Interaction of Candida albicans biofilms with antifungals: Transcriptional response and binding of antifungals to beta-glucans

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 5, 2010, Pages 2096-2111

  Vediyappan, Govindsamy ^a,b   Rossignol, Tristan ^a   D'Enfert, Christophe ^a  

^a INSTITUT PASTEUR   (France)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALS3 PROTEIN; AMPHOTERICIN B; BETA GLUCAN; CASPOFUNGIN; FLUCONAZOLE; FUNGAL PROTEIN; HWP1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CANDIDA ALBICANS; CARBOHYDRATE SYNTHESIS; DRUG BINDING; DRUG EXPOSURE; EXTRACELLULAR MATRIX; FUNGAL GENE; FUNGUS CULTURE; FUNGUS HYPHAE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; LETHALITY; NONHUMAN; PLANKTON; PRIORITY JOURNAL; UPREGULATION;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; BETA-GLUCANS; BIOFILMS; CANDIDA ALBICANS; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; EXTRACELLULAR MATRIX PROTEINS; FLUCONAZOLE; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; LUCIFERASES; MEMBRANE GLYCOPROTEINS; TRANSCRIPTION, GENETIC;

EID: 77951233308     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01638-09     Document Type: Article

References (77)

1. Al-Dhaheri, R. S., and L. J. Douglas. 2008. Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob. Agents Chemother. 52:1884-1887.
2. Al-Fattani, M. A., and L. J. Douglas. 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J. Med. Microbiol. 55:999-1008.
3. Al-Fattani, M. A., and L. J. Douglas. 2004. Penetration of Candida biofilms by antifungal agents. Antimicrob. Agents Chemother. 48:3291-3297.
4. Anderson, G. G., and G. A. O'Toole. 2008. Innate and induced resistance mechanisms of bacterial biofilms. Curr. Top. Microbiol. Immunol. 322:85-105.
5. Bachmann, S. P., K. VandeWalle, G. Ramage, T. F. Patterson, B. L. Wickes, J. R. Graybill, and J. L. Lopez-Ribot. 2002. In vitro activity of caspofungin against Candida albicans biofilms. Antimicrob. Agents Chemother. 46:3591-3596.
6. Baillie, G. S., and L. J. Douglas. 1999. Candida biofilms and their susceptibility to antifungal agents. Methods Enzymol. 310:644-656.
7. Baillie, G. S., and L. J. Douglas. 1998. Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob. Agents Chemother. 42:1900-1905.
8. Baillie, G. S., and L. J. Douglas. 2000. Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J. Antimicrob. Chemother. 46:397-403.
9. Banerjee, M., D. S. Thompson, A. Lazzell, P. L. Carlisle, C. Pierce, C. Monteagudo, J. L. Lopez-Ribot, and D. Kadosh. 2008. UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol. Biol. Cell 19:1354-1365.
10. Barker, K. S., S. Crisp, N. Wiederhold, R. E. Lewis, B. Bareither, J. Eckstein, R. Barbuch, M. Bard, and P. D. Rogers. 2004. Genome-wide expression profiling reveals genes associated with amphotericin B and fluconazole resistance in experimentally induced antifungal resistant isolates of Candida albicans. J. Antimicrob. Chemother. 54:376-385.
11. Blankenship, J. R., and A. P. Mitchell. 2006. How to build a biofilm: a fungal perspective. Curr. Opin. Microbiol. 9:588-594.
12. Carlisle, P. L., M. Banerjee, A. Lazzell, C. Monteagudo, J. L. Lopez-Ribot, and D. Kadosh. 2009. Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc. Natl. Acad. Sci. U. S. A. 106:599-604.
13. Chandra, J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick, and M. A. Ghannoum. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183:5385-5394.
14. Chandra, J., P. K. Mukherjee, S. D. Leidich, F. F. Faddoul, L. L. Hoyer, L. J. Douglas, and M. A. Ghannoum. 2001. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J. Dent. Res. 80:903-908.
