Comparison of sterol import under aerobic and anaerobic conditions in three fungal species, Candida albicans, Candida glabrata, and Saccharomyces cerevisiae

Eukaryotic Cell

Volumn 12, Issue 5, 2013, Pages 725-738

  Zavrel, Martin ^a   Hoot, Sam J ^b   White, Theodore C ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; CHOLESTEROL; ERGOSTEROL; FLUCONAZOLE;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; CANDIDA ALBICANS; CANDIDA GLABRATA; COMPARATIVE STUDY; CULTURE MEDIUM; DRUG EFFECT; ESTERIFICATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; SACCHAROMYCES CEREVISIAE;

AEROBIOSIS; ANAEROBIOSIS; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CANDIDA GLABRATA; CHOLESTEROL; CULTURE MEDIA; ERGOSTEROL; ESTERIFICATION; FLUCONAZOLE; GENE KNOCKOUT TECHNIQUES; MICROBIAL SENSITIVITY TESTS; SACCHAROMYCES CEREVISIAE;

BOVINAE; CANDIDA ALBICANS; CANDIDA GLABRATA; EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 84876866643     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00345-12     Document Type: Article

References (53)

1. Fidel PL, Jr, Vazquez JA, Sobel JD. 1999. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin. Microbiol. Rev. 12:80-96.
2. Jacquier N, Schneiter R. 2012. Mechanisms of sterol uptake and transport in yeast. J. Steroid Biochem. Mol. Biol. 129:70-78.
3. Raychaudhuri S, Prinz WA. 2006. Uptake and trafficking of exogenous sterols in Saccharomyces cerevisiae. Biochem. Soc. Trans. 34:359-362.
4. Schneiter R. 2007. Intracellular sterol transport in eukaryotes, a connection to mitochondrial function? Biochimie 89:255-259.
5. Schneiter R, Brugger B, Sandhoff R, Zellnig G, Leber A, Lampl M, Athenstaedt K, Hrastnik C, Eder S, Daum G, Paltauf F, Wieland FT, Kohlwein SD. 1999. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell Biol. 146:741-754.
6. Dahl C, Biemann HP, Dahl J. 1987. A protein kinase antigenically related to pp60v-src possibly involved in yeast cell cycle control: positive in vivo regulation by sterol. Proc. Natl. Acad. Sci. U. S. A. 84:4012-4016.
7. Rodriguez RJ, Parks LW. 1983. Structural and physiological features of sterols necessary to satisfy bulk membrane and sparking requirements in yeast sterol auxotrophs. Arch. Biochem. Biophys. 225:861-871.
8. Zhang L, Hach A. 1999. Molecular mechanism of heme signaling in yeast: the transcriptional activator HapI serves as the key mediator. Cell. Mol. Life Sci. 56:415-426.
9. Andreasen AA, Stier TJ. 1953. Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J. Cell Physiol. 41:23-36.
10. Andreasen AA, Stier TJ. 1954. Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J. Cell Physiol. 43:271-281.
11. Lewis TA, Taylor FR, Parks LW. 1985. Involvement of heme biosynthesis in control of sterol uptake by Saccharomyces cerevisiae. J. Bacteriol. 163: 199-207.
12. Lorenz RT, Parks LW. 1987. Regulation of ergosterol biosynthesis and sterol uptake in a sterol-auxotrophic yeast. J. Bacteriol. 169:3707-3711.
13. Lorenz RT, Parks LW. 1990. Effects of lovastatin (mevinolin) on sterol levels and on activity of azoles in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 34:1660-1665.
14. Lorenz RT, Parks LW. 1991. Physiological effects of fenpropimorph on wild-type Saccharomyces cerevisiae and fenpropimorph-resistant mutants. Antimicrob. Agents Chemother. 35:1532-1537.
15. Lorenz RT, Rodriguez RJ, Lewis TA, Parks LW. 1986. Characteristics of sterol uptake in Saccharomyces cerevisiae. J. Bacteriol. 167:981-985.
