2,486
Views
363
CrossRef citations to date
0
Altmetric
Review Article

Our Current Understanding of Fungal Biofilms

, , , &
Pages 340-355 | Received 09 Mar 2009, Accepted 06 Aug 2009, Published online: 28 Oct 2009

References

  • Adam B, Baillie GS, Douglas LJ. (2002). Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol, 51, 344–9.
  • Agus S, Spektor S, Israel Z. (2000). CNS granulomatosis in a child with chronic granulomatous disease. Br J Neurosurg, 14, 59–61.
  • Al-Dhaheri RS, Douglas LJ. (2008). Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob Agents Chemother, 52, 1884–7.
  • Alem MA, Oteef MD, Flowers TH, Douglas LJ. (2006). Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot Cell, 5, 1770–9.
  • Al-Fattani MA, Douglas LJ. (2004). Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother, 48, 3291–7.
  • 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.
  • Alvarez M, Saylor C, Casadevall A. (2008). Antibody action after phagocytosis promotes Cryptococcus neoformans and Cryptococcus gattii macrophage exocytosis with biofilm-like microcolony formation. Cell Microbiol, 10, 1622–33.
  • Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A. (2004). Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun, 72, 6023–31.
  • Bach MC, Tally PW, Godofsky EW. (1997). Use of cerebrospinal fluid shunts in patients having acquired immunodeficiency syndrome with cryptococcal meningitis and uncontrollable intracranial hypertension. Neurosurgery, 41, 1280–2; discussion 1282–3.
  • Bachmann SP, Ramage G, VandeWalle K, Patterson TF, Wickes BL, Lopez-Ribot JL. (2003). Antifungal combinations against Candida albicans biofilms in vitro. Antimicrob Agents Chemother, 47, 3657–9.
  • Bachmann SP, VandeWalle K, Ramage G, Patterson TF, Wickes BL, Graybill JR, Lopez-Ribot JL. (2002). In vitro activity of caspofungin against Candida albicans biofilms. Antimicrob Agents Chemother, 46, 3591–6.
  • Baillie GS, Douglas LJ. (1998a). Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother, 42, 1900–5.
  • Baillie GS, Douglas LJ. (1998b). Iron-limited biofilms of Candida albicans and their susceptibility to amphotericin. B Antimicrob Agents Chemother, 42, 2146–9.
  • Baillie GS, Douglas LJ. (1999). Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol, 48, 671–9.
  • Baillie GS, Douglas LJ. (2000). Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother, 46, 397–403.
  • Banerjee M, Thompson DS, Lazzell A, Carlisle PL, Pierce C, Monteagudo C, Lopez-Ribot JL, Kadosh D. (2008). UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol Biol Cell, 19, 1354–65.
  • Banerjee U, Gupta K, Venugopal P. (1997). A case of prosthetic valve endocarditis caused by Cryptococcus neoformans var neoformans. J Med Vet Mycol, 35, 139–41.
  • Bates S, Hughes HB, Munro CA, Thomas WP, MacCallum DM, Bertram G, Atrih A, Ferguson MA, Brown AJ, Odds FC, Gow NA. (2006). Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem, 281, 90–8.
  • Bates S, MacCallum DM, Bertram G, Munro CA, Hughes HB, Buurman ET, Brown AJ, Odds FC, Gow NA. (2005). Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J Biol Chem, 280, 23408–15.
  • Beauvais A, Bruneau JM, Mol PC, Buitrago MJ, Legrand R, Latge JP. (2001). Glucan synthase complex of Aspergillus fumigatus. J Bacteriol, 183, 2273–9.
  • Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, Henry C, Paris S, Mallet A, Prevost MC, Latge JP. (2007). An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol, 9, 1588–600.
  • Blankenship JR, Mitchell AP. (2006). How to build a biofilm: A fungal perspective. Curr Opin Microbiol, 9, 588–94.
  • Braun DK, Janssen DA, Marcus JR, Kauffman CA. (1994). Cryptococcal infection of a prosthetic dialysis fistula. Am J Kidney Dis, 24, 864–7.
  • Bruce AS, Kerry RM, Norman P, Stockley I. (2001). Fluconazole-impregnated beads in the management of fungal infection of prosthetic joints. J Bone Joint Surg Br, 83, 183–4.
  • Calderone R. (2002). Candida and Candidiasis. ASM Press, Washington, DC.
