Recent insights into Candida albicans biofilm resistance mechanisms

Lotte Mathé, Patrick Van Dijck, Lotte Mathé, Patrick Van Dijck

Abstract

Like other microorganisms, free-living Candida albicans is mainly present in a three-dimensional multicellular structure, which is called a biofilm, rather than in a planktonic form. Candida albicans biofilms can be isolated from both abiotic and biotic surfaces at various locations within the host. As the number of abiotic implants, mainly bloodstream and urinary catheters, has been increasing, the number of biofilm-associated bloodstream or urogenital tract infections is also strongly increasing resulting in a raise in mortality. Cells within a biofilm structure show a reduced susceptibility to specific commonly used antifungals and, in addition, it has recently been shown that such cells are less sensitive to killing by components of our immune system. In this review, we summarize the most important insights in the mechanisms underlying biofilm-associated antifungal drug resistance and immune evasion strategies, focusing on the most recent advances in this area of research.

References

    1. Al-Dhaheri RS, Douglas LJ. Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob Agents Chemother. 2008;52:1884–1887.
    1. Al-Dhaheri RS, Douglas LJ. Apoptosis in Candida biofilms exposed to amphotericin B. J Med Microbiol. 2010;59:149–157.
    1. Al-Fattani MA, Douglas LJ. Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother. 2004;48:3291–3297.
    1. Al-Fattani MA, Douglas LJ. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol. 2006;55:999–1008.
    1. Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A. Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun. 2004;72:6023–6031.
    1. Bachmann SP, VandeWalle K, Ramage G, Patterson TF, Wickes BL, Graybill JR, López-Ribot JL. In vitro activity of echinocandins against Candida albicans biofilms. Antimicrob Agents Chemother. 2002;46:3591–3596.
    1. Baillie GS, Douglas LJ. Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother. 1998;42:1900–1905.
    1. Baillie GS, Douglas LJ. Candida biofilms and their susceptibility to antifungal agents. Methods Enzymol. 1999;310:644–656.
    1. Baillie GS, Douglas LJ. Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol. 1999;48:671–679.
    1. Baillie GS, Douglas LJ. Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother. 2000;46:397–403.
    1. Banerjee M, Uppuluri P, Zhao XR, Carlisle PL, Vipulanandan G, Villar CC, López-Ribot JL, Kadosh D. Expression of UME6, a key regulator of Candida albicans hyphal development, enhances biofilm formation via Hgc1- and Sun41-dependent mechanisms. Eukaryot Cell. 2013;12:224–232.
    1. Ben-Yaacov R, Knoller S, Caldwell GA, Becker JM, Koltin Y. Candida albicans gene encoding resistance to benomyl and methotrexate is a multidrug resistance gene. Antimicrob Agents Chemother. 1994;38:648–652.
    1. Berman J, Sudbery P. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet. 2002;3:918–930.
    1. Bigger JW. Treatment of Staphylococcal infections with penicillin. Lancet. 1944;ii:497–500.
    1. Bink A, Vandenbosch D, Coenye T, Nelis H, Cammue BP, Thevissen K. Superoxide dismutases are involved in Candida albicans biofilm persistence against miconazole. Antimicrob Agents Chemother. 2011;55:4033–4037.
    1. Bink A, Kucharicová S, Neirinck B, Vleugels J, Van Dijck P, Cammue BP, Thevissen K. The nonsteroidal antiinflammatory drug diclofenac potentiates the in vivo activity of caspofungin against Candida albicans biofilms. J Infect Dis. 2012;206:1790–1797.
    1. Blankenship JR, Heitman J. Calcineurin is required for Candida albicans to survive calcium stress in serum. Infect Immun. 2005;73:5767–5774.
    1. Blankenship JR, Mitchell AP. How to build a biofilm: a fungal perspective. Curr Opin Microbiol. 2006;9:588–594.
    1. Bonhomme J, Chauvel M, Goyard S, Roux P, Rossignol T, d’ Enfert C. Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol Microbiol. 2011;80:995–1013.