16. Kohut P, Wustner D, Hronska L, Kuchler K, Hapala I, Valachovic M. 2010. The role of ABC proteins Aus1p and Pdr11p in the uptake of external sterols in yeast: dehydroergosterol fluorescence study. Biochem. Biophys. Res. Commun. 404:233-238.
17. Wilcox LJ, Balderes DA, Wharton B, Tinkelenberg AH, Rao G, Sturley SL. 2002. Transcriptional profiling identifies two members of the ATPbinding cassette transporter superfamily required for sterol uptake in yeast. J. Biol. Chem. 277:32466-32472.
18. Li Y, Prinz WA. 2004. ATP-binding cassette (ABC) transporters mediate nonvesicular, raft-modulated sterol movement from the plasma membrane to the endoplasmic reticulum. J. Biol. Chem. 279:45226-45234.
19. Kwast KE, Lai LC, Menda N, James DT, III, Aref S, Burke PV. 2002. Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae: functional roles of Rox1 and other factors in mediating the anoxic response. J. Bacteriol. 184:250-265.
20. Crowley JH, Leak FW, Jr, Shianna KV, Tove S, Parks LW. 1998. A mutation in a purported regulatory gene affects control of sterol uptake in Saccharomyces cerevisiae. J. Bacteriol. 180:4177-4183.
21. Lewis TL, Keesler GA, Fenner GP, Parks LW. 1988. Pleiotropic mutations in Saccharomyces cerevisiae affecting sterol uptake and metabolism. Yeast 4:93-106.
22. Bottema CD, Rodriguez RJ, Parks LW. 1985. Influence of sterol structure on yeast plasma membrane properties. Biochim. Biophys. Acta 813:313-320.
23. Reiner S, Micolod D, Zellnig G, Schneiter R. 2006. A genomewide screen reveals a role of mitochondria in anaerobic uptake of sterols in yeast. Mol. Biol. Cell 17:90-103.
24. Alimardani P, Regnacq M, Moreau-Vauzelle C, Ferreira T, Rossignol T, Blondin B, Berges T. 2004. SUT1-promoted sterol uptake involves the ABC transporter Aus1 and the mannoprotein Dan1 whose synergistic action is sufficient for this process. Biochem. J. 381:195-202.
25. Zweytick D, Leitner E, Kohlwein SD, Yu C, Rothblatt J, Daum G. 2000. Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 267:1075-1082.
26. Valachovic M, Hronska L, Hapala I. 2001. Anaerobiosis induces complex changes in sterol esterification pattern in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Lett. 197:41-45.
27. Bard M, Sturm AM, Pierson CA, Brown S, Rogers KM, Nabinger S, Eckstein J, Barbuch R, Lees ND, Howell SA, Hazen KC. 2005. Sterol uptake in Candida glabrata: rescue of sterol auxotrophic strains. Diagn. Microbiol. Infect. Dis. 52:285-293.
28. Nakayama H, Tanabe K, Bard M, Hodgson W, Wu S, Takemori D, Aoyama T, Kumaraswami NS, Metzler L, Takano Y, Chibana H, Niimi M. 2007. The Candida glabrata putative sterol transporter gene CgAUS1 protects cells against azoles in the presence of serum. J. Antimicrob. Chemother. 60:1264-1272.
29. Nakayama H, Izuta M, Nakayama N, Arisawa M, Aoki Y. 2000. Depletion of the squalene synthase (ERG9) gene does not impair growth of Candida glabrata in mice. Antimicrob. Agents Chemother. 44:2411-2418.
30. Nakayama H, Nakayama N, Arisawa M, Aoki Y. 2001. In vitro and in vivo effects of 14α-demethylase (ERG11) depletion in Candida glabrata. Antimicrob. Agents Chemother. 45:3037-3045.
31. Kurtz MB, Marrinan J. 1989. Isolation of hem3 mutants from Candida albicans by sequential gene disruption. Mol. Gen. Genet. 217:47-52.
32. Tsai HF, Bard M, Izumikawa K, Krol AA, Sturm AM, Culbertson NT, Pierson CA, Bennett JE. 2004. Candida glabrata erg1 mutant with increased sensitivity to azoles and to low oxygen tension. Antimicrob. Agents Chemother. 48:2483-2489.