15. CLSI/NCCLS. 1997. Reference method for broth dilution antifungal susceptibility testing of yeasts. M27-A. NCCLS, Wayne, PA.
16. Cowen, L. E., and W. J. Steinbach. 2008. Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot. Cell 7:747-764.
17. d'Enfert, C. 2006. Biofilms and their role in the resistance of pathogenic Candida to antifungal agents. Curr. Drug Targets 7:465-470.
18. Douglas, L. J. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11:30-36.
19. Ene, I. V., and R. J. Bennett. 2009. Hwp1 and related adhesins contribute to both mating and biofilm formation in Candida albicans. Eukaryot. Cell 8:1909-1913.
20. Enjalbert, B., A. Rachini, G. Vediyappan, D. Pietrella, R. Spaccapelo, A. Vecchiarelli, A. J. Brown, and C. d'Enfert. 2009. A multifunctional, synthetic Gaussia princeps luciferase reporter for live imaging of Candida albicans infections. Infect. Immun. 77:4847-4858.
21. Filler, S. G., and B. J. Kuhlberg. 2002. Deep-seated candidal infections, p. 341-348. In R. Calderone (ed.), Candida and candidiasis. ASM Press, Washington, DC.
22. Firon, A., S. Aubert, I. Iraqui, S. Guadagnini, S. Goyard, M. C. Prevost, G. Janbon, and C. d'Enfert. 2007. The SUN41 and SUN42 genes are essential for cell separation in Candida albicans. Mol. Microbiol. 66:1256-1275.
23. Fonzi, W. A. 1999. PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of beta-1,3- and beta-1,6-glucans. J. Bacteriol. 181:7070-7079.
24. Garcia-Sánchez, S., S. Aubert, I. Iraqui, G. Janbon, J. M. Ghigo, and C. d'Enfert. 2004. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3:536-545.
25. Gillum, A. M., E. Y. Tsay, and D. R. Kirsch. 1984. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198:179-182.
26. Granger, B. L., M. L. Flenniken, D. A. Davis, A. P. Mitchell, and J. E. Cutler. 2005. Yeast wall protein 1 of Candida albicans. Microbiology 151:1631-1644.
27. Hawser, S. P., G. S. Baillie, and L. J. Douglas. 1998. Production of extracellular matrix by Candida albicans biofilms. J. Med. Microbiol. 47:253-256.
28. Hawser, S. P., and L. J. Douglas. 1995. Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob. Agents Chemother. 39:2128-2131.
29. Henry-Stanley, M. J., R. M. Garni, and C. L. Wells. 2004. Adaptation of FUN-1 and Calcofluor white stains to assess the ability of viable and nonviable yeast to adhere to and be internalized by cultured mammalian cells. J. Microbiol. Methods 59:289-292.
30. Honraet, K., E. Goetghebeur, and H. J. Nelis. 2005. Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J. Microbiol. Methods 63:287-295.
31. Hoyle, B. D., and J. W. Costerton. 1991. Bacterial resistance to antibiotics: the role of biofilms. Prog. Drug Res. 37:91-105.
32. Hoyle, B. D., J. Jass, and J. W. Costerton. 1990. The biofilm glycocalyx as a resistance factor. J. Antimicrob. Chemother. 26:1-5.
33. Kawabata, M., M. Onda, and T. Mita. 2001. Effect of aggregation of amphotericin B on lysophosphatidylcholine micelles as related to its complex formation with cholesterol or ergosterol. J. Biochem. 129:725-732.
34. Kojic, E. M., and R. O. Darouiche. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17:255-267.
35. Kuhn, D. M., T. George, J. Chandra, P. K. Mukherjee, and M. A. Ghannoum. 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob. Agents Chemother. 46:1773-1780.
36. Kuhn, D. M., and M. A. Ghannoum. 2004. Candida biofilms: antifungal resistance and emerging therapeutic options. Curr. Opin. Investig. Drugs 5:186-197.
37. Kullberg, B. J., and A. M. Oude Lashof. 2002. Epidemiology of opportunistic invasive mycoses. Eur. J. Med. Res. 7:183-191.