  • Cannizzo FT, Eraso E, Ezkurra PA, Villar-Vidal M, Bollo E, Castella G, Cabanes FJ, Vidotto V, Quindos G. (2007). Biofilm development by clinical isolates of Malassezia pachydermatis. Med Mycol, 45, 357–61.
  • Cao YY, Cao YB, Xu Z, Ying K, Li Y, Xie Y, Zhu ZY, Chen WS, Jiang YY. (2005). cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol. Antimicrob Agents Chemother, 49, 584–9.
  • Carter JE, Laurini JA, Evans TN, Estrada B. (2008). Neonatal Candida parapsilosis meningitis and empyema related to epidural migration of a central venous catheter. Clin Neurol Neurosurg 110, 614–8.
  • Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. (2001a). Biofilm formation by the fungal pathogen Candida albicans: Development, architecture, drug resistance. J Bacteriol, 183, 5385–94.
  • Chandra J, McCormick TS, Imamura Y, Mukherjee PK, Ghannoum MA. (2007). 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, 75, 2612–20.
  • Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, Douglas LJ, Ghannoum MA. (2001b). Antifungal resistance of Candida biofilms formed on denture acrylic in vitro. J Dent Res, 80, 903–8.
  • Chandra J, Patel JD, Li J, Zhou G, Mukherjee PK, McCormick TS, Anderson JM, Ghannoum MA. (2005). Modification of surface properties of biomaterials influences the ability of Candida albicans to form biofilms. Appl Environ Microbiol, 71, 8795–801.
  • Chen H, Fujita M, Feng Q, Clardy J, Fink GR. (2004). Tyrosol is a quorum-sensing molecule in Candida albicans. Proc Natl Acad Sci USA, 101, 5048–52.
  • Choi HW, Shin JH, Jung SI, Park KH, Cho D, Kee SJ, Shin MG, Suh SP, Ryang DW. (2007). Species-specific differences in the susceptibilities of biofilms formed by Candida bloodstream isolates to echinocandin antifungals. Antimicrob Agents Chemother, 51, 1520–3.
  • Coco BJ, Bagg J, Cross LJ, Jose A, Cross J, Ramage G. (2008). Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol Immunol, 23, 377–83.
  • Coco BJ. (2009). Antifungal resistance and pathogenesis of Candida albicans biofilms in patients with denture stomatitis. Glasgow: Glasgow Caledonian University.
  • Coghlan A. (1996). “Slime city”. New Scientist, 2045(15):32–6 .
  • Costerton JW, Irvin RT, Cheng KJ. (1981a). The bacterial glycocalyx in nature and disease. Annu Rev Microbiol, 35, 299–324.
  • Costerton JW, Irvin RT, Cheng KJ. (1981b). The role of bacterial surface structures in pathogenesis. Crit Rev Microbiol, 8, 303–38.
  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. (1995). Microbial biofilms. Annu Rev Microbiol, 49, 711–45.
  • Crump JA, Collignon PJ. (2000). Intravascular catheter-associated infections. Eur J Clin Microbiol Infect Dis, 19, 1–8.
  • Cushion MT, Collins MS, Linke MJ. (2009). Biofilm formation by Pneumocystis spp. Eukaryot Cell, 8, 197–206.
  • Daniels KJ, Srikantha T, Lockhart SR, Pujol C, Soll DR. (2006). Opaque cells signal white cells to form biofilms in Candida albicans. Embo J, 25, 2240–52.
  • D’Antonio D, Parruti G, Pontieri E, Di Bonaventura G, Manzoli L, Sferra R, Vetuschi A, Piccolomini R, Romano F, Staniscia T. (2004). Slime production by clinical isolates of Blastoschizomyces capitatus from patients with hematological malignancies and catheter-related fungemia. Eur J Clin Microbiol Infect Dis, 23, 787–9.
  • Darwazah A, Berg G, Faris B. (1999). Candida parapsilosis: An unusual organism causing prosthetic heart valve infective endocarditis. J Infect, 38, 130–1.
  • Davis LE, Cook G, Costerton JW. (2002). Biofilm on ventriculo-peritoneal shunt tubing as a cause of treatment failure in coccidioidal meningitis. Emerg Infect Dis, 8, 376–9.
  • de Beer D, Stoodley P, Lewandowski Z. (1994). Liquid flow in heterogeneous biofilms. Biotechnol Bioeng, 44, 636–41.