33. Dumitru R, Hornby JM, Nickerson KW. 2004. Defined anaerobic growth medium for studying Candida albicans basic biology and resistance to eight antifungal drugs. Antimicrob. Agents Chemother. 48:2350-2354.
34. Bard M, Lees ND, Barbuch RJ, Sanglard D. 1987. Characterization of a cytochrome P450 deficient mutant of Candida albicans. Biochem. Biophys. Res. Commun. 147:794-800.
35. Mas J, Pina E. 1980. Disappearance of nystatin resistance in Candida mediated by ergosterol. J. Gen. Microbiol. 117:249-252.
36. Nagi M, Nakayama H, Tanabe K, Bard M, Aoyama T, Okano M, Higashi S, Ueno K, Chibana H, Niimi M, Yamagoe S, Umeyama T, Kajiwara S, Ohno H, Miyazaki Y. 2011. Transcription factors CgUPC2A and CgUPC2B regulate ergosterol biosynthetic genes in Candida glabrata. Genes Cells 16:80-89.
37. Reuss O, Vik A, Kolter R, Morschhauser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119-127.
38. Gietz RD, Woods RA. 2006. Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol. Biol. 313:107-120.
39. Schneiter R, Daum G. 2006. Analysis of yeast lipids. Methods Mol. Biol. 313:75-84.
40. Davies BS, Wang HS, Rine J. 2005. Dual activators of the sterol biosynthetic pathway of Saccharomyces cerevisiae: similar activation/regulatory domains but different response mechanisms. Mol. Cell. Biol. 25:7375-7385.
41. Shianna KV, Dotson WD, Tove S, Parks LW. 2001. Identification of a UPC2 homolog in Saccharomyces cerevisiae and its involvement in aerobic sterol uptake. J. Bacteriol. 183:830-834.
42. MacPherson S, Akache B, Weber S, De Deken X, Raymond M, Turcotte B. 2005. Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes. Antimicrob. Agents Chemother. 49:1745-1752.
43. Silver PM, Oliver BG, White TC. 2004. Role of Candida albicans transcription factor Upc2p in drug resistance and sterol metabolism. Eukaryot. Cell 3:1391-1397.
44. Vik A, Rine J. 2001. Upc2p and Ecm22p, dual regulators of sterol biosynthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:6395-6405.
45. Mansfield BE, Oltean HN, Oliver BG, Hoot SJ, Leyde SE, Hedstrom L, White TC. 2010. Azole drugs are imported by facilitated diffusion in Candida albicans and other pathogenic fungi. PLoS Pathog. 6:e1001126. doi:10.1371/journal.ppat.1001126.
46. Davies BS, Rine J. 2006. A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 174:191-201.
47. Gaisne M, Becam AM, Verdiere J, Herbert CJ. 1999. A 'natural' mutation in Saccharomyces cerevisiae strains derived from S288c affects the complex regulatory gene HAP1 (CYP1). Curr. Genet. 36:195-200.
48. Abramova NE, Cohen BD, Sertil O, Kapoor R, Davies KJ, Lowry CV. 2001. Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodeling of the cell wall in Saccharomyces cerevisiae. Genetics 157:1169-1177.
49. Hoot SJ, Smith AR, Brown RP, White TC. 2011. An A643V amino acid substitution in Upc2p contributes to azole resistance in well-characterized clinical isolates of Candida albicans. Antimicrob. Agents Chemother. 55: 940-942.
50. Gollub EG, Liu KP, Dayan J, Adlersberg M, Sprinson DB. 1977. Yeast mutants deficient in heme biosynthesis and a heme mutant additionally blocked in cyclization of 2,3-oxidosqualene. J. Biol. Chem. 252:2846-2854.
51. Wilson RB, Davis D, Mitchell AP. 1999. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181:1868-1874.
52. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
53. Ueno K, Uno J, Nakayama H, Sasamoto K, Mikami Y, Chibana H. 2007. Development of a highly efficient gene targeting system induced by transient repression of YKU80 expression in Candida glabrata. Eukaryot. Cell 6:1239-1247.