    1. Borecká-Melkusová S, Moran GP, Sullivan DJ, Kucharicová S, Chorvát DJ, Bujdákova H. The expression of genes involved in the ergosterol biosynthesis pathway in Candida albicans and Candida dubliniensis biofilms exposed to fluconazole. Mycoses. 2009;52:118–128.
    1. Bourgeois C, Majer O, Frohner IE, Tierney L, Kuchler K. Fungal attacks on mammalian hosts: pathogen elimination requires sensing and tasting. Curr Opin Microbiol. 2010;13:401–408.
    1. Bouza E, Burillo A, Muñoz P, Guinea J, Marin M, Rodriguez-Créixems M. Mixed bloodstream infections involving bacteria and Candida spp. J Antimicrob Chemother. 2013;68(8):1881–1888.
    1. Calabrese D, Bille J, Sanglard D. A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology. 2000;146:2743–2754.
    1. Cannon RD, Lamping E, Holmes AR, Niimi K, Tanabe K, Niimi M, Monk BC. Candida albicans drug resistance another way to cope with stress. Microbiology. 2007;153:3211–3217.
    1. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum M. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. J Bacteriol. 2001;183:5385–5394.
    1. Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, Douglas LJ, Ghannoum MA. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res. 2001;80:903–908.
    1. Chandra J, McCormick TS, Imamura Y, Mukherjee PK, Ghannoum MA. Interaction of Candida albicans with adherent human peripheral blood mononuclear cells increases C. albicans biofilm formation and results in differential expression of pro- and anti-inflammatory cytokines. Infect Immun. 2007;75:2612–2620.
    1. Chandra J, Long L, Ghannoum MA, Mukherjee PK. A rabbit model for evaluation of catheter-associated fungal biofilms. Virulence. 2011;2:466–474.
    1. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol. 1995;49:711–745.
    1. Cowen LE, Steinbach WJ. Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot Cell. 2008;7:747–764.
    1. da Silva WJ, Gonçalves LM, Seneviratne J, Parahitiyawa N, Samaranayake LP, Del Bel Cury AA. Exopolysaccharide matrix of developed Candida albicans biofilms after exposure to antifungal agents. Braz Dent J. 2012;23:716–722.
    1. Darouiche RO. Treatment of infections associated with surgical implants. N Engl J Med. 2004;350:1422–1429.
    1. Denning DW, Hope WW. Therapy for fungal diseases: opportunities and priorities. Trends Microbiol. 2010;18:195–204.
    1. Diez-Orejas R, Molero G, Navarro-Garcia F, Pla J, Nombela C, Sanchez-Perez M. Reduced virulence of Candida albicansMKC1 mutants: a role for mitogen-activated protein kinase in pathogenesis. Infect Immun. 1997;65:833–837.
    1. Dongari-Bagtzoglou A, Kashleva H, Dwivedi P, Diaz P, Vasilakos J. Characterization of mucosal Candida albicans biofilms. PLoS ONE. 2009;4:e7976.
    1. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–193.
    1. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 2003;11:30–36.
    1. Falagas ME, Apostolou KE, Pappas VD. Attributable mortality of candidemia: a systematic review of matched cohort and case-control studies. Eur J Clin Microbiol Infect Dis. 2006;25:419–425.
    1. Fanning S, Xu W, Solis N, Woolford CA, Filler SG, Mitchell AP. Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell. 2012;11:896–904.
    1. Finkel JS, Mitchell AP. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol. 2011;9:109–118.
    1. Fiori A, Kucharicová S, Govaert G, Cammue BP, Thevissen K, Van Dijck P. The heat-induced molecular disaggregase Hsp104 of Candida albicans plays a role in biofilm formation and pathogenicity in a worm infection model. Eukaryot Cell. 2012;11:1012–1020.
    1. Fiori A, Van Dijck P (2012) Potent synergistic effect of doxycycline with Fluconazole against Candida albicans is mediated by interference with iron homeostasis. Antimicrob Agents Chemother 56:3785–3796
    1. Fling ME, Kopf J, Tamarkin A, Gorman JA, Smith HA, Koltin Y. Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate. Mol Gen Genet. 1991;227:318–329.
