RPD3 and ROM2 are required for multidrug resistance in Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 8, Issue 3, 2008, Pages 414-424

  Borecka Melkusova, Silvia ^a   Kozovska, Zuzana ^a   Hikkel, Imrich ^a   Dzugasova, Vladimira ^a   Subik, Julius ^a  

^a Faculty of Natural Sciences   (Slovakia)

Author keywords

Multidrug resistance; PDR3; PDR5; ROM2; RPD3; Transcription

Indexed keywords

CYCLOHEXIMIDE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HISTONE DEACETYLASE; MESSENGER RNA; PROTEIN RHO1P; PROTEIN RHO2P; RHO FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PDR1P; TRANSCRIPTION FACTOR PDR3P; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; FUNGAL GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; MULTIDRUG RESISTANCE; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; ROM2 GENE; RPD3 GENE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSPOSON; UPREGULATION;

ANTIFUNGAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; DRUG RESISTANCE, MULTIPLE, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HISTONE DEACETYLASES; RHODAMINES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 42549133119     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2007.00352.x     Document Type: Article

References (76)

1. Audhy A Emr SD (2002) Stt4 PI kinase localizes to the plasma membrane and functions in the PKC1-mediated MAP kinase cascade. Dev Cell 2 : 593 605.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA Struhl K (1989) Current Protocol in Molecular Biology. Willey, New York.
3. Balzi E, Chen W, Ulaszewski S, Capieaux E Goffeau A (1987) The multidrug resistance gene PDR1 from Saccharomyces cerevisiae. J Biol Chem 262 : 16871 16879.
4. Balzi E Goffeau A (1991) Multiple or pleiotropic drug resistance in yeast. Biochim Biophys Acta 1073 : 241 252.
5. Bernstein BE, Tong JK Schreiber SL (2000) Genome-wide studies of histone deacetylase function in yeast. Proc Natl Acad Sci USA 97 : 13708 13713.
6. Bickle M, Deley PA, Schmidt A Hall MN (1998) Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J 17 : 2235 2245.
7. Broco N, Tenreiro S, Viegas CA Sa-Correia I (1999) FLR1 gene (ORF YBR008c) is required for benomyl and methotrexate resistance in Saccharomyces cerevisiae and its benomyl-induced expression is dependent on Pdr3p transcriptional regulator. Yeast 15 : 1595 1608.
8. Burns N, Grimwade B, Ross-Macdonald PB, Choi EY, Finberg K, Roeder GS Snyder M (1994) Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev 8 : 1087 1105.
9. Carrozza MJ, Li B, Flores L et al 2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123 : 581 592.
10. Carvajal E, van den Hazel HB, Cybularz-Kolaczkowska A, Balzi E Goffeau A (1997) Molecular and phenotypic characterization of yeast PDR1 mutants that show hyperactive transcription of various ABC multidrug transporter genes. Mol Gen Genet 256 : 406 415.
11. Chua G, Morris QD, Sopko R, Robinson MD, Ryan O, Chan ET, Frey BJ, Andrews BJ, Boone C Hughes TR (2006) Identifying transcription factor functions and targets by phenotypic activation. Proc Natl Acad Sci USA 103 : 12045 12050.
12. 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.
13. Delahodde A, Pandjaitan R, Corral-Debrinski M Jacq C (2001) Pse1/Kap121-dependent nuclear localization of the major yeast multidrug resistance (MDR) transcription factor Pdr1. Mol Microbiol 39 : 304 312.
14. 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.
15. De Nadal E, Zapater M, Alepuz EM, Sumoy L, Mas G Posas F (2004) The MAPK hog1 recruits Rpd3 histone deacetylase to activate osmoreponsive genes. Nature 427 : 370 374.
16. DeRisi J, van den Hazel B, Marc P, Balzi E, Brown Jacq C Goffeau A (2000) Genome microarray analysis of transcriptional activation in multidrug resistant yeast mutants. FEBS Lett 470 : 156 160.
17. Drgonova J, Drgon T, Tanaka K, Kollar R, Chen GC, Ford RA, Chan CS, Takai Y Cabib E (1996) Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272 : 277 279.
18. Edlind Y, Smith L, Henry K, Katiyar S Nickels J (2002) Antifungal activity in Saccharomyces cerevisiae is modulated by calcium signaling. Mol Microbiol 46 : 257 268.
19. Edlind TD, Henry KW, Vermitsky JP, Edlind MP, Raj S Katyar SK (2005) Promoter-dependent disruption of genes: simple, rapid, and specific PCR-based method with application to three different yeast. Curr Genet 48 : 117 125.
20. Ekwall K (2005) Genome-wide analysis of HDAC function. Trends Gen 21 : 608 615.
21. Fardeau V, Lelandais G, Oldfield A, Salin H, Lemoine S, Garcia M, Tanty V, Le Crom S, Jacq C Devaux F (2006) The central role of PDR1 in the foundation of yeast drug resistance. J Biol Chem 282 : 5063 5074.
22. 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.