38. LaFleur, M. D., C. A. Kumamoto, and K. Lewis. 2006. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob. Agents Chemother. 50:3839-3846.
39. Liu, T. T., R. E. Lee, K. S. Barker, R. E. Lee, L. Wei, R. Homayouni, and P. D. Rogers. 2005. Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob. Agents Chemother. 49:2226-2236.
40. Maertens, J., M. Vrebos, and M. Boogaerts. 2001. Assessing risk factors for systemic fungal infections. Eur. J. Cancer Care (Engl.) 10:56-62.
41. Mah, T. F., B. Pitts, B. Pellock, G. C. Walker, P. S. Stewart, and G. A. O'Toole. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306-310.
42. Mermel, L. A., B. M. Farr, R. J. Sherertz, I. I. Raad, N. O'Grady, J. S. Harris, and D. E. Craven. 2001. Guidelines for the management of intravascular catheter-related infections. Clin. Infect. Dis. 32:1249-1272.
43. Mio, T., M. Adachi-Shimizu, Y. Tachibana, H. Tabuchi, S. B. Inoue, T. Yabe, T. Yamada-Okabe, M. Arisawa, T. Watanabe, and H. Yamada-Okabe. 1997. Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/FKS1 and its involvement in beta-1,3-glucan synthesis. J. Bacteriol. 179:4096-4105.
44. Moreno-Ruiz, E., G. Ortu, P. W. de Groot, F. Cottier, C. Loussert, M. C. Prevost, C. de Koster, F. M. Klis, S. Goyard, and C. d'Enfert. 2009. The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155:2004-2020.
45. Mukherjee, P. K., and J. Chandra. 2004. Candida biofilm resistance. Drug Resist. Updat. 7:301-309.
46. Mukherjee, P. K., J. Chandra, D. M. Kuhn, and M. A. Ghannoum. 2003. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71:4333-4340.
47. Mukherjee, P. K., G. Zhou, R. Munyon, and M. A. Ghannoum. 2005. Candida biofilm: a well-designed protected environment. Med. Mycol. 43:191-208.
48. Mulcahy, H., L. Charron-Mazenod, and S. Lewenza. 2008. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213.
49. Nett, J., L. Lincoln, K. Marchillo, R. Massey, K. Holoyda, B. Hoff, M. VanHandel, and D. Andes. 2007. Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob. Agents Chemother. 51:510-520.
50. Nobile, C. J., D. R. Andes, J. E. Nett, F. J. Smith, F. Yue, Q. T. Phan, J. E. Edwards, S. G. Filler, and A. P. Mitchell. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63.
51. Nobile, C. J., and A. P. Mitchell. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15:1150-1155.
52. Nobile, C. J., J. E. Nett, D. R. Andes, and A. P. Mitchell. 2006. Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot. Cell 5:1604-1610.
53. Nobile, C. J., H. A. Schneider, J. E. Nett, D. C. Sheppard, S. G. Filler, D. R. Andes, and A. P. Mitchell. 2008. Complementary adhesin function in C. albicans biofilm formation. Curr. Biol. 18:1017-1024.
54. Pappas, P. G., J. H. Rex, J. D. Sobel, S. G. Filler, W. E. Dismukes, T. J. Walsh, and J. E. Edwards. 2004. Guidelines for treatment of candidiasis. Clin. Infect. Dis. 38:161-189.
55. Pardini, G., P. W. De Groot, A. T. Coste, M. Karababa, F. M. Klis, C. G. de Koster, and D. Sanglard. 2006. The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J. Biol. Chem. 281:40399-40411.
56. Peeters, E., H. J. Nelis, and T. Coenye. 2008. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods 72:157-165.
57. Peltroche-Llacsahuanga, H., S. Goyard, C. d'Enfert, S. K. Prill, and J. F. Ernst. 2006. Protein O-mannosyltransferase isoforms regulate biofilm formation in Candida albicans. Antimicrob. Agents Chemother. 50:3488-3491.