    1. Fox EP, Nobile CJ. A sticky situation: untangling the transcriptional network controlling biofilm development in Candida albicans. Transcription. 2012;3:315–322.
    1. Galan-Diez M, Arana DM, Serrano-Gomez D, Kremer L, Casasnovas JM, Ortega M, Cuesta-Dominguez A, Corbi AL, Pla J, Fernandez-Ruiz E. Candida albicans beta-glucan exposure is controlled by the fungal CEK1-mediated mitogen-activated protein kinase pathway that modulates immune responses triggered through dectin-1. Infect Immun. 2010;78:1426–1436.
    1. Gao Y, Zhang C, Lu C, Liu P, Li Y, Li H, Sun S. Synergistic effect of doxycycline and fluconazole against Candida albicans biofilms and the impact of calcium channel blockers. FEMS Yeast Res. 2013;13:453–462.
    1. García-Sánchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM, d’ Enfert C. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell. 2004;3:536–545.
    1. Gropp K, Schild L, Schindler S, Hube B, Zipfel PF, Skerka C. The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol Immunol. 2009;47:465–475.
    1. Harriott MM, Noverr MC. Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation. Antimicrob Agents Chemother. 2010;54:3746–3755.
    1. Harrison JJ, Wade WD, Akierman S, Vacchi-Suzzi C, Stremick CA, Turner RJ, Ceri H. The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing in a biofilm. Antimicrob Agents Chemother. 2009;53:2253–2258.
    1. Hawser S. Comparisons of the susceptibilities of planktonic and adherent Candida albicans to antifungal agents: a modified XTT tetrazolium assay using synchronised C. albicans cells. J Med Vet Mycol. 1996;34:149–152.
    1. Hawser SP, Douglas LJ. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun. 1994;62:915–921.
    1. Hawser SP, Douglas LJ. Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother. 1995;39:2128–2131.
    1. Hawser SP, Baillie GS, Douglas LJ. Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol. 1998;47:253–256.
    1. Hill JA, Ammar R, Torti D, Nislow C, Cowen LE. Genetic and genomic architecture of the evolution of resistance to antifungal drug combinations. PLoS Genet. 2013;9:e1003390.
    1. Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, Marr KA, Pfaller MA, Chang CH, Webster KM. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis. 2009;48:1695–1703.
    1. Kaneko Y, Miyagawa S, Takedo O, Hakariya M, Matsumoto S, Ohno H, Miyazaki Y. Real-time microscopic observation of Candida biofilm development and effects due to micafungin and fluconazole. Antimicrob Agents Chemother. 2013;57:2226–2230.
    1. Katragkou A, Kruhlak MJ, Simitsopoulou M, Chatzimoschou A, Taparkou A, Cotton CJ, Paliogianni F, Diza-Mataftsi E, Tsantali C, Walsh TJ, Roilides E. Interactions between human phagocytes and Candida albicans biofilms alone and in combination with antifungal agents. J Infect Dis. 2010;201:1941–1949.
    1. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol. 2004;186:8172–8180.
    1. Khot PD, Suci PA, Miller RL, Nelson RD, Tyler BJ. A small subpopulation of blastospores in Candida albicans biofilms exhibit resistance to amphotericin B associated with differential regulation of ergosterol and beta-1,6-glucan pathway genes. Antimicrob Agents Chemother. 2006;50:3708–3716.
    1. Kibbler CC, Seaton S, Barnes RA, Gransden WR, Holliman RE, Johnson EM, Perry JD, Sullivan DJ, Wilson JA. Management and outcome of bloodstream infections due to Candida species in England and Wales. J Hosp Infect. 2003;54:18–24.
    1. Kim J, Sudbery P. Candida albicans, a major human fungal pathogen. J Microbiol. 2011;49:171–177.
    1. Klotz SA, Chasin BS, Powell B, Gaur NK, Lipke PN. Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn Microbiol Infect Dis. 2007;59:401–406.