  • de Kievit TR, Iglewski BH. (2000). Bacterial quorum sensing in pathogenic relationships. Infect Immun, 68, 4839–49.
  • d’Enfert C. (2006). Biofilms and their role in the resistance of pathogenic Candida to antifungal agents. Curr Drug Targets, 7, 465–70.
  • Di Bonaventura G, Pompilio A, Picciani C, Lezzi M, D’Antonio D, Piccolomini R. (2006). Biofilm formation by the emerging fungal pathogen Trichosporon asahii: Development, architecture, antifungal resistance. Antimicrob Agents Chemother, 50, 3269–76.
  • Ding C, Butler G. (2007). Development of a gene knockout system in Candida parapsilosis reveals a conserved role for BCR1 in biofilm formation. Eukaryot Cell, 6, 1310–9.
  • Donlan RM. (2002). Biofilms: Microbial life on surfaces. Emerg Infect Dis, 8, 881–90.
  • Duffner F, Brandner S, Opitz H, Klier R, Grote EH. (1997). Primary Candida albicans empyema associated with epidural hematomas in craniocervical junction. Clin Neuropathol, 16, 143–6.
  • El-Azizi MA, Starks SE, Khardori N. (2004). Interactions of Candida albicans with other Candida spp and bacteria in the biofilms. J Appl Microbiol, 96, 1067–73.
  • Ellepola AN, Samaranayake LP. (1998). Adhesion of oral Candida albicans isolates to denture acrylic following limited exposure to antifungal agents. Arch Oral Biol, 43, 999–1007.
  • Elving GJ, van der Mei H, Busscher H, van Weissenbruch R, Albers F. (2003). Influence of different combinations of bacteria and yeasts in voice prosthesis biofilms on air flow resistance. Antonie Van Leeuwenhoek, 83, 45–55.
  • Emerson RJ t, Camesano TA. (2004). Nanoscale investigation of pathogenic microbial adhesion to a biomaterial. Appl Environ Microbiol, 70, 6012–22.
  • Enjalbert B, Whiteway M. (2005). Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell, 4, 1203–10.
  • Garcia-Sanchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM, d’Enfert C. (2004). Candida albicans biofilms: A developmental state associated with specific and stable gene expression patterns. Eukaryot Cell, 3, 536–45.
  • Garcia-Sanchez S, Mavor AL, Russell CL, Argimon S, Dennison P, Enjalbert B, Brown AJ. (2005). Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans. Mol Biol Cell, 16, 2913–25.
  • Ghigo JM. (2003). Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res Microbiol, 154, 1–8.
  • Granger BL, Flenniken ML, Davis DA, Mitchell AP, Cutler JE. (2005). Yeast wall protein 1 of Candida albicans. Microbiology, 151, 1631–44.
  • Green CB, Cheng G, Chandra J, Mukherjee P, Ghannoum MA, Hoyer LL. (2004). RT-PCR detection of Candida albicans ALS gene expression in the reconstituted human epithelium (RHE) model of oral candidiasis and in model biofilms. Microbiology, 150, 267–75.
  • Hawser S. (1996). Adhesion of different Candida spp to plastic: XTT formazan determinations. J Med Vet Mycol, 34, 407–10.
  • Hawser SP, Baillie GS, Douglas LJ. (1998). Production of extra-cellular matrix by Candida albicans biofilms. J Med Microbiol, 47, 253–6.
  • Hawser SP, Douglas LJ. (1994). Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun, 62, 915–21.
  • Hiller E, Heine S, Brunner H, Rupp S. (2007). Candida albicans Sun41p, a putative glycosidase, is involved in morphogenesis, cell wall biogenesis, biofilm formation. Eukaryot Cell, 6, 2056–65.
  • Hogan DA, Vik A, Kolter R. (2004). A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol, 54, 1212–23.
  • Holmes AR, Bandara BM, Cannon RD. (2002). Saliva promotes Candida albicans adherence to human epithelial cells. J Dent Res, 81, 28–32.
  • Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW. (2001). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol, 67, 2982–92.
  • Infante-Cossio P, Martinez-de-Fuentes R, Torres-Carranza E, Gutierrez-Perez JL. (2007). Inflammatory papillary hyperplasia of the palate: Treatment with carbon dioxide laser, followed by restoration with an implant-supported prosthesis. Br J Oral Maxillofac Surg, 45, 658–60.
  • Jabra-Rizk MA, Falkler WA, Meiller TF. (2004). Fungal biofilms and drug resistance. Emerg Infect Dis, 10, 14–9.
