Azole drugs are imported by facilitated diffusion in Candida albicans and other pathogenic fungi

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Mansfield, Bryce E ^a   Oltean, Hanna N ^a   Oliver, Brian G ^a   Hoot, Samantha J ^a   Leyde, Sarah E ^a   Hedstrom, Lizbeth ^b   White, Theodore C ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; AZACONAZOLE; BENZNIDAZOLE; FLUCONAZOLE; FLUCYTOSINE; IMIDAZOLE; ITRACONAZOLE; KETOCONAZOLE; PACLOBUTRAZOL; POSACONAZOLE; PYRROLE DERIVATIVE; TIPIFARNIB; TRIAZOLE; UNCLASSIFIED DRUG; VORICONAZOLE;

ANTIBIOTIC RESISTANCE; ARTICLE; CANDIDA ALBICANS; CANDIDA KRUSEI; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; DIFFUSION; DRUG ACCUMULATION; DRUG MECHANISM; DRUG TRANSPORT; DRUG UPTAKE; FUNGAL CELL; FUNGAL STRAIN; FUNGUS; HALOGENATION; IN VITRO STUDY; NONHUMAN; PUMP; SACCHAROMYCES CEREVISIAE;

ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CANDIDIASIS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DIFFUSION; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; GENE DELETION; HUMANS; OXYGEN; SACCHAROMYCES CEREVISIAE;

CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; FUNGI; ISSATCHENKIA ORIENTALIS; SACCHAROMYCES CEREVISIAE;

EID: 78149321014     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001126     Document Type: Article

References (49)