    1. Koh AY, Köhler JR, Coggshall KT, Van Rooijen N, Pier GB. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 2008;4:e35.
    1. Kojic EM, Darouiche RO. Candida infections on medical devices. Clin Microbiol Rev. 2004;17:255–267.
    1. Kucharicová S, Sharma N, Spriet I, Maertens J, Van Dijck P, Lagrou K. Activities of systematically administered echinocandins against in vivo mature Candida albicans biofilms developed in a rat subcutaneous model. Antimicrob Agents Chemother. 2013;57:2365–2368.
    1. Kucharíková S, Tournu H, Holtappels M, Van Dijck P, Lagrou K. In vivo efficacy of anidulafungin against Candida albicans mature biofilms in a novel rat model of catheter-associated candidiasis. Antimicrob Agents Chemother. 2010;54:4474–4478.
    1. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother. 2002;46:1773–1780.
    1. Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA. Uses and limitations of he XTT assay in studies of Candida growth and metabolism. J Clin Microbiol. 2003;41:506–508.
    1. Kullberg BJ, Oude Lashof AM, Netea MG (2004) Design of efficacy trials of cytokines in combination with antifungal drugs. Clin Infect Dis 39:S218–S223
    1. Kumamoto CA. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci USA. 2005;102:5576–5581.
    1. LaFleur MD, Kumamoto CA, Lewis K. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother. 2006;50:3839–3846.
    1. Lal P, Sharma D, Pruthi P, Pruthi V. Exopolysaccharide analysis of biofilm-forming Candida albicans. J Appl Microbiol. 2010;109:128–136.
    1. Lepak AJ, Nett J, Lincoln L, Marchillo K, Andes D. Time course of microbiologic outcome and gene expression in Candida albicans during and following in vitro and in vivo exposure to fluconazole. Antimicrob Agents Chemother. 2006;50:1311–1319.
    1. Lewis K. Persister cells. Annu Rev Microbiol. 2010;64:357–372.
    1. Lewis K. Persister cells: molecular mechanisms related to antibiotic tolerance. Handb Exp Pharmacol. 2012;211:121–133.
    1. Lewis RE, Kontoyiannis DP, Darouiche RO, Raad II, Prince RA. Antifungal activity of amphotericin B, fluconazole, and voriconazole in an in vitro model of Candida catheter-related bloodstream infection. Antimicrob Agents Chemother. 2002;46:3499–3505.
    1. Li R, Kumar R, Tati S, Puri S, Edgerton M. Candida albicans flu1-mediated efflux of salivary histatin 5 reduces its cytosolic concentration and fungicidal activity. Antimicrob Agents Chemother. 2013;57:1832–1839.
    1. Luo S, Hoffmann R, Skerka C, Zipfel PF. Glycerol-3-phosphate dehydrogenase 2 is a novel factor H-, factor H-like protein 1-, and plasminogen-binding surface protein of Candida albicans. J Infect Dis. 2013;207:594–603.
    1. Luo S, Poltermann S, Kunert A, Rupp S, Zipfel, PF (2009) Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a Factor H, FHL-1 and plasminogen binding surface protein. Mol Immunol 47:541–550
    1. Marger MD, Saier MHJ. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 1993;18:13–20.
    1. Martins M, Uppuluri P, Thomas DP, Cleary IA, Henriques M, Lopez-Ribot JL, Oliveira R. Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia. 2010;169:323–331.
    1. Martins M, Henriques M, Lopez-Ribot JL, Oliveira R. Addition of DNAse improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses. 2012;55:80–85.
    1. Mateus C, Crow SAJ, Ahearn DG. Adherence of Candida albicans to silicone induces immediate enhanced tolerance to fluconazole. Antimicrob Agents Chemother. 2004;48:3358–3366.
    1. Meiller TF, Hube B, Schild L, Shirtliff M, Scheper MA, Winkler R, Ton A, Jabra-Rizk MA. A novel immune evasion strategy of Candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS ONE. 2009;4:e5039.
