The regulatory inputs controlling pleiotropic drug resistance and hypoxic response in yeast converge at the promoter of the aminocholesterol resistance gene RTA1

FEMS Yeast Research

Volumn 12, Issue 3, 2012, Pages 279-292

  Kolaczkowska, Anna ^a   Manente, Myriam ^b   Kolaczkowski, Marcin ^c   Laba, Justyna ^a,e   Ghislain, Michel ^b   Wawrzycka, Donata ^d  

^a WROC AW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c WROCLAW MEDICAL UNIVERSITY   (Poland)

^d UNIVERSITY OF WROC AW   (Poland)

^e UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

7 aminocholesterol; Antifungal resistance; Phytosphingosine; Stress response; Transcriptional repressor; Yeast

Indexed keywords

AMINOCHOLESTEROL; PHYTOSPHINGOSINE; SPHINGOLIPID; STEROL; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ARTICLE; CELL FRACTIONATION; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FUNGAL GENE; FUNGAL STRAIN; GENE; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENE MAPPING; HYPOXIA; LACZ GENE; MOT3P GENE; NONHUMAN; PLEIOTROPY; RTA1P GENE; TUP1 GENE;

ANTIFUNGAL AGENTS; CHOLESTEROL; DRUG RESISTANCE, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK RESPONSE; MEMBRANE PROTEINS; OXYGEN; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOLIPIDS; STEROLS; TRANSCRIPTION FACTORS;

EID: 84859620677     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2011.00768.x     Document Type: Article

References (69)