  • Jarvensivu A, Hietanen J, Rautemaa R, Sorsa T, Richardson M. (2004). Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo. Oral Dis, 10, 106–12.
  • Joly V, Belmatoug N, Leperre A, Robert J, Jault F, Carbon C, Yeni P. (1997). Pacemaker endocarditis due to Candida albicans: Case report and review. Clin Infect Dis, 25, 1359–62.
  • Joubert LM, Wolfaardt GM, Botha A. (2006). Microbial exopolymers link predator and prey in a model yeast biofilm system. Microb Ecol, 52, 187–97.
  • Kadosh D, Johnson AD. (2005). Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: A genome-wide analysis. Mol Biol Cell, 16, 2903–12.
  • Kelly MT, MacCallum DM, Clancy SD, Odds FC, Brown AJ, Butler G. (2004). The Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence. Mol Microbiol, 53, 969–83.
  • Khot PD, Suci PA, Miller RL, Nelson RD, Tyler BJ. (2006). 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, 50, 3708–16.
  • Klotz SA, Gaur NK, De Armond R, Sheppard D, Khardori N, Edwards JE, Jr, Lipke PN, El-Azizi M. (2007). Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med Mycol, 45, 363–70.
  • Kojic EM, Darouiche RO. (2004). Candida infections of medical devices. Clin Microbiol Rev, 17, 255–67.
  • Krueger KE, Ghosh AK, Krom BP, Cihlar RL. (2004). Deletion of the NOT4 gene impairs hyphal development and pathogenicity in Candida albicans. Microbiology, 150, 229–40.
  • Kruppa M, Krom BP, Chauhan N, Bambach AV, Cihlar RL, Calderone RA. (2004). The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot Cell, 3, 1062–5.
  • Krzossok S, Birck R, Henke S, Hof H, van der Woude FJ, Braun C. (2004). Trichosporon asahii infection of a dialysis PTFE arteriovenous graft. Clin Nephrol, 62, 66–8.
  • Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA. (2003). Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol, 41, 506–8.
  • Kuhn DM, Chandra J, Mukherjee PK, Ghannoum MA. (2002). Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun, 70, 878–88.
  • 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, 1773–80.
  • Kuhn DM, Ghannoum MA. (2004). Candida biofilms: Antifungal resistance and emerging therapeutic options. Curr Opin Investig Drugs 5, 186–97.
  • Kumamoto CA, Vinces MD. (2005). Alternative Candida albicans lifestyles: Growth on surfaces. Annu Rev Microbiol, 59, 113–33.
  • Kumamoto CA. (2002). Candida biofilms. Curr Opin Microbiol 5, 608–11.
  • Kumamoto CA. (2005). A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci USA, 102, 5576–81.
  • Kurup A, Janardhan MN, Seng TY. (2000). Candida tropicalis pacemaker endocarditis. J Infect, 41, 275–6.
  • LaFleur MD, Kumamoto CA, Lewis K. (2006). Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother, 50, 3839–46.
  • Lamfon H, Porter SR, McCullough M, Pratten J. (2003). Formation of Candida albicans biofilms on non-shedding oral surfaces. Eur J Oral Sci, 111, 465–71.
  • Langer P, Kassim RA, Macari GS, Saleh KJ. (2003). Aspergillus infection after total knee arthroplasty. Am J Orthop, 32, 402–4.
  • Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE. (1991). Optical sectioning of microbial biofilms. J Bacteriol, 173, 6558–67.
  • Lepak A, Nett J, Lincoln L, Marchillo K, Andes D. (2006). 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, 50, 1311–9.
  • Lermann U, Morschhauser J. (2008). Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology, 154, 3281–95.
  • Lewis K. (2008). Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol, 322, 107–31.
  • Lewis RE, Lo HJ, Raad II, Kontoyiannis DP. (2002). Lack of catheter infection by the efg1/efg1 cph1/cph1 double-null mutant, a Candida albicans strain that is defective in filamentous growth. Antimicrob Agents Chemother, 46, 1153–5.
  • Li F, Palecek SP. (2003). EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell, 2, 1266–73.
  • Li F, Palecek SP. (2008). Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions. Microbiology, 154, 1193–203.
  • Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P, Andes D, Palecek SP. (2007). Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell, 6, 931–9.
  • Liu TT, Lee RE, Barker KS, Wei L, Homayouni R, Rogers PD. (2005). Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Chemother, 49, 2226–36.
