. Immunol.207–228 (2008).
   PubMed Web of Science ®Google Scholar
• Heilmann C , HussainM, PetersG, GötzF. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol.24 (5), 1013–1024 (1997).
   PubMed Web of Science ®Google Scholar
• Davies DG , ChakrabartyAM, GeeseyGG. Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl. Environ. Microbiol.59 (4), 1181–1186 (1993).
   PubMed Web of Science ®Google Scholar
• Garrett ES , PerlegasD, WozniakDJ. Negative control of flagellum synthesis in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU). J. Bacteriol.181 (23), 7401–7404 (1999).
   PubMed Web of Science ®Google Scholar
• Hall MR , McGillicuddyE, KaplanLJ. Biofilm: basic principles, pathophysiology, and implications for clinicians. Surg. Infect. (Larchmt.)15 (1), 1–7 (2014).
   PubMed Web of Science ®Google Scholar
• Fux CA , CostertonJW, StewartPS, StoodleyP. Survival strategies of infectious biofilms. Trends Microbiol.13 (1), 34–40 (2005).
   PubMed Web of Science ®Google Scholar
• Davies D . Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov.2 (2), 114–122 (2003).
   PubMed Web of Science ®Google Scholar
• Lyczak JB , CannonCL, PierGB. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev.15 (2), 194–222 (2002).
   PubMed Web of Science ®Google Scholar
• Pedersen SS , KochC, H⊘ibyN, RosendalK. An epidemic spread of multiresistant Pseudomonas aeruginosa in a cystic fibrosis centre. J. Antimicrob. Chemother.17 (4), 505–516 (1986).
   PubMed Web of Science ®Google Scholar
• Jones AM , GovanJR, DohertyCJet al. Spread of a multiresistant strain of Pseudomonas aeruginosa in an adult cystic fibrosis clinic. Lancet358 (9281), 557–558 (2001).
   PubMed Web of Science ®Google Scholar
• Römling U , FiedlerB, BosshammerJet al. Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J. Infect. Dis.170 (6), 1616–1621 (1994).
   PubMed Web of Science ®Google Scholar
• Costerton JW , StewartPS, GreenbergEP. Bacterial biofilms: a common cause of persistent infections. Science284 (5418), 1318–1322 (1999).
   PubMed Web of Science ®Google Scholar
• Moreau-Marquis S , StantonBA, O'TooleGA. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm. Pharmacol. Ther.21 (4), 595–599 (2008).
   PubMed Web of Science ®Google Scholar
• Pedersen SS , H⊘ibyN, EspersenF, KochC. Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax47 (1), 6–13 (1992).
   PubMed Web of Science ®Google Scholar
• Hojo K , NagaokaS, OhshimaT, MaedaN. Bacterial interactions in dental biofilm development. J. Dent. Res.88 (11), 982–990 (2009).
   PubMed Web of Science ®Google Scholar
• Marsh PD . Dental plaque as a microbial biofilm. Caries Res.38 (3), 204–211 (2004).
   PubMed Web of Science ®Google Scholar
• Marsh PD . Dental plaque as a biofilm and a microbial community – implications for health and disease. BMC Oral Health6 (Suppl 1), 14 (2006).
   PubMedGoogle Scholar
• Zaura E , KeijserB, HuseS, CrielaardW. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol.9 (1), 259 (2009).
   PubMedGoogle Scholar
• Li J , HelmerhorstEJ, LeoneCWet al. Identification of early microbial colonizers in human dental biofilm. J. Appl. Microbiol.97 (6), 1311–1318 (2004).
   PubMed Web of Science ®Google Scholar
• Marquis RE . Oxygen metabolism, oxidative stress and acid–base physiology of dental plaque biofilms. J. Ind. Microbiol.15 (3), 198–207 (1995).
   PubMedGoogle Scholar
• Sbordone L , BortolaiaC. Oral microbial biofilms and plaque-related diseases: microbial communities and their role in the shift from oral health to disease. Clin. Oral Investig.7 (4), 181–188 (2003).
   PubMed Web of Science ®Google Scholar
• Dige I , NilssonH, KilianM, NyvadB. In situ identification of streptococci and other bacteria in initial dental biofilm by confocal laser scanning microscopy and fluorescence in situ hybridization. Eur. J. Oral Sci.115 (6), 459–467 (2007).
   PubMed Web of Science ®Google Scholar
• Dige I , RaarupMK, NyengaardJR, KilianM, NyvadB. Actinomyces naeslundii in initial dental biofilm formation. Microbiology155 (7), 2116–2126 (2009).
