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Candida Biofilm Tolerance: Comparison of Planktonic and Biofilm Resistance Mechanisms

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Candida albicans: Cellular and Molecular Biology

Abstract

Candida species are opportunistic fungal pathogens residing as commensal organisms in approximately 70% of the human population. During times of decreased immune function, Candida spp. are able to transition from harmless members of the human microbiota into pathogens capable of causing life-threatening infections boasting mortality rates as high as 50%. Commonly adhering to implanted medical devices, Candida spp. grow as highly structured biofilms with inherent resistance to antifungal drug therapies and the host immune system. A multitude of investigations have found this resistance to be multifactorial involving mechanisms associated with planktonic antifungal resistance (efflux pump activity) along with biofilm-specific mechanisms. One biofilm-specific mechanism involves the complex extracellular matrix. Components of the matrix, specifically β-glucan, mannan, and extracellular DNA, have been found to promote resistance against multiple antifungal drug classes. Here we will review molecular mechanisms contributing to Candida biofilm drug resistance.

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References

  • Al-Fattani MA, Douglas LJ (2004) Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother 48:3291–3297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Fattani MA, Douglas LJ (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55:999–1008

    Article  CAS  PubMed  Google Scholar 

  • Albertson GD, Niimi M, Cannon RD, Jenkinson HF (1996) Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob Agents Chemother 40:2835–2841

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baginski M, Czub J (2009) Amphotericin B and its new derivatives—mode of action. Curr Drug Metab 10:459–469

    Article  CAS  PubMed  Google Scholar 

  • Balashov SV, Park S, Perlin DS (2006) Assessing resistance to the echinocandin antifungal drug caspofungin in Candida albicans by profiling mutations in FKS1. Antimicrob Agents Chemother 50:2058–2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bizerra FC, Melo AS, Katchburian E, Freymuller E, Straus AH, Takahashi HK, Colombo AL (2011) Changes in cell wall synthesis and ultrastructure during paradoxical growth effect of caspofungin on four different Candida species. Antimicrob Agents Chemother 55:302–310

    Article  CAS  PubMed  Google Scholar 

  • Bizerra FC, Nakamura CV, de Poersch C, Estivalet Svidzinski TI, Borsato Quesada RM, Goldenberg S, Krieger MA, Yamada-Ogatta SF (2008) Characteristics of biofilm formation by Candida tropicalis and antifungal resistance. FEMS Yeast Res 8:442–450

    Article  CAS  PubMed  Google Scholar 

  • Cannon RD, Lamping E, Holmes AR, Niimi K, Baret PV, Keniya MV, Tanabe K, Niimi M, Goffeau A, Monk BC (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22:291–321, Table of Contents

    Google Scholar 

  • Chaffin WL, Lopez-Ribot JL, Casanova M, Gozalbo D, Martinez JP (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62:130–180

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183:5385–5394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleveland AA, Farley MM, Harrison LH, Stein B, Hollick R, Lockhart SR, Magill SS, Derado G, Park BJ, Chiller TM (2012) Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008–2011. Clin Infect Dis 55:1352–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coste A, Selmecki A, Forche A, Diogo D, Bougnoux ME, d’Enfert C, Berman J, Sanglard D (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6:1889–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science (New York, NY) 284:1318–1322

    Article  CAS  Google Scholar 

  • Denning DW (2003) Echinocandin antifungal drugs. Lancet 362:1142–1151

    Article  CAS  PubMed  Google Scholar 

  • Desnos-Ollivier M, Bretagne S, Raoux D, Hoinard D, Dromer F, Dannaoui E (2008) Mutations in the fks1 gene in Candida albicans, C-tropicalis, and C-krusei correlate with elevated caspofungin MICs uncovered in AM3 medium using the method of the European Committee on antibiotic susceptibility testing. Antimicrob Agents Chemother 52:3092–3098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donlan RM (2001) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 33:1387–1392

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11:30–36

    Article  CAS  PubMed  Google Scholar 

  • Faria-Oliveira F, Carvalho J, Belmiro CL, Martinez-Gomariz M, Hernaez ML, Pavao M, Gil C, Lucas C, Ferreira C (2014) Methodologies to generate, extract, purify and fractionate yeast ECM for analytical use in proteomics and glycomics. BMC Microbiol 14:244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fernandes T, Silva S, Henriques M (2015) Candida tropicalis biofilm’s matrix–involvement on its resistance to amphotericin B. Diagn Microbiol Infect Dis 83:165–169

    Article  CAS  PubMed  Google Scholar 

  • Finkel JS, Mitchell AP (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9:109–118