  • Lopez-Ribot JL. (2005). Candida albicans biofilms: More than filamentation. Curr Biol, 15, R453–5.
  • Lusini M, Chello M, Pollari F, Covino E. (2008). Giant vegetation in prosthetic valve Candida albicans endocarditis. Eur J Cardiothorac Surg, 34, 456.
  • Lye DC, Hughes A, O’Brien D, Athan E. (2005). Candida glabrata prosthetic valve endocarditis treated successfully with fluconazole plus caspofungin without surgery: A case report and literature review. Eur J Clin Microbiol Infect Dis, 24, 753–5.
  • Machida K, Tanaka T. (1999). Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F(0)F(1)-ATPase in yeast. FEBS Lett, 462, 108–12.
  • Martinez LR, Bryan RA, Apostolidis C, Morgenstern A, Casadevall A, Dadachova E. (2006). Antibody-guided alpha radiation effectively damages fungal biofilms. Antimicrob Agents Chemother, 50, 2132–6.
  • Martinez LR, Casadevall A. (2005). Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect Immun, 73, 6350–62.
  • Martinez LR, Casadevall A. (2006). Cryptococcus neoformans cells in biofilms are less susceptible than planktonic cells to antimicrobial molecules produced by the innate immune system. Infect Immun, 74, 6118–23.
  • Martinez LR, Casadevall A. (2006). Susceptibility of Cryptococcus neoformans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother, 50, 1021–33.
  • Martinez LR, Casadevall A. (2007). Cryptococcus neoformans biofilm formation depends on surface support and carbon source and reduces fungal cell susceptibility to heat, cold, and UV light. Appl Environ Microbiol, 73, 4592–601.
  • Martinez LR, Christaki E, Casadevall A. (2006). Specific antibody to Cryptococcus neoformans glucurunoxylomannan antagonizes antifungal drug action against cryptococcal biofilms in vitro. J Infect Dis, 194, 261–6.
  • Martins M, Henriques M, Azeredo J, Rocha SM, Coimbra MA, Oliveira R. (2007). Morphogenesis control in Candida albicans and Candida dubliniensis through signaling molecules produced by planktonic and biofilm cells. Eukaryot Cell, 6, 2429–36.
  • Mateus C, Crow Jr SA, Ahearn DG. (2004). Adherence of Candida albicans to silicone induces immediate enhanced tolerance to fluconazole. Antimicrob Agents Chemother, 48, 3358–66.
  • Mercier-Bonin M, Ouazzani K, Schmitz P, Lorthois S. (2004). Study of bioadhesion on a flat plate with a yeast/glass model system. J Colloid Interface Sci, 271, 342–50.
  • Miller MB, Bassler BL. (2001). Quorum sensing in bacteria. Annu Rev Microbiol, 55, 165–99.
  • Mowat E, Butcher J, Lang S, Williams C, Ramage G. (2007). Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol, 56, 1205–12.
  • Mowat E, Lang S, Williams C, McCulloch E, Jones B, Ramage G. (2008). Phase-dependent antifungal activity against Aspergillus fumigatus developing multicellular filamentous biofilms. J Antimicrob Chemother 62, 1281–4.
  • Mowat E, Ward PN, Patterson TF, Williams C, Ramage G. (2008). The potential role of AfuMdr4 in azole resistance during Aspergillus fumigatus multicellular growth, ICAAC. Vol M-2190, Washington DC.
  • Mowat E, Williams C, Jones B, McChlery S, Ramage G. (2008). The characteristics of Aspergillus fumigatus mycetoma development: Is this a biofilm? Med Mycol, 1–7.
  • Mukherjee PK, Chand DV, Chandra J, Anderson JM, Ghannoum MA. (2008). Shear stress modulates the thickness and architecture of Candida albicans biofilms in a phase-dependent manner Mycoses Epub ahead of print (19076284).
  • 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, 4333–40.
  • Mukherjee PK, Chandra J. (2004). Candida biofilm resistance. Drug Resist Updat, 7, 301–9.
  • Mukherjee PK, Mohamed S, Chandra J, Kuhn D, Liu S, Antar OS, Munyon R, Mitchell AP, Andes D, Chance MR, Rouabhia M, Ghannoum MA. (2006). Alcohol dehydrogenase restricts the ability of the pathogen Candida albicans to form a biofilm on catheter surfaces through an ethanol-based mechanism. Infect Immun, 74, 3804–16.