   PubMed Web of Science ®Google Scholar
• Kolenbrander PE , PalmerRJJr, PeriasamyS, JakubovicsNS. Oral multispecies biofilm development and the key role of cell–cell distance. Nat. Rev. Micro.8 (7), 471–480 (2010).
   PubMed Web of Science ®Google Scholar
• Hardie KR , HeurlierK. Establishing bacterial communities by ‘word of mouth’: LuxS and autoinducer 2 in biofilm development. Nat. Rev. Micro.6 (8), 635–643 (2008).
   PubMed Web of Science ®Google Scholar
• Bassler BL , GreenbergEP, StevensAM. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol.179 (12), 4043–4045 (1997).
   PubMed Web of Science ®Google Scholar
• James GA , SwoggerE, WolcottRet al. Biofilms in chronic wounds. Wound Repair Regen.16 (1), 37–44 (2008).
   PubMed Web of Science ®Google Scholar
• Tenke P , KovacsB, JäckelM, NagyE. The role of biofilm infection in urology. World J. Urol.24 (1), 13–20 (2006).
   PubMed Web of Science ®Google Scholar
• Jacobsen SM , SticklerDJ, MobleyHL, ShirtliffME. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev.21 (1), 26–59 (2008).
   PubMed Web of Science ®Google Scholar
• Matthews PC , BerendtAR, McNallyMA, ByrenI. Diagnosis and management of prosthetic joint infection. BMJ338, b1773 (2009).
   PubMed Web of Science ®Google Scholar
• Trampuz A , ZimmerliW. Prosthetic joint infections: update in diagnosis and treatment. Swiss Med. Wkly.135 (1718), 243–251 (2005).
   PubMedGoogle Scholar
• Khardori N , YassienM. Biofilms in device-related infections. J. Ind. Microbiol.15 (3), 141–147 (1995).
   PubMedGoogle Scholar
• Costerton JW , LewandowskiZ, CaldwellDE, KorberDR, Lappin-ScottHM. Microbial Biofilms. Annu. Rev. Microbiol.49 (1), 711–745 (1995).
   PubMed Web of Science ®Google Scholar
• Nickel JC , RuseskaI, WrightJB, CostertonJW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob. Agents Chemother.27 (4), 619–624 (1985).
   PubMed Web of Science ®Google Scholar
• Luppens SB , ReijMW, van der HeijdenRW, RomboutsFM, AbeeT. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl. Environ. Microbiol.68 (9), 4194–4200 (2002).
   PubMed Web of Science ®Google Scholar
• Suci PA , MittelmanMW, YuFP, GeeseyGG. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother.38 (9), 2125–2133 (1994).
   PubMed Web of Science ®Google Scholar
• Anderl JN , FranklinMJ, StewartPS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother.44 (7), 1818–1824 (2000).
   PubMed Web of Science ®Google Scholar
• Savage VJ , ChopraI, O'NeillAJ. Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrob. Agents Chemother.57 (4), 1968–1970 (2013).
   PubMed Web of Science ®Google Scholar
• Ashby MJ , NealeJE, KnottSJ, CritchleyIA. Effect of antibiotics on non-growing planktonic cells and biofilms of Escherichia coli. J. Antimicrob. Chemother.33 (3), 443–452 (1994).
   PubMed Web of Science ®Google Scholar
• Lewis K . Persister cells, dormancy and infectious disease. Nat. Rev. Microbiol.5 (1), 48–56 (2007).
   PubMed Web of Science ®Google Scholar
• Keren I , ShahD, SpoeringA, KaldaluN, LewisK. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol.186 (24), 8172–8180 (2004).
   PubMed Web of Science ®Google Scholar
• Zhang L , MahTF. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol.190 (13), 4447–4452 (2008).
   PubMed Web of Science ®Google Scholar
• Leid JG , WillsonCJ, ShirtliffME, HassettDJ, ParsekMR, JeffersAK. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J. Immunol.175 (11), 7512–7518 (2005).
   PubMed Web of Science ®Google Scholar
• Lyon GJ , MuirTW. Chemical signaling among bacteria and its inhibition. Chem. Biol.10 (11), 1007–1021 (2003).
   PubMedGoogle Scholar
• West SA , WinzerK, GardnerA, DiggleSP. Quorum sensing and the confusion about diffusion. Trends Microbiol.20 (12), 586–594 (2012).