1. 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.
2. Balasubramanian B, Lowry CV & Zitomer RS (1993) The Rox1 repressor of the Saccharomyces cerevisiae hypoxic genes is a specific DNA-binding protein with a high-mobility-group motif. Mol Cell Biol 13: 6071-6078.
3. Balzi E, Wang M, Leterme S, Van Dyck L & Goffeau A (1994) PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J Biol Chem 269: 2206-2214.
4. Bauer BE, Wolfger H & Kuchler K (1999) Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim Biophys Acta 1461: 217-236.
5. Berge KE, Tian H, Graf GA, Yu L, Grishin NV, Schultz J, Kwiterovich P, Shan B, Barnes R & Hobbs HH (2000) Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 290: 1771-1775.
6. Bodzioch M, Orso E, Klucken J et al. (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22: 347-351.
7. 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.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
9. Brooks-Wilson A, Marcil M, Clee SM et al. (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22: 336-345.
10. Capieaux E, Rapin C, Thines D, Dupont Y & Goffeau A (1993) Overexpression in Escherichia coli and purification of an ATP-binding peptide from the yeast plasma membrane H(+)-ATPase. J Biol Chem 268: 21895-21900.
11. Chen DC, Yang BC & Kuo TT (1992) One-step transformation of yeast in stationary phase. Curr Genet 21: 83-84.
12. Christianson TW, Sikorski RS, Dante M, Shero JH & Hieter P (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
13. Chung N, Jenkins G, Hannun YA, Heitman J & Obeid LM (2000) Sphingolipids signal heat stress-induced ubiquitin-dependent proteolysis. J Biol Chem 275: 17229-17232.
14. Cohen BD, Sertil O, Abramova NE, Davies KJ & Lowry CV (2001) Induction and repression of DAN1 and the family of anaerobic mannoprotein genes in Saccharomyces cerevisiae occurs through a complex array of regulatory sites. Nucleic Acids Res 29: 799-808.
15. Dardalhon M, Lin W, Nicolas A & Averbeck D (2007) Specific transcriptional responses induced by 8-methoxypsoralen and UVA in yeast. FEMS Yeast Res 7: 866-878.
16. Davies BS & Rine J (2006) A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 174: 191-201.
17. Decottignies A, Grant AM, Nichols JW, de Wet H, McIntosh DB & Goffeau A (1998) ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J Biol Chem 273: 12612-12622.
18. Decottignies A, Evain A & Ghislain M (2004) Binding of Cdc48p to a ubiquitin-related UBX domain from novel yeast proteins involved in intracellular proteolysis and sporulation. Yeast 21: 127-139.
19. Delahodde A, Delaveau T & Jacq C (1995) Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol Cell Biol 15: 4043-4051.
20. Delaveau T, Delahodde A, Carvajal E, Subik J & Jacq C (1994) PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol Gen Genet 244: 501-511.
21. DeRisi J, van den Hazel B, Marc P, Balzi E, Brown P, Jacq C & Goffeau A (2000) Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. FEBS Lett 470: 156-160.
22. Devaux F, Marc P, Bouchoux C, Delaveau T, Hikkel I, Potier MC & Jacq C (2001) An artificial transcription activator mimics the genome-wide properties of the yeast Pdr1 transcription factor. EMBO Rep 2: 493-498.
23. Dherbomez M, el kihel L & Letourneux Y (1995) Antibacterial activity of 7-aminocholesterol, a new sterol. FEMS Microbiol Lett 126: 91-92.
24. Dickson RC & Lester RL (1999) Yeast sphingolipids. Biochim Biophys Acta 1426: 347-357.
25. Dufour JP, Amory A & Goffeau A (1988) Plasma membrane ATPase from the yeast Schizosaccharomyces pombe. Methods Enzymol 157: 513-528.
26. Elkihel L, Soustre I, Karst F & Letourneux Y (1994) Amino- and aminomethylcholesterol derivatives with fungicidal activity. FEMS Microbiol Lett 120: 163-167.
27. Emr SD, Vassarotti A, Garrett J, Geller BL, Takeda M & Douglas MG (1986) The amino terminus of the yeast F1-ATPase beta-subunit precursor functions as a mitochondrial import signal. J Cell Biol 102: 523-533.
28. Gaber RF, Copple DM, Kennedy BK, Vidal M & Bard M (1989) The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol Cell Biol 9: 3447-3456.
29. Gee KR, Sun WC, Bhalgat MK, Upson RH, Klaubert DH, Latham KA & Haugland RP (1999) Fluorogenic substrates based on fluorinated umbelliferones for continuous assays of phosphatases and beta-galactosidases. Anal Biochem 273: 41-48.
30. Ghislain M, Dohmen RJ, Levy F & Varshavsky A (1996) Cdc48p interacts with Ufd3p, a WD repeat protein required for ubiquitin-mediated proteolysis in Saccharomyces cerevisiae. EMBO J 15: 4884-4899.
31. Guarente L (1983) Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol 101: 181-191.
32. Hallstrom TC & Moye-Rowley WS (1998) Divergent transcriptional control of multidrug resistance genes in Saccharomyces cerevisiae. J Biol Chem 273: 2098-2104.
33. Hallstrom TC & Moye-Rowley WS (2000) Multiple signals from dysfunctional mitochondria activate the pleiotropic drug resistance pathway in Saccharomyces cerevisiae. J Biol Chem 275: 37347-37356.
34. Hallstrom TC, Lambert L, Schorling S, Balzi E, Goffeau A & Moye-Rowley WS (2001) Coordinate control of sphingolipid biosynthesis and multidrug resistance in Saccharomyces cerevisiae. J Biol Chem 276: 23674-23680.
35. Iwahashi H, Odani M, Ishidou E & Kitagawa E (2005) Adaptation of Saccharomyces cerevisiae to high hydrostatic pressure causing growth inhibition. FEBS Lett 579: 2847-2852.
36. Iwahashi H, Kitagawa E, Suzuki Y, Ueda Y, Ishizawa YH, Nobumasa H, Kuboki Y, Hosoda H & Iwahashi Y (2007) Evaluation of toxicity of the mycotoxin citrinin using yeast ORF DNA microarray and Oligo DNA microarray. BMC Genomics 8: 95.
