Small-molecule suppressors of Candida albicans biofilm formation synergistically enhance the antifungal activity of amphotericin b against clinical Candida isolates

ACS Chemical Biology

Volumn 8, Issue 4, 2013, Pages 840-848

  You, Jianlan ^a   Du, Lin ^a   King, Jarrod B ^a   Hall, Brian E ^b   Cichewicz, Robert H ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b EMD Millipore   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; ANTIFUNGAL AGENT; SHEARININE D; SHEARININE E; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ARTICLE; BIOFILM; CANDIDA; CANDIDA ALBICANS; CANDIDA GLABRATA; CANDIDA KRUSEI; CANDIDA PARAPSILOSIS; CANDIDA TROPICALIS; CELL ASSAY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG POTENTIATION; FLOW CYTOMETRY; FUNGUS HYPHAE; KLUYVEROMYCES MARXIANUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; BIOFILMS; CANDIDA ALBICANS; DRUG SYNERGISM; INDOLE ALKALOIDS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, CONFOCAL; SMALL MOLECULE LIBRARIES;

CANDIDA; CANDIDA ALBICANS; PENICILLIUM SP.; SACCHAROMYCETALES;

EID: 84876550853     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400009f     Document Type: Article

References (48)

1. Lass-Flörl, C. (2009) The changing face of epidemiology of invasive fungal disease in Europe Mycoses 52, 197-205
2. Ruan, S. Y. and Hsueh, P. R. (2009) Invasive candidiasis: an overview from Taiwan J. Formosan Med. Assoc. 108, 443-451
3. Playford, E. G., Nimmo, G. R., Tilse, M., and Sorrell, T. C. (2010) Increasing incidence of candidaemia: long-term epidemiological trends, Queensland, Australia, 1999-2008 J. Hosp. Infect. 76, 46-51
4. Falagas, M. E., Roussos, N., and Vardakas, K. Z. (2010) Relative frequency of albicans and the various non-Albicans Candida spp. among candidemia isolates from inpatients in various parts of the world: a systematic review Int. J. Infect. Dis. 14, e954-e966
5. Hobson, R. P. (2003) The global epidemiology of invasive Candida infections-is the tide turning? J. Hosp. Infect. 55, 159-168
6. Pfaller, M. A. and Diekema, D. J. (2007) Epidemiology of invasive candidiasis: a persistent public health problem Clin. Microbiol. Rev. 20, 133-163
7. Tumbarello, M., Fiori, B., Trecarichi, E. M., Posteraro, P., Losito, A. R., De Luca, A., Sanguinetti, M., Fadda, G., Cauda, R., and Posteraro, B. (2012) Risk factors and outcomes of candidemia caused by biofilm-forming isolates in a tertiary care hospital PLoS ONE 7, e33705
8. Tumbarello, M., Posteraro, B., Trecarichi, E. M., Fiori, B., Rossi, M., Porta, R., de Gaetano Donati, K., La Sorda, M., Spanu, T., Fadda, G., Cauda, R., and Sanguinetti, M. (2007) Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia J. Clin. Microbiol 45, 1843-1850
9. Harriott, M. M. and Noverr, M. C. (2011) Importance of Candida -bacterial polymicrobial biofilms in disease Trends Microbiol. 19, 557-563
10. Harriott, M. M., Lilly, E. A., Rodriguez, T. E., Fidel, P. L., and Noverr, M. C. (2010) Candida albicans forms biofilms on the vaginal mucosa Microbiology 156, 3635-3644
11. Ganguly, S. and Mitchell, A. P. (2011) Mucosal biofilms of Candida albicans Curr. Opin. Microbiol. 14, 380-385
12. Douglas, L. J. (2003) Candida biofilms and their role in infection Trends Microbiol. 11, 30-36
13. Nett, J. E., Sanchez, H., Cain, M. T., and Andes, D. R. (2010) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan J. Infect. Dis. 202, 171-175
14. Nett, J. E., Sanchez, H., Cain, M. T., Ross, K. M., and Andes, D. R. (2011) Interface of Candida albicans biofilm matrix-Associated drug resistance and cell wall integrity regulation Eukaryotic Cell 10, 1660-1669
15. Lewis, K. (2010) Persister cells Annu. Rev. Microbiol. 64, 357-372
16. Dawson, C. C., Intapa, C., and Jabra-Rizk, M. A. (2011) Persisters": survival at the cellular level PLoS Pathog. 7, e1002121
17. LaFleur, M. D., Qi, Q., and Lewis, K. (2010) Patients with long-term oral carriage harbor high-persister mutants of Candida albicans Antimicrob. Agents Chemother. 54, 39-44
18. LaFleur, M. D., Kumamoto, C. A., and Lewis, K. (2006) Candida albicans biofilms produce antifungal-tolerant persister cells Antimicrob. Agents Chemother. 50, 3839-3846
19. Ramage, G., Martínez, J. P., and López-Ribot, J. L. (2006) Candida biofilms on implanted biomaterials: a clinically significant problem FEMS Yeast Res. 6, 979-986
20. Hasan, F., Xess, I., Wang, X., Jain, N., and Fries, B. C. (2009) Biofilm formation in clinical Candida isolates and its association with virulence Microbes Infect. 11, 753-761
21. Kojic, E. M. and Darouiche, R. O. (2004) Candida infections of medical devices Clin. Microbiol. Rev. 17, 255-267
22. Chandra, J., Mukherjee, P., and Ghannoum, M. (2010) Fungal biofilms in the clinical lab setting Curr. Fungal Infect. Rep. 4, 137-144