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Garcia-Effron G, Park S, Perlin DS (2009) Correlating echinocandin MIC and kinetic inhibition of fks1 mutant glucan synthases for Candida albicans: implications for interpretive breakpoints. Antimicrob Agents Chemother 53:112–122

    Article  CAS  PubMed  Google Scholar 

  • Ghannoum MA, Rice LB (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12:501–517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray KC, Palacios DS, Dailey I, Endo MM, Uno BE, Wilcock BC, Burke MD (2012) Amphotericin primarily kills yeast by simply binding ergosterol. Proc Natl Acad Sci USA 109:2234–2239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez S, Lopez-Ribot JL, Najvar LK, McCarthy DI, Bocanegra R, Graybill JR (2004) Caspofungin resistance in Candida albicans: correlating clinical outcome with laboratory susceptibility testing of three isogenic isolates serially obtained from a patient with progressive Candida esophagitis. Antimicrob Agents Chemother 48:1382–1383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hope W, Tabernero L, Denning DW, Anderson MJ (2004) Molecular mechanisms of primary resistance to flucytosine in Candida albicans. Antimicrob Agents Chemother 48:4377–4386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, et al (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67(7):2982–2992

    Google Scholar 

  • Johnson ME, Katiyar SK, Edlind TD (2011) New Fks hot spot for acquired echinocandin resistance in Saccharomyces cerevisiae and its contribution to intrinsic resistance of Scedosporium species. Antimicrob Agents Chemother 55:3774–3781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabir MA, Hussain MA, Ahmad Z (2012) Candida albicans: a model organism for studying fungal pathogens. ISRN Microbiol 2012:538694

    Article  PubMed  PubMed Central  Google Scholar 

  • Katiyar SK, Edlind TD (2009) Role for Fks1 in the intrinsic echinocandin resistance of Fusarium solani as evidenced by hybrid expression in Saccharomyces cerevisiae. Antimicrob Agents Chemother 53:1772–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly SL, Lamb DC, Corran AJ, Baldwin BC, Kelly DE (1995) Mode of action and resistance to azole antifungals associated with the formation of 14 alpha-methylergosta-8,24(28)-dien-3 beta,6 alpha-diol. Biochem Biophys Res Commun 207:910–915

    Article  CAS  PubMed  Google Scholar 

  • Kelly SL, Lamb DC, Kelly DE, Loeffler J, Einsele H (1996) Resistance to fluconazole and amphotericin in Candida albicans from AIDS patients. Lancet 348:1523–1524

    Article  CAS  PubMed  Google Scholar 

  • Kelly SL, Lamb DC, Kelly DE, Manning NJ, Loeffler J, Hebart H, Schumacher U, Einsele H (1997) Resistance to fluconazole and cross-resistance to amphotericin B in Candida albicans from AIDS patients caused by defective sterol delta5,6-desaturation. FEBS Lett 400:80–82

    Article  CAS  PubMed  Google Scholar 

  • Kojic EM, Darouiche RO (2004) Candida infections of medical devices. Clin Microbiol Rev 17:255–267

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302

    Article  CAS  PubMed  Google Scholar 

  • Kontoyiannis DP (2000) Efflux-mediated resistance to fluconazole could be modulated by sterol homeostasis in Saccharomyces cerevisiae. J Antimicrob Chemother 46:199–203

    Article  CAS  PubMed  Google Scholar 

  • Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA (2002) Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46:1773–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaFleur MD, Kumamoto CA, Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50:3839–3846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb DC, Kelly DE, Schunck WH, Shyadehi AZ, Akhtar M, Lowe DJ, Baldwin BC, Kelly SL (1997) The mutation T315A in Candida albicans sterol 14alpha-demethylase causes reduced enzyme activity and fluconazole resistance through reduced affinity. J Biol Chem 272:5682–5688

    Article  CAS  PubMed  Google Scholar 

  • Lamfon H, Porter SR, McCullough M, Pratten J (2004) Susceptibility of Candida albicans biofilms grown in a constant depth film fermentor to chlorhexidine, fluconazole and miconazole: a longitudinal study. J Antimicrob Chemother 53:383–385

    Article  CAS  PubMed  Google Scholar 

  • Laverdiere M, Lalonde RG, Baril JG, Sheppard DC, Park S, Perlin DS (2006) Progressive loss of echinocandin activity following prolonged use for treatment of Candida albicans oesophagitis. J Antimicrob Chemoth 57:705–708