1. Lai CC, Tan CK, Huang YT, Shao PL, Hsueh PR (2008) Current challenges in the management of invasive fungal infections. J Infect Chemother 14: 77-85.
2. Picazo JJ, Gonzalez-Romo F, Candel FJ (2008) Candidemia in the critically ill patient. Int J Antimicrob Agents 32(Suppl 2): S83-85.
3. Clark TA, Hajjeh RA (2002) Recent trends in the epidemiology of invasive mycoses. Curr Opin Infect Dis 15: 569-574.
4. Tortorano AM, Kibbler C, Peman J, Bernhardt H, Klingspor L, et al. (2006) Candidaemia in Europe: epidemiology and resistance. Int J Antimicrob Agents 27: 359-366.
5. Greenspan D, Greenspan J, Schiodt M, Pindborg J (1990) AIDS and the mouth. Copenhagen: Munksgaard. pp 91-102.
6. Morschhauser J (2002) The genetic basis of fluconazole resistance development in Candida albicans. Biochim Biophys Acta 1587: 240-248.
7. White TC, Marr KA, Bowden RA (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clinical Microbiology Reviews 11: 382-402.
8. Sanglard D, White TC (2005) Chapter 14 - Molecular Principles of Antifungal Drug Resistance. In: Heitman J, Filler SG, Edwards JE, Mitchell AP, eds. Molecular principles of fungal pathogenesis. Washington, D.C.: ASM Press. pp 197-212.
9. Albertson GD, Niimi M, Cannon RD, Jenkinson HF (1996) Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrobial Agents & Chemotherapy 40: 2835-2841.
10. Maesaki S, Marichal P, Vanden Bossche H, Sanglard D, Kohno S (1999) Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains. Journal of Antimicrobial Chemotherapy 44: 27-31.
11. Lamb DC, Kelly DE, Manning NJ, Kelly SL (1997) Reduced intracellular accumulation of azole antifungal results in resistance in Candida albicans isolate NCPF 3363. Fems Microbiology Letters 147: 189-193.
12. Sanglard D, Kuchler K, Ischer F, Pagani JL, Monod M, et al. (1995) Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrobial Agents and Chemotherapy 39: 2378-2386.
13. Prasad T, Chandra A, Mukhopadhyay CK, Prasad R (2006) Unexpected link between iron and drug resistance of Candida spp.: iron depletion enhances membrane fluidity and drug diffusion, leading to drug-susceptible cells. Antimicrob Agents Chemother 50: 3597-3606.
14. Mukhopadhyay K, Kohli A, Prasad R (2002) Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob Agents Chemother 46: 3695-3705.
15. Pasrija R, Krishnamurthy S, Prasad T, Ernst JF, Prasad R (2005) Squalene epoxidase encoded by ERG1 affects morphogenesis and drug susceptibilities of Candida albicans. Journal Of Antimicrobial Chemotherapy 55: 905-913.
16. Boiron P, Drouhet E, Dupont B, Improvisi L (1987) Entry of ketoconazole into Candida albicans. Antimicrob Agents Chemother 31: 244-248.
17. Lyons CN, White TC (2000) Transcriptional analyses of antifungal drug resistance in Candida albicans. Antimicrobial Agents and Chemotherapy 44: 2296-2303.
18. White TC (1997) 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. Antimicrobial Agents And Chemotherapy 41: 1482-1487.
19. Yamazaki T, Sanglard D, Sato Y, Arasaza M (1998) Fluconazole (FCZ) treatment for murine systemic candidiasis with Candida ablicans null mutants of nultidrug resistance genes. Intersci Conf Antimicrob Agents Chemother: ASM. pp 112 (abstract no. C-149).
20. Noel T, Francois F, Paumard P, Chastin C, Brethes D, et al. (2003) Flucytosine-fluconazole cross-resistance in purine-cytosine permease-deficient Candida lusitaniae clinical isolates: indirect evidence of a fluconazole uptake transporter. Antimicrob Agents Chemother 47: 1275-1284.
21. Bourot S, Karst F (1995) Isolation and characterization of the Saccharomyces cerevisiae SUT1 gene involved in sterol uptake. Gene 165: 97-102.
22. National Center for Biotechnology Information N, NIH (2010) PubChem Compound. 2010. http://pubchem.ncbi.nlm.nih.gov/.
23. Kraus JM, Verlinde CL, Karimi M, Lepesheva GI, Gelb MH, et al. (2009) Rational modification of a candidate cancer drug for use against Chagas disease. J Med Chem 52: 1639-1647.
24. Suryadevara PK, Olepu S, Lockman JW, Ohkanda J, Karimi M, et al. (2009) Structurally simple inhibitors of lanosterol 14alpha-demethylase are efficacious in a rodent model of acute Chagas disease. J Med Chem 52: 3703-3715.
25. Lamping E, Monk BC, Niimi K, Holmes AR, Tsao S, et al. (2007) Characterization of three classes of membrane proteins involved in fungal azole resistance by functional hyperexpression in Saccharomyces cerevisiae. Eukaryot Cell 6: 1150-1165.
26. Niimi M, Wada S, Tanabe K, Kaneko A, Takano Y, et al. (2005) Functional analysis of fungal drug efflux transporters by heterologous expression in Saccharomyces cerevisiae. Jpn J Infect Dis 58: 1-7.
27. Invitrogen (2010) Invitrogen Clones. 2010. http://clones.invitrogen.com/bacpacsearch.php.
28. Raiborg C, Stenmark H (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458: 445-452.
29. Nickerson DP, Russell MR, Odorizzi G (2007) A concentric circle model of multivesicular body cargo sorting. EMBO Rep 8: 644-650.
30. Tuch BB, Galgoczy DJ, Hernday AD, Li H, Johnson AD (2008) The evolution of combinatorial gene regulation in fungi. PLoS Biol 6: e38.
31. Rokas A, Hittinger CT (2007) Transcriptional rewiring: the proof is in the eating. Current Biology 17: R626-628.
32. Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Current Biology 17: 1007-1013.
33. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, et al. (2005) Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938-940.
34. White TC, Holleman S, Dy F, Mirels LF, Stevens DA (2002) Resistance mechanisms in clinical isolates of Candida albicans. Antimicrobial Agents and Chemotherapy 46: 1704-1713.
35. Jorgensen P, Edgington NP, Schneider BL, Rupes I, Tyers M, et al. (2007) The size of the nucleus increases as yeast cells grow. Mol Biol Cell 18: 3523-3532.
36. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, et al. (2007) Putative Role of {beta}-1,3 Glucans in Candida albicans Biofilm Resistance. Antimicrob Agents Chemother 51: 510-520.
37. Chapeland-Leclerc F, Bouchoux J, Goumar A, Chastin C, Villard J, et al. (2005) Inactivation of the FCY2 gene encoding purine-cytosine permease promotes cross-resistance to Flucytosine and Fluconazole in Candida lusitaniae. Antimicrobial Agents and Chemotherapy 49: 3101-3108.
38. Papon N, Noel T, Florent M, Gibot-Leclerc S, Jean D, et al. (2007) Molecular mechanism of flucytosine resistance in Candida lusitaniae: contribution of the FCY2, FCY1, and FUR1 genes to 5-fluorouracil and fluconazole crossresistance. Antimicrob Agents Chemother 51: 369-371.
39. Muller FM, Staudigel A, Salvenmoser S, Tredup A, Miltenberger R, et al. (2007) Cross-resistance to medical and agricultural azole drugs in yeasts from the oropharynx of human immunodeficiency virus patients and from environmental Bavarian vine grapes. Antimicrob Agents Chemother 51: 3014-3016.
40. Eshel D, Ben-Arie R, Dinoor A, Prusky D (2000) Resistance of Gibberellin-Treated Persimmon Fruit to Alternaria alternata Arises from the Reduced Ability of the Fungus to Produce Endo-1,4-beta-Glucanase. Phytopathology 90: 1256-1262.
41. Norman SM, Bennett RD, Poling SM, Maier VP, Nelson MD (1986) Paclobutrazol Inhibits Abscisic Acid Biosynthesis in Cercospora rosicola. Plant Physiology 80: 122-125.
42. Baya M, Soulounganga P, Gelhaye E, Gerardin P (2001) Fungicidal activity of beta-thujaplicin analogues. Pest Manag Sci 57: 833-838.
43. Rankin GO, Yang DJ, Cressey-Veneziano K, Wang RT, Brown PI (1985) In vivo and in vitro effects of azaconazole on renal function in the Fischer 344 rat. Toxicology 34: 1-11.
44. Fonzi WA, Irwin MY (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
45. White TC, Pfaller MA, Rinaldi RG, Smith J, Redding SW (1997) Stable azole drug resistance associated with a substrain of Candida albicans from an HIV-infected patient. Oral Diseases 3: S102-S109.
46. Hua J, Meyer JD, Lodge JK (2000) Development of positive selectable markers for the fungal pathogen Cryptococcus neoformans. Clin Diagn Lab Immunol 7: 125-128.
47. Oliver BG, Silver PM, Marie C, Hoot SJ, Leyde SE, et al. (2008) Tetracycline alters drug susceptibility in Candida albicans and other pathogenic fungi. Microbiology 154: 960-970.
48. Marie C, Leyde S, White TC (2008) Cytoplasmic localization of sterol transcription factors Upc2p and Ecm22p in S. cerevisiae. Fungal Genet Biol 45: 1430-1438.
49. Song JL, Harry JB, Eastman RT, Oliver BG, White TC (2004) The Candida albicans lanosterol 14-alpha-demethylase (ERG11) gene promoter is maximally induced after prolonged growth with antifungal drugs. Antimicrob Agents Chemother 48: 1136-1144.