37. Johnson SS, Hanson PK, Manoharlal R, Brice SE, Cowart LA & Moye-Rowley WS (2010) Regulation of yeast nutrient permease endocytosis by ATP-binding cassette transporters and a seven-transmembrane protein, RSB1. J Biol Chem 285: 35792-35802.
38. Katzmann DJ, Burnett PE, Golin J, Mahe Y & Moye-Rowley WS (1994) Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol Cell Biol 14: 4653-4661.
39. Katzmann DJ, Epping EA & Moye-Rowley WS (1999) Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Mol Cell Biol 19: 2998-3009.
40. Kean LS, Grant AM, Angeletti C, Mahe Y, Kuchler K, Fuller RS & Nichols JW (1997) Plasma membrane translocation of fluorescent-labeled phosphatidylethanolamine is controlled by transcription regulators, PDR1 and PDR3. J Cell Biol 138: 255-270.
41. Kihara A & Igarashi Y (2002) Identification and characterization of a Saccharomyces cerevisiae gene, RSB1, involved in sphingoid long-chain base release. J Biol Chem 277: 30048-30054.
42. Kihara A & Igarashi Y (2004) Cross talk between sphingolipids and glycerophospholipids in the establishment of plasma membrane asymmetry. Mol Biol Cell 15: 4949-4959.
43. Klinkenberg LG, Mennella TA, Luetkenhaus K & Zitomer RS (2005) Combinatorial repression of the hypoxic genes of Saccharomyces cerevisiae by DNA binding proteins Rox1 and Mot3. Eukaryot Cell 4: 649-660.
44. Kolaczkowska A & Goffeau A (1999) Regulation of pleiotropic drug resistance in yeast. Drug Resist Updat 2: 403-414.
45. Kolaczkowska A, Kolaczkowski M, Goffeau A & Moye-Rowley WS (2008) Compensatory activation of the multidrug transporters Pdr5p, Snq2p, and Yor1p by Pdr1p in Saccharomyces cerevisiae. FEBS Lett 582: 977-983.
46. Kolaczkowski M, Kolaczowska A, Luczynski J, Witek S & Goffeau A (1998) In vivo characterization of the drug resistance profile of the major ABC transporters and other components of the yeast pleiotropic drug resistance network. Microb Drug Resist 4: 143-158.
47. Kolaczkowski M, Kolaczkowska A, Gaigg B, Schneiter R & Moye-Rowley WS (2004) Differential regulation of ceramide synthase components LAC1 and LAG1 in Saccharomyces cerevisiae. Eukaryot Cell 3: 880-892.
48. Kolaczkowski M, Kolaczkowska A, Motohashi N & Michalak K (2009) New high-throughput screening assay to reveal similarities and differences in inhibitory sensitivities of multidrug ATP-binding cassette transporters. Antimicrob Agents Chemother 53: 1516-1527.
49. Kwast KE, Lai LC, Menda N, James DT, 3rd, 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.
50. Manente M & Ghislain M (2009) The lipid-translocating exporter family and membrane phospholipid homeostasis in yeast. FEMS Yeast Res 9: 673-687.
51. Monteiro PT, Mendes ND, Teixeira MC et al. (2008) YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 36: D132-136.
52. Mumberg D, Muller R & Funk M (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 22: 5767-5768.
53. Ness F & Aigle M (1995) RTM1: a member of a new family of telomeric repeated genes in yeast. Genetics 140: 945-956.
54. Niedenthal RK, Riles L, Johnston M & Hegemann JH (1996) Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12: 773-786.
55. Onda M, Ota K, Chiba T, Sakaki Y & Ito T (2004) Analysis of gene network regulating yeast multidrug resistance by artificial activation of transcription factors: involvement of Pdr3 in salt tolerance. Gene 332: 51-59.
56. Panwar SL & Moye-Rowley WS (2006) Long chain base tolerance in Saccharomyces cerevisiae is induced by retrograde signals from the mitochondria. J Biol Chem 281: 6376-6384.
57. Protchenko O, Shakoury-Elizeh M, Keane P, Storey J, Androphy R & Philpott CC (2008) Role of PUG1 in inducible porphyrin and heme transport in Saccharomyces cerevisiae. Eukaryot Cell 7: 859-871.
58. Rahier A, Taton M & Benveniste P (1990) Inhibition of sterol biosynthesis enzymes in vitro by analogues of high-energy carbocationic intermediates. Biochem Soc Trans 18: 48-52.
59. Rose M, Casadaban MJ & Botstein D (1981) Yeast genes fused to beta-galactosidase in Escherichia coli can be expressed normally in yeast. P Natl Acad Sci USA 78: 2460-2464.
60. Rust S, Rosier M, Funke H et al. (1999) Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet 22: 352-355.
61. Sanati H, Belanger P, Fratti R & Ghannoum M (1997) A new triazole, voriconazole (UK-109, 496), blocks sterol biosynthesis in Candida albicans and Candida krusei. Antimicrob Agents Chemother 41: 2492-2496.
62. Sertil O, Kapoor R, Cohen BD, Abramova N & Lowry CV (2003) Synergistic repression of anaerobic genes by Mot3 and Rox1 in Saccharomyces cerevisiae. Nucleic Acids Res 31: 5831-5837.
63. Shahi P & Moye-Rowley WS (2009) Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim Biophys Acta 1794: 852-859.
64. Skrzypek MS, Nagiec MM, Lester RL & Dickson RC (1998) Inhibition of amino acid transport by sphingoid long chain bases in Saccharomyces cerevisiae. J Biol Chem 273: 2829-2834.
65. Soustre I, Letourneux Y & Karst F (1996) Characterization of the Saccharomyces cerevisiae RTA1 gene involved in 7-aminocholesterol resistance. Curr Genet 30: 121-125.
66. van den Hazel HB, Pichler H, do Valle Matta MA, Leitner E, Goffeau A & Daum G (1999) PDR16 and PDR17, two homologous genes of Saccharomyces cerevisiae, affect lipid biosynthesis and resistance to multiple drugs. J Biol Chem 274: 1934-1941.
67. Vik A & Rine J (2001) Upc2p and Ecm22p, dual regulators of sterol biosynthesis in Saccharomyces cerevisiae. Mol Cell Biol 21: 6395-6405.
68. Wach A (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12: 259-265.
69. Wilcox LJ, Balderes DA, Wharton B, Tinkelenberg AH, Rao G & Sturley SL (2002) Transcriptional profiling identifies two members of the ATP-binding cassette transporter superfamily required for sterol uptake in yeast. J Biol Chem 277: 32466-32472.