    Article  CAS  Google Scholar 

  • Law D, Moore CB, Wardle HM, Ganguli LA, Keaney MG, Denning DW (1994) High prevalence of antifungal resistance in Candida spp. from patients with AIDS. The Journal of antimicrobial chemotherapy 34:659–668

    Article  CAS  PubMed  Google Scholar 

  • Lewis K (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322:107–131

    CAS  PubMed  Google Scholar 

  • Lindsay AK, Deveau A, Piispanen AE, Hogan DA (2012) Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans. Eukaryot Cell 11:1219–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lupetti A, Danesi R, Campa M, Del Tacca M, Kelly S (2002) Molecular basis of resistance to azole antifungals. Trends Mol Med 8:76–81

    Article  CAS  PubMed  Google Scholar 

  • Mah TF (2012) Biofilm-specific antibiotic resistance. Future Microbiol 7:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Marichal P, Koymans L, Willemsens S, Bellens D, Verhasselt P, Luyten W, Borgers M, Ramaekers FC, Odds FC, Bossche HV (1999) Contribution of mutations in the cytochrome P450 14alpha-demethylase (Erg11p, Cyp51p) to azole resistance in Candida albicans. Microbiology 145(Pt 10):2701–2713

    Article  CAS  PubMed  Google Scholar 

  • Marie C, White TC (2009) Genetic basis of antifungal drug resistance. Curr Fungal Infect Rep 3:163–169

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins M, Henriques M, Lopez-Ribot JL, Oliveira R (2012) Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses 55:80–85

    Article  CAS  PubMed  Google Scholar 

  • Martins M, Uppuluri P, Thomas DP, Cleary IA, Henriques M, Lopez-Ribot JL, Oliveira R (2010) Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 169:323–331

    Article  CAS  PubMed  Google Scholar 

  • Mayer FL, Wilson D, Hube B (2013) Candida albicans pathogenicity mechanisms. Virulence 4:119–128

    Article  PubMed  PubMed Central  Google Scholar 

  • Meiller TF, Hube B, Schild L, Shirtliff ME, Scheper MA, Winkler R, Ton A, Jabra-Rizk MA (2009) A novel immune evasion strategy of candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS ONE 4:e5039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell KF, Taff HT, Cuevas MA, Reinicke EL, Sanchez H, Andes DR (2013) Role of matrix beta-1,3 glucan in antifungal resistance of non-albicans Candida biofilms. Antimicrob Agents Chemother 57:1918–1920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell KF, Zarnowski R, Sanchez H, Edward JA, Reinicke EL, Nett JE, Mitchell AP, Andes DR (2015) Community participation in biofilm matrix assembly and function. Proc Natl Acad Sci U S A 112:4092–4097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morschhauser J (2002) The genetic basis of fluconazole resistance development in Candida albicans. Biochim Biophys Acta 1587:240–248

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA (2003) Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 71:4333–4340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D (2007) Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51:510–520

    Article  CAS  PubMed  Google Scholar 

  • Nett JE, Crawford K, Marchillo K, Andes DR (2010a) Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 54:3505–3508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nett JE, Lepak AJ, Marchillo K, Andes DR (2009) Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 200:307–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nett JE, Sanchez H, Cain MT, Andes DR (2010b) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202:171–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen MH, Yu CY (1999) Influence of incubation time, inoculum size, and glucose concentrations on spectrophotometric endpoint determinations for amphotericin B, fluconazole, and itraconazole. J Clin Microbiol 37:141–145

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nobile CJ, Johnson AD (2015) Candida albicans biofilms and human disease. Annu Rev Microbiol 69:71–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A, Andes DR, Johnson AD, Mitchell AP (2009) Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7:e1000133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Toole GA (2003) To build a biofilm. J Bacteriol 185:2687–2689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ostrosky-Zeichner L, Casadevall A, Galgiani JN, Odds FC, Rex JH (2010) An insight into the antifungal pipeline: selected new molecules and beyond. Nat Rev Drug Discov 9:719–727

    Article  CAS  PubMed  Google Scholar 

  • Pappas PG, Kauffman CA, Andes D, Benjamin DK Jr, Calandra TF, Edwards JE Jr, Filler SG, Fisher JF, Kullberg BJ, Ostrosky-Zeichner L et al (2009) Clinical practice guidelines for the management of candidiasis: 2009 update by the infectious diseases society of America. Clin Infect Dis 48:503–535