   PubMed Web of Science ®Google Scholar
• Camilli A , BasslerBL. Bacterial small-molecule signaling pathways. Science311 (5764), 1113–1116 (2006).
   PubMed Web of Science ®Google Scholar
• Rezzonico F , DuffyB. Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol.8 (1), 154 (2008).
   PubMedGoogle Scholar
• Miller MB , BasslerBL. Quorum sensing in bacteria. Annu. Rev. Microbiol.55 (1), 165–199 (2001).
   PubMed Web of Science ®Google Scholar
• Romeo T , IrieY, ParsekMR. Quorum sensing and microbial biofilms. Curr. Top. Microbiol. Immunol. 67–84 (2008).
   Web of Science ®Google Scholar
• Allesen-Holm M , BarkenKB, YangLet al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol.59 (4), 1114–1128 (2006).
   PubMed Web of Science ®Google Scholar
• Sakuragi Y , KolterR. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J. Bacteriol.189 (14), 5383–5386 (2007).
   PubMed Web of Science ®Google Scholar
• Boles BR , HorswillAR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog.4 (4), e1000052 (2008).
   PubMed Web of Science ®Google Scholar
• Novick RP , GeisingerE. Quorum sensing in staphylococci. Annu. Rev. Genet.42, 541–564 (2008).
   PubMed Web of Science ®Google Scholar
• López D , FischbachMA, ChuF, LosickR, KolterR. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl Acad. Sci. USA106 (1), 280–285 (2009).
   PubMed Web of Science ®Google Scholar
• Weinhouse H , SapirS, AmikamDet al. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett.416 (2), 207–211 (1997).
   PubMed Web of Science ®Google Scholar
• Ross P , MayerR, WeinhouseHet al. The cyclic diguanylic acid regulatory system of cellulose synthesis in Acetobacter xylinum chemical synthesis and biological activity of cyclic nucleotide dimer, trimer, and phosphothioate derivatives. J. Biol. Chem.265 (31), 18933–18943 (1990).
   PubMed Web of Science ®Google Scholar
• Kalia D , MereyG, NakayamaSet al. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis. Chem. Soc. Rev.42 (1), 305–341 (2013).
   PubMed Web of Science ®Google Scholar
• Ross P , WeinhouseH, AloniYet al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature325 (6101), 279–281 (1987).
   PubMed Web of Science ®Google Scholar
• Ryjenkov DA , TarutinaM, MoskvinOV, GomelskyM. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol.187 (5), 1792–1798 (2005).
   PubMed Web of Science ®Google Scholar
• Paul R , WeiserS, AmiotNCet al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev.18 (6), 715–727 (2004).
   PubMed Web of Science ®Google Scholar
• Tischler AD , CamilliA. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun.73 (9), 5873–5882 (2005).
   PubMed Web of Science ®Google Scholar
• Boyd CD , O'TooleGA. Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu. Rev. Cell Dev. Biol.28 (1), 439–462 (2012).
   PubMedGoogle Scholar
• Newell PD , MondsRD, O'TooleGA. LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl Acad. Sci. USA106 (9), 3461–3466 (2009).
   PubMed Web of Science ®Google Scholar
• Newell PD , BoydCD, SondermannH, O'TooleGA. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol.9 (2), e1000587 (2011).
   PubMed Web of Science ®Google Scholar
• Monds RD , NewellPD, GrossRH, O'TooleGA. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0–1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol.63 (3), 656–679 (2007).
   PubMed Web of Science ®Google Scholar
• Ryjenkov DA , SimmR, RömlingU, GomelskyM. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem.281 (41), 30310–30314 (2006).
   PubMed Web of Science ®Google Scholar
• Boehm A , KaiserM, LiHet al. Second messenger-mediated adjustment of bacterial swimming velocity. Cell141 (1), 107–116 (2010).
   PubMed Web of Science ®Google Scholar
• Paul K , NietoV, CarlquistWC, BlairDF, HarsheyRM. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol. Cell38 (1), 128–139 (2010).
   PubMed Web of Science ®Google Scholar
• Martinez-Wilson HF , TamayoR, TischlerAD, LazinskiDW, CamilliA. The Vibrio cholerae hybrid sensor kinase VieS contributes to motility and biofilm regulation by altering the cyclic diguanylate level. J. Bacteriol.190 (19), 6439–6447 (2008).