    1. Miller LG, Hajjeh RA, Edwards JEJ. Estimating the cost of nosocomial candidemia in the United States. Clin Infect Dis. 2001;32:1110.
    1. Mitchell KF, Taff HT, Cuevas MA, Reinicke EL, Sanchez H, Andes DR. Role of matrix ß-1,3 glucan in antifungal resistance of non-albicans Candida biofilms. Antimicrob Agents Chemother. 2013;57:1918–1920.
    1. Monge RA, Roman E, Nombela C, Pla J. The MAP kinase signal transduction network in Candida albicans. Microbiology. 2006;152:905–912.
    1. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun. 2003;71:4333–4340.
    1. Mukherjee PK, Long LA, Kim HG, Ghannoum MA. Amphotericin B lipid complex is efficacious in the treatment of Candida albicans biofilms using a model of catheter-associated Candida biofilms. Int J Antimicrob Agents. 2009;33:149–153.
    1. Murillo LA, Newport G, Lan CY, Habelitz S, Dungan J, Agabian NM. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell. 2005;4:1562–1573.
    1. Nace HL, Horn DL, Neofytos D. Epidemiology and outcome of multiple-species candidemia at a tertiary care center between 2004 and 2007. Diagn Microbiol Infect Dis. 2009;64:289–294.
    1. Nailis H, Kucharikova S, Ricicova M, Van Dijck P, Deforce D, Nelis H, Coenye T. Real-time PCR expression profiling of genes encoding potential virulence factors in Candida albicans biofilms: identification of model-dependent and -independent gene expression. BMC Microbiol. 2010;10:114.
    1. Navarro-Garcia F, Sanchez M, Pla J, Nombela C. Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol Cell Biol. 1995;15:2197–2206.
    1. Navarro-Garcia F, Alonso-Monge R, Rico H, Pla J, Sentandreu R, Nombela C. A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology. 1998;144:411–424.
    1. Netea MG, Brown GD, Kullberg BJ, Gow NA. An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol. 2008;6:67–78.
    1. Nett J, Lincoln L, Marchillo K, Andes D. Beta -1,3 glucan as a test for central venous catheter biofilm infection. J Infect Dis. 2007;195:1705–1712.
    1. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D. Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother. 2007;51:510–520.
    1. Nett JE, Lepak AJ, Marchillo K, Andes DR. Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis. 2009;200:307–313.
    1. Nett J, Crawford K, Marchillo K, Andes DR. Role of Fks1p and matrix glucan on C. albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother. 2010;54:3505–3508.
    1. Nett JE, Sanchez H, Cain MT, Ross KM, Andes DR. Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot Cell. 2011;10:1660–1669.
    1. Niimi K, Maki K, Ikeda F, Holmes AR, Lamping E, Niimi M, Monk BC, Cannon RD. Overexpression of Candida albicans CDR1, CDR2, or MDR1 does not produce significant changes in echinocandin susceptibility. Antimicrob Agents Chemother. 2006;50:1148–1155.
    1. Nobile CJ, Mitchell AP. Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol. 2006;8:1382–1391.
    1. Nobile CJ, Fox EP, Nett JE, Sorrelis TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell. 2012;148:126–138.
    1. Ostrosky-Zeichner L, Casadevall A, Galgiani JN, Odds FC, Rex JH. An insight into the antifungal pipeline: selected new molecules and beyond. Nat Rev Drug Discov. 2010;9:719–727.
    1. Paull KD, Shoemaker RH, Boyd MR, Parsons JL, Risbood PA, Barbera WA, Sharma MN, Baker DC, Hand E, Scudiero DA, Monks A, Alley MC, Grote M. The synthesis of XTT: a new tetrazolium reagent that is bioreducible to a water-soluble formazan. J Heterocycl Chem. 1988;25:911–914.
    1. Peng S, Lu Y. Clinical epidemiology of central venous catheter-related bloodstream infections in an intensive care unit in China. J Crit Care. 2013;28:277–283.