    Article  CAS  PubMed  Google Scholar 

  • Park S, Kelly R, Kahn JN, Robles J, Hsu MJ, Register E, Li W, Vyas V, Fan H, Abruzzo G et al (2005) Specific substitutions in the echinocandin target Fks1p account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrob Agents Chemother 49:3264–3273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perlin DS (2007) Resistance to echinocandin-class antifungal drugs. Drug Resist Updat 10:121–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perlin DS (2015a) Echinocandin resistance in Candida. Clin Infect Dis 61(Suppl 6):S612–S617

    Article  PubMed  PubMed Central  Google Scholar 

  • Perlin DS (2015b) Mechanisms of echinocandin antifungal drug resistance. Ann N Y Acad Sci 1354:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perumal P, Mekala S, Chaffin WL (2007) Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother 51:2454–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaller MA, Castanheira M, Messer SA, Moet GJ, Jones RN (2010) Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY antimicrobial surveillance program (2008–2009). Diagn Microbiol Infect Dis 68:278–283

    Article  PubMed  Google Scholar 

  • Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaller MA, Diekema DJ, Rinaldi MG, Barnes R, Hu B, Veselov AV, Tiraboschi N, Nagy E, Gibbs DL (2005) Results from the ARTEMIS DISK Global Antifungal Surveillance Study: a 6.5-year analysis of susceptibilities of Candida and other yeast species to fluconazole and voriconazole by standardized disk diffusion testing. J Clin Microbiol 43:5848–5859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramage G, Bachmann S, Patterson TF, Wickes BL, Lopez-Ribot JL (2002a) Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother 49:973–980

    Article  CAS  PubMed  Google Scholar 

  • Ramage G, Rajendran R, Sherry L, Williams C (2012) Fungal biofilm resistance. Int J Microbiol 2012:528521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramage G, Saville SP, Thomas DP, Lopez-Ribot JL (2005) Candida biofilms: an update. Eukaryot Cell 4:633–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramage G, Saville SP, Wickes BL, Lopez-Ribot JL (2002b) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68:5459–5463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramage G, Vande Walle K, Wickes BL, Lopez-Ribot JL (2001) Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45:2475–2479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riesselman MH, Hazen KC, Cutler JE (2000) Determination of antifungal MICs by a rapid susceptibility assay. J Clin Microbiol 38:333–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roder HL, Sorensen SJ, Burmolle M (2016) Studying bacterial multispecies biofilms: where to start? Trends Microbiol

    Google Scholar 

  • Romling U, Balsalobre C (2012) Biofilm infections, their resilience to therapy and innovative treatment strategies. J Intern Med 272:541–561

    Article  CAS  PubMed  Google Scholar 

  • Rosenbach A, Dignard D, Pierce JV, Whiteway M, Kumamoto CA (2010) Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot Cell 9:1075–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruhnke M, Maschmeyer G (2002) Management of mycoses in patients with hematologic disease and cancer—review of the literature. Eur J Med Res 7:227–235

    PubMed  Google Scholar 

  • Sanglard D, Ischer F, Koymans L, Bille J (1998) Amino acid substitutions in the cytochrome P-450 lanosterol 14alpha-demethylase (CYP51A1) from azole-resistant Candida albicans clinical isolates contribute to resistance to azole antifungal agents. Antimicrob Agents Chemother 42:241–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanglard D, Kuchler K, Ischer F, Pagani JL, Monod M, Bille J (1995) Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob Agents Chemother 39:2378–2386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulze J, Sonnenborn U (2009) Yeasts in the gut: from commensals to infectious agents. Dtsch Arztebl Int 106:837–842

    PubMed  PubMed Central  Google Scholar 

  • Seneviratne CJ, Jin LJ, Samaranayake H, Samaranayake LP (2008) Cell density and cell aging as factors modulating antifungal resistance of Candida albicans biofilms. Antimicrob Agents Chemother 52:3259–3266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shapiro RS, Robbins N, Cowen LE (2011) Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75:213–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Prasad R (2011) The quorum-sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans. Antimicrob Agents Chemother 55:4834–4843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimokawa O, Nakayama H (1992) Increased sensitivity of Candida albicans cells accumulating 14 alpha-methylated sterols to active oxygen: possible relevance to in vivo efficacies of azole antifungal agents. Antimicrob Agents Chemother 36:1626–1629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva AP, Miranda IM, Guida A, Synnott J, Rocha R, Silva R, Amorim A, Pina-Vaz C, Butler G, Rodrigues AG (2011) Transcriptional profiling of azole-resistant Candida parapsilosis strains. Antimicrob Agents Chemother 55:3546–3556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobel JD (1997) Vaginitis. N Engl J Med 337:1896–1903