  • Mukherjee PK, Zhou G, Munyon R, Ghannoum MA. (2005). Candida biofilm: A well-designed protected environment. Med Mycol, 43, 191–208.
  • Munro CA, Bates S, Buurman ET, Hughes HB, Maccallum DM, Bertram G, Atrih A, Ferguson MA, Bain JM, Brand A, Hamilton S, Westwater C, Thomson LM, Brown AJ, Odds FC, Gow NA. (2005). Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1,2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J Biol Chem, 280, 1051–60.
  • Murillo LA, Newport G, Lan CY, Habelitz S, Dungan J, Agabian NM. (2005). Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell, 4, 1562–73.
  • Nagaraja PA, Mathew T, Shetty DP. (2005). Candida tropicalis causing prosthetic valve endocarditis. Indian J Med Microbiol, 23, 139–40.
  • Naglik J, Albrecht A, Bader O, Hube B. (2004). Candida albicans proteinases and host/pathogen interactions. Cell Microbiol, 6, 915–26.
  • Naglik JR, Challacombe SJ, Hube B. (2003). Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev, 67, 400–28, table of contents.
  • Naglik JR, Fostira F, Ruprai J, Staab JF, Challacombe SJ, Sundstrom P. (2006). Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J Med Microbiol, 55, 1323–7.
  • Naglik JR, Moyes D, Makwana J, Kanzaria P, Tsichlaki E, Weindl G, Tappuni AR, Rodgers CA, Woodman AJ, Challacombe SJ, Schaller M, Hube B. (2008). Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology, 154, 3266–80.
  • Naglik JR, Rodgers CA, Shirlaw PJ, Dobbie JL, Fernandes-Naglik, Greenspan D, Agabian N, Challacombe SJ. (2003). Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J Infect Dis, 188, 469–79.
  • Nealson KH, Platt T, Hastings JW. (1970). Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol, 104, 313–22.
  • Nett J, Andes D. (2006). Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol, 9, 340–5.
  • 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, 510–20.
  • Nikawa H, Jin C, Makihira S, Egusa H, Hamada T, Kumagai H. (2003). Biofilm formation of Candida albicans on the surfaces of deteriorated soft denture lining materials caused by denture cleansers in vitro. J Oral Rehabil, 30, 243–50.
  • Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. (2006). Critical role of Bcr1-dependent adhesins in C albicans biofilm formation in vitro and in vivo. PLoS Pathog, 2, e63.
  • Nobile CJ, Mitchell AP. (2005). Regulation of cell-surface genes and biofilm formation by the C albicans transcription factor Bcr1p. Curr Biol, 15, 1150–5.
  • Nobile CJ, Nett JE, Andes DR, Mitchell AP. (2006). Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell, 5, 1604–10.
  • Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR, Mitchell AP. (2008). Complementary adhesin function in C albicans biofilm formation. Curr Biol, 18, 1017–24.
  • Norice CT, Smith Jr FJ, Solis N, Filler SG, Mitchell AP. (2007). Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot Cell, 6, 2046–55.
  • Odds F. (1988). Candida and Candidosis. 2nd ed. Bailliere Tindall, London.
  • Oh KB, Miyazawa H, Naito T, Matsuoka H. (2001). Purification and characterization of an autoregulatory substance capable of regulating the morphological transition in Candida albicans. Proc Natl Acad Sci USA, 98, 4664–8.
  • Parahitiyawa NB, Samaranayake YH, Samaranayake LP, Ye J, Tsang PW, Cheung BP, Yau JY, Yeung SK. (2006). Interspecies variation in Candida biofilm formation studied using the Calgary biofilm device. Apmis, 114, 298–306.
  • Penk A, Pittrow L. (1999). Role of fluconazole in the long-term suppressive therapy of fungal infections in patients with artificial implants. Mycoses, 42(Suppl 2), 91–6.
  • Perumal P, Mekala S, Chaffin WL. (2007). Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother, 51, 2454–63.
  • Pierce CG, Thomas DP, Lopez-Ribot JL. (2008). Effect of tunicamycin on Candida albicans biofilm formation and maintenance. J Antimicrob Chemother.
  • Pierce CG, Uppuluri P, Tristan AR, Wormley Jr FL, Mowat E, Ramage G, Lopez-Ribot JL. (2008). A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc, 3, 1494–500.
