Farnesol-induced apoptosis in Candida albicans is mediated by CDR1-p extrusion and depletion of intracellular glutathione

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Zhu, Jingsong ^a   Krom, Bastiaan P ^b   Sanglard, Dominique ^c   Intapa, Chaidan ^a,d   Dawson, Clinton C ^a   Peters, Brian M ^e,f   Shirtliff, Mark E ^e,f   Jabra Rizk, Mary Ann ^a,e  

^a UNIVERSITY OF MARYLAND   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d NARESUAN UNIVERSITY   (Thailand)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDR1P PROTEIN; FARNESOL; FUNGAL PROTEIN; GLUTATHIONE; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; CARRIER PROTEIN; CASPASE; CDR1 PROTEIN, CANDIDA ALBICANS; GLUTATHIONE DISULFIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; CANDIDA ALBICANS; CDR1 GENE; CELL DEATH; CELL LEVEL; CELL VIABILITY; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; FUNGAL GENE; FUNGAL STRAIN; GENE OVEREXPRESSION; NONHUMAN; OXIDATIVE STRESS; SOD GENE; UPREGULATION; VALIDATION STUDY; CELL SURVIVAL; CYTOLOGY; DRUG EFFECT; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; INTRACELLULAR SPACE; METABOLISM; OXIDATION REDUCTION REACTION; REPRODUCIBILITY;

ANTIFUNGAL AGENTS; APOPTOSIS; CANDIDA ALBICANS; CASPASES; CELL SURVIVAL; ENZYME ACTIVATION; FARNESOL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLUTATHIONE; GLUTATHIONE DISULFIDE; HOMEOSTASIS; INTRACELLULAR SPACE; MEMBRANE TRANSPORT PROTEINS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; REPRODUCIBILITY OF RESULTS; SUPEROXIDE DISMUTASE;

EID: 83655181842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028830     Document Type: Article

References (45)