    Article  CAS  PubMed  Google Scholar 

  • Stevens DA, Ichinomiya M, Koshi Y, Horiuchi H (2006) Escape of Candida from caspofungin inhibition at concentrations above the MIC (Paradoxical effect) accomplished by increased cell wall chitin; evidence for beta-1,6-glucan synthesis inhibition by caspofungin. Antimicrob Agents Chemother 50:3160–3161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Li Z, Chu H, Guo J, Jiang G, Qi Q (2016) Candida albicans amphotericin B-Tolerant persister formation is closely related to surface adhesion. Mycopathologia 181:41–49

    Article  CAS  PubMed  Google Scholar 

  • Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, Cain MT, Hamaker J, Mitchell AP, Andes DR (2012) A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8:e1002848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taff HT, Mitchell KF, Edward JA, Andes DR. (2013) Mechanisms of Candida biofilm drug resistance. Future Microbiol 8(10):1325–1337

    Google Scholar 

  • Thomas DP, Bachmann SP, Lopez-Ribot JL (2006) Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6:5795–5804

    Article  CAS  PubMed  Google Scholar 

  • Tobudic S, Kratzer C, Lassnigg A, Graninger W, Presterl E (2010) In vitro activity of antifungal combinations against Candida albicans biofilms. J Antimicrob Chemother 65:271–274

    Article  CAS  PubMed  Google Scholar 

  • Tobudic S, Kratzer C, Lassnigg A, Presterl E (2012) Antifungal susceptibility of Candida albicans in biofilms. Mycoses 55:199–204

    Article  PubMed  Google Scholar 

  • Vanden Bossche H, Marichal P, Odds FC, Le Jeune L, Coene MC (1992) Characterization of an azole-resistant Candida glabrata isolate. Antimicrob Agents Chemother 36:2602–2610

    Google Scholar 

  • Vandeputte P, Larcher G, Berges T, Renier G, Chabasse D, Bouchara JP (2005) Mechanisms of azole resistance in a clinical isolate of Candida tropicalis. Antimicrob Agents Chemother 49:4608–4615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandeputte P, Tronchin G, Berges T, Hennequin C, Chabasse D, Bouchara JP (2007) Reduced susceptibility to polyenes associated with a missense mutation in the ERG6 gene in a clinical isolate of Candida glabrata with pseudohyphal growth. Antimicrob Agents Chemother 51:982–990

    Article  CAS  PubMed  Google Scholar 

  • Vediyappan G, Rossignol T, d’Enfert C (2010) Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother 54:2096–2111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TC (1997a) Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob Agents Chemother 41:1482–1487

    CAS  PubMed  PubMed Central  Google Scholar 

  • White TC (1997b) The presence of an R467 K amino acid substitution and loss of allelic variation correlate with an azole-resistant lanosterol 14alpha demethylase in Candida albicans. Antimicrob Agents Chemother 41:1488–1494

    CAS  PubMed  PubMed Central  Google Scholar 

  • White TC, Marr KA, Bowden RA (1998a) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11:382–402

    CAS  PubMed  PubMed Central  Google Scholar 

  • White TC, Marr KA, Bowden RA (1998b) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11, 382- + 

    Google Scholar 

  • Wongsuk T, Pumeesat P, Luplertlop N (2016) Fungal quorum sensing molecules: role in fungal morphogenesis and pathogenicity. J Basic Microbiol 56:440–447

    Article  CAS  PubMed  Google Scholar 

  • Yi S, Sahni N, Daniels KJ, Lu KL, Srikantha T, Huang G, Garnaas AM, Soll DR (2011) Alternative mating type configurations (a/alpha versus a/a or alpha/alpha) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol 9:e1001117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarnowski R, Westler WM, Lacmbouh GA, Marita JM, Bothe JR, Bernhardt J, Lounes-Hadj Sahraoui A, Fontaine J, Sanchez H, Hatfield RD et al (2014) Novel entries in a fungal biofilm matrix encyclopedia. MBio 5:e01333–01314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, WI, USA

    Eddie G. Dominguez & David R. Andes

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  1. Eddie G. Dominguez
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  2. David R. Andes
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Correspondence to David R. Andes .

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  1. Amity Institute of Integrative Sciences and Health and Amity Institute of Biotechnology, Amity Institute of Integrative Sciences and Health and Amity Institute of Biotechnology, Amity University Haryana, Gurgaon, Haryana, India

    Rajendra Prasad

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Dominguez, E.G., Andes, D.R. (2017). Candida Biofilm Tolerance: Comparison of Planktonic and Biofilm Resistance Mechanisms. In: Prasad, R. (eds) Candida albicans: Cellular and Molecular Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-50409-4_6

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