    1. Perumal P, Mekala S, Chaffin WL. Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother. 2007;51:2454–2463.
    1. Pfaller M, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20:133–163.
    1. Pfaller MA, Diekema DJ. Epidemiology of invasive mycoses in North America. Crit Rev Microbiol. 2010;36:1–53.
    1. Pierce CG, Uppuluri P, Tummala S, Lopez-Ribot JL (2010) A 96 well microtiter plate-based method for monitoring formation and antifungal susceptibility testing of Candida albicans biofilms. J Vis Exp 21:44
    1. Prasad R, De Wergifosse P, Goffeau A, Balzi E. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr Genet. 1995;27:320–329.
    1. Ramage G, Vande Walle K, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2001;45:2475–2479.
    1. Ramage G, Vandewalle K, Wickes BL, Lopez-Ribot JL. Characteristics of biofilm formation by Candida albicans. Rev Iberoam Micol. 2001;18:163–170.
    1. Ramage G, Wickes BL, López-Ribot JL. Biofilms of Candida albicans and their associated resistance to antifungal agents. Am Clin Lab. 2001;20:42–44.
    1. Ramage G, Bachmann SP, Patterson TF, Wickes BL, López-Ribot JL. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother. 2002;49:973–980.
    1. Ramage G, VandeWalle K, Bachmann SP, Wickes BL, López-Ribot JL. In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob Agents Chemother. 2002;46:3634–3636.
    1. Ramage G, Martínez JP, López-Ribot JL. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 2006;6:979–986.
    1. Ramage G, Jose A, Sherry L, Lappin DF, Jones B, Williams C. Liposomal amphotericin B displays rapid dose-dependent activity against Candida albicans biofilms. Antimicrob Agents Chemother. 2013;57:2369–2371.
    1. Řičicová M, Kucharíková S, Tournu H, Hendrix J, Bujdákova H, Van Eldere J, Lagrou K, Van Dijck P. Candida albicans biofilm formation in a new in vivo rat model. Microbiol. 2010;156:909–919.
    1. Robbins N, Uppuluri P, Nett J, Rajendran R, Ramage G, Lopez-Ribot JL, Andes D, Cowen LE. Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog. 2011;7:e1002257.
    1. Sanglard D. Resistance of human fungal pathogens to antifungal drugs. Curr Opin Microbiol. 2002;5:379–385.
    1. Sanglard D, Kuchler K, Ischer F, Pagani JL, Monod M, Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob Agents Chemother. 1995;39:2378–2386.
    1. Sanglard D, Ischer F, Monod M, Bille J. Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob Agents Chemother. 1996;40:2300–2305.
    1. Sanglard D, Ischer F, Monod M, Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiol. 1997;143:405–416.
    1. Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ. Candida species: current epidemiology, pathology, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol. 2013;62:10–24.
    1. Sasse C, Hasenberg M, Weyler M, Gunzer M, Morschhäuser J. White-opaque switching of Candida albicans, allows immune evasion in an environment-dependent fashion. Eukaryot Cell. 2013;12:50–58.
    1. Seider K, Heyken A, Lüttich A, Miramon P, Hube B. Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Curr Opin Microbiol. 2010;13:392–400.
    1. Selmecki AM, Dulmage K, Cowen LE, Anderson JB, Berman J. Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet. 2009;5:e1000705.
    1. Seneviratne CJ, Jin L, Samaranayake LP. Biofilm lifestyle of Candida: a mini review. Oral Dis. 2008;14:582–590.
    1. Shin JH, Kee SJ, Shin MG, Kim SH, Shin DH, Lee SK, Suh SP, Ryang DW. Biofilm production by isolates of Candida species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol. 2002;40:1244–1248.
    1. Shinde RB, Chauhan NM, Raut JS, Karuppayil SM. Sensitization of Candida albicans biofilms to various antifungal drugs by cyclosporine A. Ann Clin Microbiol Antimicrob. 2012;11:27.
    1. Silva S, Henriques M, Oliveira R, Willams D, Azeredo J. In vitro biofilm activity of non-Candida albicans Candida species. Curr Microbiol. 2010;61:534–540.