  • Pini G, Faggi E, Donato R, Fanci R. (2005). Isolation of Trichosporon in a hematology ward. Mycoses, 48, 45–9.
  • Radford DR, Challacombe SJ, Walter JD. (1999). Denture plaque and adherence of Candida albicans to denture-base materials in vivo and in vitro. Crit Rev Oral Biol Med, 10, 99–116.
  • 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, 973–80.
  • Ramage G, Martinez JP, Lopez-Ribot JL. (2006). Candida biofilms on implanted biomaterials: A clinically significant problem. FEMS Yeast Res, 6, 979–86.
  • Ramage G, Saville SP, Thomas DP, Lopez-Ribot JL. (2005). Candida biofilms: An update. Eukaryot Cell, 4, 633–8.
  • 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, 5459–63.
  • Ramage G, Tomsett K, Wickes BL, Lopez-Ribot JL, Redding SW. (2004). Denture stomatitis: A role for Candida biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 98, 53–9.
  • Ramage G, VandeWalle K, Bachmann SP, Wickes BL, Lopez-Ribot JL. (2002c). In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob Agents Chemother, 46, 3634–6.
  • Ramage G, VandeWalle K, Lopez-Ribot JL, Wickes BL. (2002d). The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett, 214, 95–100.
  • Ramage G, Vandewalle K, Wickes BL, Lopez-Ribot JL. (2001). Characteristics of biofilm formation by Candida albicans. Rev Iberoam Micol, 18, 163–70.
  • Ramage G, VandeWalle K, Wickes BL, Lopez-Ribot JL. (2001). Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother, 45, 2475–9.
  • Ramage G, Wickes BL, Lopez-Ribot JL. (2008). A seed and feed model for the formation of Candida albicans biofilms under flow conditions using an improved modified Robbins device. Rev Iberoam Micol, 25, 37–40.
  • Rasmussen TB, Givskov M. (2006). Quorum sensing inhibitors: A bargain of effects. Microbiology, 152, 895–904.
  • Reddy BT, Torres HA, Kontoyiannis DP. (2002). Breast implant infection caused by Trichosporon beigelii. Scand J Infect Dis, 34, 143–4.
  • Reynolds TB, Fink GR. (2001). Bakers’ yeast, a model for fungal biofilm formation. Science, 291, 878–81.
  • Richard ML, Nobile CJ, Bruno VM, Mitchell AP. (2005). Candida albicans biofilm-defective mutants. Eukaryot Cell, 4, 1493–502.
  • Roger PM, Boissy C, Gari-Toussaint M, Foucher R, Mondain V, Vandenbos F, le Fichoux Y, Michiels JF, Dellamonica P. (2000). Medical treatment of a pacemaker endocarditis due to Candida albicans and to Candida glabrata. J Infect, 41, 176–8.
  • Rosenblatt WB, Pollock A. (1997). Aspergillus flavus cultured from a saline-filled implant. Plast Reconstr Surg, 99, 1470–2.
  • Saray A, Kilic D, Kaygusuz S, Boyunaga H, Ozluk O. (2004). Fungal growth inside saline-filled implants and the role of injection ports in fungal translocation: In vitro study. Plast Reconstr Surg, 114, 1170–8.
  • Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. (2003). Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell, 2, 1053–60.
  • Saville SP, Thomas DP, Lopez Ribot JL. (2006). A role for Efg1p in Candida albicans interactions with extracellular matrices. FEMS Microbiol Lett, 256, 151–8.
  • Schinabeck MK, Long LA, Hossain MA, Chandra J, Mukherjee PK, Mohamed S, Ghannoum MA. (2004). Rabbit model of Candida albicans biofilm infection: Liposomal amphotericin B antifungal lock therapy. Antimicrob Agents Chemother, 48, 1727–32.
  • Seidler MJ, Salvenmoser S, Muller FM. (2008). Aspergillus fumigatus forms biofilms with reduced antifungal drug susceptibility on bronchial epithelial cells. Antimicrob Agents Chemother, 52, 4130–6.
  • Semighini CP, Hornby JM, Dumitru R, Nickerson KW, Harris SD. (2006). Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol, 59, 753–64.
  • Semighini CP, Murray N, Harris SD. (2008). Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol Lett, 279, 259–64.
  • Sen BH, Safavi KE, Spangberg LS. (1997). Colonization of Candida albicans on cleaned human dental hard tissues. Arch Oral Biol, 42, 513–20.