   PubMed Web of Science ®Google Scholar
• Tamayo R , TischlerAD, CamilliA. TheEAL Domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem.280 (39), 33324–33330 (2005).
   PubMed Web of Science ®Google Scholar
• Simm R , MorrM, KaderA, NimtzM, RömlingU. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol.53 (4), 1123–1134 (2004).
   PubMed Web of Science ®Google Scholar
• Kirillina O , FetherstonJD, BobrovAG, AbneyJ, PerryRD. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol. Microbiol.54 (1), 75–88 (2004).
   PubMed Web of Science ®Google Scholar
• Wilksch JJ , YangJ, ClementsAet al. MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog.7 (8), e1002204 (2011).
   PubMed Web of Science ®Google Scholar
• Carlson HK , VanceRE, MarlettaMA. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol. Microbiol.77 (4), 930–942 (2010).
   PubMed Web of Science ®Google Scholar
• Nakhamchik A , WildeC, Rowe-MagnusDA. Cyclic-di-GMP regulates extracellular polysaccharide production, biofilm formation, and rugose colony development by Vibrio vulnificus. Appl. Environ. Microbiol.74 (13), 4199–4209 (2008).
   PubMed Web of Science ®Google Scholar
• Romeo T , GongM, LiuMY, Brun-ZinkernagelAM. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol.175 (15), 4744–4755 (1993).
   PubMed Web of Science ®Google Scholar
• Liu MY , GuiG, WeiBet al. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem.272 (28), 17502–17510 (1997).
   PubMed Web of Science ®Google Scholar
• Jackson DW , SuzukiK, OakfordL, SimeckaJW, HartME, RomeoT. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol.184 (1), 290–301 (2002).
   PubMed Web of Science ®Google Scholar
• Ventre I , GoodmanAL, Vallet-GelyIet al. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl Acad. Sci. USA103 (1), 171–176 (2006).
   PubMed Web of Science ®Google Scholar
• Kay E , HumairB, DénervaudVet al. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J. Bacteriol.188 (16), 6026–6033 (2006).
   PubMed Web of Science ®Google Scholar
• Jimenez PN , KochG, ThompsonJA, XavierKB, CoolRH, QuaxWJ. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev.76 (1), 46–65 (2012).
   PubMed Web of Science ®Google Scholar
• Babitzke P , RomeoT. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol.10 (2), 156–163 (2007).
   PubMed Web of Science ®Google Scholar
• Ogasawara H , YamamotoK, IshihamaA. Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J. Bacteriol.193 (10), 2587–2597 (2011).
   PubMed Web of Science ®Google Scholar
• Mika F , HenggeR. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli. RNA Biol.11 (5), 494–507 (2014).
   PubMed Web of Science ®Google Scholar
• Chambers JR , SauerK. Small RNAs and their role in biofilm formation. Trends Microbiol.21 (1), 39–49 (2013).
   PubMed Web of Science ®Google Scholar
• Dalton T , DowdSE, WolcottRDet al. An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoS One6 (11), e27317 (2011).
   PubMed Web of Science ®Google Scholar
• Hoffmann N , RasmussenTB, JensenPØet al. Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis. Infect. Immun.73 (4), 2504–2514 (2005).
   PubMed Web of Science ®Google Scholar
• Buret A , WardKH, OlsonME, CostertonJW. An in vivo model to study the pathobiology of infectious biofilms on biomaterial surfaces. J. Biomed. Mater. Res.25 (7), 865–874 (1991).
   PubMed Web of Science ®Google Scholar
• Chauhan A , LebeauxD, DecanteBet al. A rat model of central venous catheter to study establishment of long-term bacterial biofilm and related acute and chronic infections. PLoS One7 (5), e37281 (2012).
   PubMed Web of Science ®Google Scholar
• Cole SJ , RecordsAR, OrrMW, LindenSB, LeeVT. Catheter-associated urinary tract infection by Pseudomonas aeruginosa is mediated by exopolysaccharide independent biofilms. Infect. Immun.82 (5), 2048–2058 (2014).
   PubMed Web of Science ®Google Scholar
• Watters C , DeLeonK, TrivediUet al. Pseudomonas aeruginosa biofilms perturb wound resolution and antibiotic tolerance in diabetic mice. Med. Microbiol. Immunol.202 (2), 131–141 (2013).
   PubMed Web of Science ®Google Scholar
• Bjarnsholt T , JensenPØ, FiandacaMJet al. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol.44 (6), 547–558 (2009).
   PubMed Web of Science ®Google Scholar