    1. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, Cowen LE. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 2009;5:e1000532.
    1. Soto SM. Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence. 2013;4:223–229.
    1. Spoering AL, Lewis K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol. 2001;183:6746–6751.
    1. Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, Cain MT, Hamaker J, Mitchell AP, Andes DR. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog. 2012;8:e1002848.
    1. Tournu H, Van Dijck P. Candida biofilms and the host: models and new concepts for eradication. Int J Microbiol. 2012;2012:845352.
    1. Uppuluri P, Nett J, Heitman J, Andes D. Synergistic effect of calcineurin inhibitors and fluconazole against Candida albicans biofilms. Antimicrob Agents Chemother. 2008;52:1127–1132.
    1. Uppuluri P, Chaturvedi AK, López-Ribot JL. Design of a simple model of Candida albicans biofilms formed under conditions of flow: development, architecture, and drug resistance. Mycopathologia. 2009;168:101–109.
    1. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Köhler JR, Kadosh D, Lopez-Ribot JL. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 2010;6:e1000828.
    1. Uppuluri P, Srinivasan A, Ramasubramaniam AK, López-Ribot JL. Effects of fluconazole, amphotericin B, and caspofungin on Candida albicans biofilms under conditions of flow and on biofilm dispersion. Antimicrob Agents Chemother. 2011;55:3591–3593.
    1. Vediyappan G, Rossignol T, d’ Enfert C. Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother. 2010;54:2096–2111.
    1. Walraven CJ, Lee SA. Antifungal lock therapy. Antimicrob Agents Chemother. 2013;57:1–8.
    1. Watnick P, Kolter R. Biofilm, city of microbes. J Bacteriol. 2000;182:2675–2679.
    1. Wey SB, Mori M, Pfaller MA, Woolson RF, Wenzel RP. Hospital-acquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med. 1988;148:2642–2645.
    1. Wheeler RT, Fink GR. A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog. 2006;2:e35.
    1. White TC. 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. 1997;41:1482–1487.
    1. White TC, Marr KA, Bowden RA. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev. 1998;11:382–402.
    1. Wilson LS, Reyes CM, Stolpman M, Speckman J, Allen K, Beney J. The direct cost and incidence of systematic fungal infections. Value Health. 2002;5:26–34.
    1. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis. 2004;39:309–317.
    1. Xie Z, Thompson A, Sobue T, Kashieva H, Xu H, Vasilakos J, Dongari-Bagtzoglou A. Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. J Infect Dis. 2012;206:1936–1945.
    1. Yi S, Sahni N, Daniels KJ, Lu KL, Huang G, Srikantha T, Soll DR. Self-induction of a/a or alpha/alpha biofilms in Candida albicans is a pheromone-based paracrine system requiring switching. Eukaryot Cell. 2011;10:753–760.
    1. Yi S, Sahni N, Daniels KJ, Lu KL, Srikantha T, Huang G, Garnaas AM, Soll DR. Alternative mating type configurations (a/α versus a/a or α/α) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol. 2011;9:e1001117.
    1. Yu LH, Wei X, Ma M, Chen XJ, Xu SB. Possible inhibitory molecular mechanism of farnesol on the development of fluconazole resistance in Candida albicans biofilm. Antimicrob Agents Chemother. 2012;56:770–775.
    1. Zelante T, Lannitti RG, De Luca A, Arroyo J, Blanco N, Servillo G, Sanglard D, Reichard U, Palmer GE, Latgè JP, Puccetti P, Romani L. Sensing of mammalian IL-17A regulates fungal adaptation and virulence. Nat Commun. 2012;3:683.
    1. Zhou Y, Wang G, Li Y, Liu Y, Song Y, Zheng W, Zhang N, Hu X, Yan S, Jia J. In vitro interactions between aspirin and amphotericin B against planktonic cells and biofilm cells of Candida albicans and C. parapsilosis. Antimicrob Agents Chemother. 2012;56:3250–3260.

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