  • Shin JH, Kee SJ, Shin MG, Kim SH, Shin DH, Lee SK, Suh SP, Ryang DW. (2002). Biofilm production by isolates of Candida species recovered from nonneutropenic patients: Comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol, 40, 1244–8.
  • Shuford JA, Rouse MS, Piper KE, Steckelberg JM, Patel R. (2006). Evaluation of caspofungin and amphotericin B deoxycholate against Candida albicans biofilms in an experimental intravascular catheter infection model. J Infect Dis, 194, 710–3.
  • Sohn K, Urban C, Brunner H, Rupp S. (2003). EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol, 47, 89–102.
  • Soll DR. (2008). Candida biofilms: Is adhesion sexy? Curr Biol, 18, R717–20.
  • Stewart PS, Costerton JW. (2001). Antibiotic resistance of bacteria in biofilms. Lancet, 358, 135–8.
  • Tellier R, Krajden M, Grigoriew GA, Campbell I. (1992). Innovative endpoint determination system for antifungal susceptibility testing of yeasts. Antimicrob Agents Chemother, 36, 1619–25.
  • Thein ZM, Samaranayake YH, Samaranayake LP. (2006). Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch Oral Biol, 51, 672–80.
  • Thein ZM, Samaranayake YH, Samaranayake LP. (2007). In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch Oral Biol, 52, 761–7.
  • Thomas DP, Bachmann SP, Lopez-Ribot JL. (2006). Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics, 6, 5795–804.
  • Tre-Hardy M, Vanderbist F, Traore H, Devleeschouwer MJ. (2008). In vitro activity of antibiotic combinations against Pseudomonas aeruginosa biofilm and planktonic cultures. Int J Antimicrob Agents, 31, 329–36.
  • Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, de Gaetano Donati K, La Sorda M, Spanu T, Fadda G, Cauda R, Sanguinetti M. (2007). Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol, 45, 1843–50.
  • Vediyappan G, Chaffin WL. (2006). Non-glucan attached proteins of Candida albicans biofilm formed on various surfaces. Mycopathologia, 161, 3–10.
  • Venturi V. (2006). Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev, 30, 274–91.
  • Villena GK, Gutierrez-Correa M. (2007). Morphological patterns of Aspergillus niger biofilms and pellets related to lignocellulolytic enzyme productivities. Lett Appl Microbiol, 45, 231–7.
  • Villena GK, Moreno P, Gutierrez-Correa M. (2001). Cellulase production by fungal biofilms on polyester cloth. Agro-food-industry Hitech, 12, 32–35.
  • Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR, DeLeo FR, Otto M. (2004). Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol, 6, 269–75.
  • Wada M, Baba H, Imura S. (1998). Prosthetic knee Candida parapsilosis infection. J Arthroplasty, 13, 479–82.
  • Walsh TJ, Schlegel R, Moody MM, Costerton JW, Salcman M. (1986). Ventriculoatrial shunt infection due to Cryptococcus neoformans: An ultrastructural and quantitative microbiological study. Neurosurgery, 18, 373–5.
  • Wang M, Mukherjee PK, Chandra J, Lattif AA, McCormick TS, Ghannoum MA. (2008). Characterization and partial purification of Candida albicans. Secretory IL-12 Inhibitory Factor BMC Microbiol, 8, 31.
  • Weindl G, Naglik JR, Kaesler S, Biedermann T, Hube B, Korting HC, Schaller M. (2007). Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J Clin Invest, 117, 3664–72.
  • Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. (2004). Nosocomial bloodstream infections in US hospitals: Analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis, 39, 309–17.
  • Won Song J, Shin JH, Kee SJ, Kim SH, Shin MG, Suh SP, Ryang DW. (2008). Expression of CgCDR1, CgCDR2, and CgERG11 in Candida glabrata biofilms formed by bloodstream isolates. Med Mycol, 1–4.
  • Yeater KM, Chandra J, Cheng G, Mukherjee PK, Zhao X, Rodriguez-Zas SL, Kwast KE, Ghannoum MA, Hoyer LL. (2007). Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology, 153, 2373–85.
  • Young VL, Hertl MC, Murray PR, Jensen J, Witt H, Schorr MW. (1997). Microbial growth inside saline-filled breast implants. Plast Reconstr Surg, 100, 182–96.
  • Zhao X, Oh SH, Yeater KM, Hoyer LL. (2005). Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology, 151, 1619–30.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.