1. Fidel PL Jr, (2006) Candida-host interactions in HIV disease: relationships in oropharyngeal candidiasis. Adv Dent Res 6 (19): 80-84.
2. Perlroth J, Choi B, Spellberg B, (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45 (4): 321-346.
3. 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 (5): 1053-1060.
4. Chandra J, Kuhn DM, Mulherjee PK, Hoyer LL, McCormick T, et al. (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183 (18): 5385-5394.
5. Jayatilake JAMS, Samaranayake YH, Samaranayake LP, (2005) An ultrastructural and a cytochemical study of candidal invasion of reconstituted human oral epithelium. J Oral Path Med 34: 240-246.
6. Ramage G, Saville SP, Wickes BL, Lopez-Ribot JL, (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. App Environ Microbiol 68 (11): 5459-5463.
7. Enjalbert B, Whiteway M, (2005) Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4 (7): 1203-1210.
8. Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, et al. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. App Environ Microbiol 67 (7): 2982-2992.
9. Oh K-B, 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 (8): 4664-4668.
10. Scheper MA, Shirtliff ME, Meiller TF, Jabra-Rizk MA, (2008) Farnesol a fungal quorum sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia 10 (9): 954-963.
11. Shirtliff ME, Krom BP, Meijering RA, Peters BM, Zhu J, et al. (2009) Farnesol-induced apoptosis in Candida albicans. Antimicrob Agents Chemother 53 (6): 2392-401.
12. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, et al. (1998) A caspase-activated Dnase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391: 43-50.
13. Hengartner MO, (2001) Apoptosis: DNA destroyers. Nature 412 (6842): 27, 29.
14. Herrero E, Ros J, Bellí G Cabiscol E, (2008) Redox control and oxidative stress in yeast cells. Biochimica et Biophysica Acta (BBA) 1780 (11): 1217-1235.
15. Trompier D, Chang X-B, Barattin R, Moulinet d'Hardemare A, Di Pietro A, et al. (2004) Verapamil and Its Derivative Trigger Apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res 64 (14): 4950-4956.
16. Dickinson DA, Forman HJ, (2002) Glutathione in Defense and Signaling. Ann NY Acad Sci 973: 488-504.
17. Pastore A, Federici G, Bertini E, Piemonte F, (2003) Analysis of glutathione: implication in redox and detoxification. Clinica Chimica Acta 333: 19-39.
18. Penninckx MJ, (2002) An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res 2 (3): 295-305.
19. Baek YU, Kim YR, Yim H-S, Kang SO, (2004) Disruption of [gamma]-glutamylcysteine synthetase results in absolute glutathione auxotrophy and apoptosis in Candida albicans. FEBS Lett 556 (1-3): 47-52.
20. Grant CM, Collinson LP, Roe JH, Dawes IW, (1996) Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol Microbiol 21 (1): 171-179.
21. Kruh GD, Belinsky MG, (2003) The MRP family of drug efflux pumps. Oncogene 22: 7537-7552.
22. Toyoda Y, Hagiya Y, Adachi T, Hoshijima K, Kuo MT, et al. (2008) MRP class of human ATP binding cassette (ABC) transporters: historical background. Xenobiotica 38 (7): 833-862.
23. Rappa G, Lorico A, Flavell RA, Sartorelli AC, (1997) Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 57 (23): 5232-5237.
24. Lorico A, Rappa G, Finch RA, Yang D, Flavell RA, et al. (1997) Disruption of the murine MRP (Multidrug Resistance Protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res 57 (23): 5238-5242.
25. Cannon RD, Holmes AR, Niimi K, Keniya MV, Tanabe K, et al. (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22 (2): 291-321.
26. White TC, Marr KA, Bowden RA, (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11 (2): 382-402.
27. Gauthier C, Weber S, Alarco AM, Alqawi O, Daoud R, et al. (2003) Functional Similarities and Differences between Candida albicans Cdr1p and Cdr2p Transporters. Antimicrob Agents Chemother 47 (5): 1543-1554.
28. Sanglard D, Ischer F, Monod M, Bille J, (1996) Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob Agents Chemother 40: 2300-2305.
29. Sanglard D, Ischer F, Monod M, Bille J, (1997) Cloning of Candida albicans genes conferring resistance to antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiol 143: 405-416.
30. Niimi M, Niimi K, Takano Y, Holmes AR, Fischer FK, (2004) Regulated overexpression of CDR1 in Candida albicans confers multidrug resistance. J Antimicrob Chemother 54: 999-1006.
31. Murad AM, Broadbent ID, Barelle CJ, Brown AJ, (2000) CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325-327.
32. Coste A, Selmecki A, Forche A, Diogo D, Bougnoux ME, D'enfert C, et al. (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6: 1889-1904.
33. Standards, N.C.F.C.L. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. 2nd ed. Vol. Document M27-A2. 2002 Wayne, PA National Committee for Clinical Laboratory Standards.
34. Gonzalez-Parragaa P, Marri FR, Arguelles J, Jose J, Hernandez J, (2005) Correlation between the intracellular content of glutathione and the formation of germ-tubes induced by human serum in Candida albicans. Biochimica et Biophysica Acta 1722: 324-330.
35. Westwater C, Balish E, Schofield DA, (2005) Candida albicans-conditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot Cell 4 (10): 1654-1661.
36. Sharma M, Prasad R, (2011) The quorum sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans. Antimicrob Agents Chemother (online).
37. Krishnamurthy S, G.V., Snehlata P, Prasad R, (1998) Characterization of the human steroid hormone transporter mediated by Cdr1p, a multidrug transporter of Candida albicans, belonging to the ATP binding cassette super family. Biochem J 158 (1): 69-74.
38. White TC, Holleman S, Dy F, Mirels LF, Stevens DA, (2002) Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob Agents Chemother 46 (6): 1704-1713.
39. Cannon R, Lamping E, Holmes A, Niimi K, Baret PV, et al. (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22 (2): 291-321.
40. Costa V, Moradas-Ferreira P, (2001) Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol Aspects Med 22: 217-246.
41. Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145 (4): 757-767.
42. Chauhan N, Latge JP, Calderone R, (2006) Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat Rev Micro 4 (6): 435-444.
43. Martchenko M, Alarco AM, Harcus D, Whiteway M, (2004) Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15 (2): 456-467.
44. Lamarre C, LeMay JD, Deslauriers N, Bourbonnais Y, (2001) Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J Biol Chem 276 (47): 43784-43791.
45. Jabra-Rizk MA, Meiller TF, James CE, Shirtliff ME, (2006) Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial resistance. Antimicrob Agents Chemother 50 (4): 1463-14.