58. Pfaller, M. A., R. N. Jones, G. V. Doern, A. C. Fluit, J. Verhoef, H. S. Sader, S. A. Messer, A. Houston, S. Coffman, and R. J. Hollis. 1999. International surveillance of bloodstream infections due to Candida species in the European SENTRY Program: species distribution and antifungal susceptibility including the investigational triazole and echinocandin agents. SENTRY Participant Group (Europe). Diagn. Microbiol. Infect. Dis. 35:19-25.
59. Ramage, G., S. Bachmann, T. F. Patterson, B. L. Wickes, and J. L. Lopez-Ribot. 2002. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J. Antimicrob. Chemother. 49:973-980.
60. Ramage, G., J. P. Martinez, and J. L. Lopez-Ribot. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6:979-986.
61. Ramage, G., K. Vande Walle, B. L. Wickes, and J. L. Lopez-Ribot. 2001. Biofilm formation by Candida dubliniensis. J. Clin. Microbiol. 39:3234-3240.
62. Ramage, G., K. Vande Walle, B. L. Wickes, and J. L. Lopez-Ribot. 2001. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob. Agents Chemother. 45:2475-2479.
63. Ramage, G., K. VandeWalle, S. P. Bachmann, B. L. Wickes, and J. L. Lopez-Ribot. 2002. In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob. Agents Chemother. 46:3634-3636.
64. Rex, J. H., T. J. Walsh, J. D. Sobel, S. G. Filler, P. G. Pappas, W. E. Dismukes, and J. E. Edwards. 2000. Practice guidelines for the treatment of candidiasis. Infectious Diseases Society of America. Clin. Infect. Dis. 30:662-678.
65. Rogers, P. D., and K. S. Barker. 2003. Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob. Agents Chemother. 47:1220-1227.
66. Romanini, D., G. Muller, and G. Pico. 2002. Use of amphotericin B as optical probe to study conformational changes and thermodynamic stability in human serum albumin. J. Protein Chem. 21:505-514.
67. Samaranayake, Y. H., J. Ye, J. Y. Yau, B. P. Cheung, and L. P. Samaranayake. 2005. In vitro method to study antifungal perfusion in Candida biofilms. J. Clin. Microbiol. 43:818-825.
68. Sanglard, D., and F. C. Odds. 2002. Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect. Dis. 2:73-85.
69. Shuford, J. A., M. S. Rouse, K. E. Piper, J. M. Steckelberg, and R. Patel. 2006. Evaluation of caspofungin and amphotericin B deoxycholate against Candida albicans biofilms in an experimental intravascular catheter infection model. J. Infect. Dis. 194:710-713.
70. Sinha, I., Y. M. Wang, R. Philp, C. R. Li, W. H. Yap, and Y. Wang. 2007. Cyclin-dependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev. Cell 13:421-432.
71. Sterling, T. R., and W. G. Merz. 1998. Resistance to amphotericin B: emerging clinical and microbiological patterns. Drug Resist. Updat. 1:161-165.
72. Stewart, P. S., and J. W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135-138.
73. Sudbery, P. 2007. Morphogenesis of a human fungal pathogen requires septin phosphorylation. Dev. Cell 13:315-316.
74. Viscoli, C., C. Girmenia, A. Marinus, L. Collette, P. Martino, B. Vandercam, C. Doyen, B. Lebeau, D. Spence, V. Krcmery, B. De Pauw, and F. Meunier. 1999. Candidemia in cancer patients: a prospective, multicenter surveillance study by the Invasive Fungal Infection Group (IFIG) of the European Organization for Research and Treatment of Cancer (EORTC). Clin. Infect. Dis. 28:1071-1079.
75. Wenzel, R. P. 1995. Nosocomial candidemia: risk factors and attributable mortality. Clin. Infect. Dis. 20:1531-1534.
76. Wisplinghoff, H., T. Bischoff, S. M. Tallent, H. Seifert, R. P. Wenzel, and M. B. Edmond. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39:309-317.
77. Zhao, X., K. J. Daniels, S. H. Oh, C. B. Green, K. M. Yeater, D. R. Soll, and L. L. Hoyer. 2006. Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152:2287-2299.