23. Toenjes, K. A., Stark, B. C., and Brooks, K. M. (2009) Johnson, D. I.: Inhibitors of cellular signalling are cytotoxic or block the budded-to-hyphal transition in the pathogenic yeast Candida albicans J. Med. Microbiol. 58, 779-790
24. Midkiff, J., Borochoff-Porte, N., White, D., and Johnson, D. I. (2011) Small molecule inhibitors of the Candida albicans budded-to-hyphal transition act through multiple signaling pathways PLoS One 6, e25395
25. Grald, A., Yargosz, P., Case, S., Shea, K., and Johnson, D. I. (2012) Small-molecule inhibitors of biofilm formation in laboratory and clinical isolates of Candida albicans J. Med. Microbiol. 61, 109-114
26. Shareck, J. and Belhumeur, P. (2011) Modulation of morphogenesis in Candida albicans by various small molecules Eukaryotic Cell 10, 1004-1012
27. Newman, D. J. and Cragg, G. M. (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010 J. Nat. Prod. 75, 311-335
28. Newman, D. J. and Cragg, G. M. (2007) Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 70, 461-477
29. Wang, X., You, J., King, J. B., Powell, D. R., and Cichewicz, R. H. (2012) Waikialoid A suppresses hyphal morphogenesis and inhibits biofilm development in pathogenic Candida albicans J. Nat. Prod. 75, 707-715
30. Wang, X., Du, L., You, J., King, J. B., and Cichewicz, R. H. (2012) Fungal biofilm inhibitors from a human oral microbiome-derived bacterium Org. Biomol. Chem. 10, 2044-2050
31. Gerea, A. L., Branscum, K. M., King, J. B., You, J., Powell, D. R., Miller, A. N., Spear, J. R., and Cichewicz, R. H. (2012) Secondary metabolites produced by fungi derived from a microbial mat encountered in an iron-rich natural spring Tetrahedron Lett. 53, 4202-4205
32. Nett, J. E., Cain, M. T., Crawford, K., and Andes, D. R. (2011) Optimizing a Candida biofilm microtiter plate model for measurement of antifungal susceptibility by tetrazolium salt assay J. Clin. Microbiol. 49, 1426-1433
33. Ramage, G., Saville, S. P., Wickes, B. L., and Lopez-Ribot, J. L. (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule Appl. Environ. Microbiol. 68, 5459-5463
34. Finkel, J. S. and Mitchell, A. P. (2011) Genetic control of Candida albicans biofilm development Nat. Rev. Microbiol. 9, 109-118
35. Uppuluri, P., Chaturvedi, A. K., Srinivasan, A., Banerjee, M., Ramasubramaniam, A. K., Kohler, J. R., Kadosh, D., and Lopez-Ribot, J. L. (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle PLoS Pathog. 6, e1000828
36. Sardi, J. C., Scorzoni, L., Bernardi, T., Fusco-Almeida, A. M., and Mendes Giannini, M. J. (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options J. Med. Microbiol. 62, 10-24
37. Chandra, J., Mukherjee, P. K., and Ghannoum, M. A. (2008) In vitro growth and analysis of Candida biofilms Nat. Protoc. 3, 1909-1924
38. Decanis, N., Tazi, N., Correia, A., Vilanova, M., and Rouabhia, M. (2011) Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by downregulating the expression of different secreted aspartyl proteinase genes Open Microbiol. J. 5, 119-126
39. Barelle, C. J., Bohula, E. A., Kron, S. J., Wessels, D., Soll, D. R., Schafer, A., Brown, A. J., and Gow, N. A. (2003) Asynchronous cell cycle and asymmetric vacuolar inheritance in true hyphae of Candida albicans Eukaryotic Cell 2, 398-410
40. Calvert, M. E. K., Lannigan, J. A., and Pemberton, L. F. (2008) Optimization of yeast cell cycle analysis and morphological characterization by multispectral imaging flow cytometry Cytometry, Part A 73, 825-833
41. Ramage, G., VandeWalle, K., Bachmann, S. P., Wickes, B. L., and Lopez-Ribot, J. L. (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
42. Mukherjee, P. K. and Chandra, J. (2004) Candida biofilm resistance Drug Resist. Update 7, 301-309
43. Vitale, R. G., Afeltra, J., and Dannaoui, E. (2005) Antifungal combinations Methods Mol. Med. 118, 143-152
44. Laniado-Laborin, R. and Cabrales-Vargas, M. N. (2009) Amphotericin B: side effects and toxicity Rev. Iberoam. Micol. 26, 223-227
45. Breger, J., Fuchs, B. B., Aperis, G., Moy, T. I., Ausubel, F. M., and Mylonakis, E. (2007) Antifungal chemical compounds identified using a C. elegans pathogenicity assay PLoS Pathog. 3, 168-178
46. Al-Fattani, M. A. and Douglas, L. J. (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance J. Med. Microbiol. 55, 999-1008
47. Calvert, M. E., Lannigan, J. A., and Pemberton, L. F. (2008) Optimization of yeast cell cycle analysis and morphological characterization by multispectral imaging flow cytometry Cytometry, Part A 73, 825-833
48. Ocampo, A. and Barrientos, A. (2011) Quick and reliable assessment of chronological life span in yeast cell populations by flow cytometry Mech. Ageing Dev. 132, 315-323