23. Heinisch JJ, Lorberg A, Schmitz HP Jacoby JJ (1999) The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol Microbiol 32 : 671 680.
24. Hohmann SM Mager WH (2003) Yeast Stress Responses. Springer, Berlin.
25. Gao C, Wang L, Milgrom E Shen WC (2004) On the mechanism of constitutive Pdr1 activator mediated PDR5 transcription in Saccharomyces cerevisiae: evidence for enhanced recruitment of coactivators and altered nucleosome structures. J Biol Chem 279 : 42677 42686.
26. Jain P, Akula I Edlind T (2003) Cyclic AMP signaling pathway modulates susceptibility of Candida species and Saccharomyces cerevisiae to antifungal azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Chemother 47 : 3195 3201.
27. Jungwirth H Kuchler K (2006) Yeast ABC transporters - a tale of sex, stress, drugs and aging. FEBS Lett 580 : 1131 1138.
28. 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.
29. Khorasanizadeh S (2004) The nucleosome: from genomic organization to genomic regulation. Cell 116 : 259 272.
30. Kolaczkowska A Goffeau A (1999) Regulation of pleiotropic drug resistance in yeast. Drug Resist Updates 2 : 403 414.
31. Kolaczkowski M, van der Rest M, Cybularz-Kolaczkowska A, Soumillion JP, Konigs WN Goffeau A (1996) Anticancer drugs, ionophoric peptides, and steroids as substrates of the multidrug transporter Pdr5p. J Biol Chem 271 : 31543 31548.
32. Kolaczkowski M, Kolaczkowska A, Luczinski 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.
33. Kurdistani SK Grunstein M (2003) Histone acetylation and deacetylation in yeast. Nat Genet 31 : 248 254.
34. MacPherson S, Larochelle M Turcotte B (2006) A fungal family of transcriptional regulators, the zinc cluster proteins. Microb Mol Biol Rev 70 : 583 604.
35. Madden K, Sheu YJ, Baetz K, Andrews B Snyder M (1997) SBF cell cycle regulator as a target of the yeast PKC-MAP kinase pathway. Science 275 : 1781 1784.
36. Mai A, Rotili D, Massa S, Brosch G, Simonetti G, Passariello C Palamara AT (2007) Discovery of uracil-based histone deacetylase inhibitors able to reduce acquired antifungal resistance and trailing growth in Candida albicans. Bioorg Med Chem Lett 17 : 1221 1225.
37. Mamnun YM, Pandjaitan R, Mahe Y, Delahodde A Kuchler K (2002) The yeast zinc finger regulators Pdr1p and Pdr3p control pleiotropic drug resistance (PDR) as homo- and heterodimers in vivo. Mol Microbiol 46 : 1429 1440.
38. Mamnun YM, Schuller C Kuchler K (2004) Expression regulation of the yeast PDR5 ATP-binding cassette (ABC) transporter suggests a role in cellular detoxification during the exponential growth phase. FEBS Lett 559 : 111 117.
39. Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20 : 2471 2472.
40. Michalkova-Papajova D, Obernauerova M Subik J (2000) Role of the PDR gene network in yeast susceptibility to the antifungal antibiotic mucidin. Antimicrob Agents Chemother 44 : 418 420.
41. Miyahara K, Hirata D Miyakawa T (1996) yAP-1- and yAP-2-mediated, heat shock-induced transcriptional activation of the multidrug resistance ABC transporter genes in Saccharomyces cerevisiae. Curr Genet 29 : 103 105.
42. Moye-Rowley WS (2003) Transcriptional control of multidrug resistance in the yeast Saccharomyces. Prog Nucleic Acid Res Mol Biol 73 : 251 279.
43. Mukhopadhyay K, Kohli A Prasad R (2002) Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob Agents Chemother 46 : 3695 3705.
44. Nakamura K, Niimi M, Niimi K, Holmes AR, Yates JE, Decottignies A, Monk BC, Goffeau A Cannon RD (2001) Functional expression of Candida albicans drug efflux pump Cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob Agents Chemother 45 : 3366 3374.
45. Nourani A, Papajova D, Delahodde A, Jacq C Subik J (1997) Clustered amino acid substitutions in the yeast transcription regulator Pdr3p increase pleiotropic drug resistance and identify a new central regulatory domain. Mol Gen Genet 256 : 397 405.
46. Ogawa A, Hashida-Okado T, Endo M, Yoshioka H, Tsuruo T, Takesako K Kato I (1998) Role of ABC transporters in aureobasidin a resistance. Antimicrob Agents Chemother 42 : 755 761.
47. Park JI, Collinson EJ, Grant CM Dawes IW (2005) Rom2p, the Rho1 GTP/GDP exchange factor of Saccharomyces cerevisiae, can mediate stress responses via the Ras-cAMP pathway. J Biol Chem 280 : 2529 2535.
48. Proft M Struhl K (2002) Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress. Mol Cell 9 : 1307 1317.
49. Reinoso-Martin C, Schuller C, Schutzer-Muehlbauer M Kuchler K (2003) The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryotic Cell 2 : 1200 1210.
50. Robyr D, Suka Y, Xenarios I, Kurdistani SK, Wang A, Suka N Grunstein M (2002) Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109 : 437 446.
51. Roth SY, Denu JM Allis CD (2001) Histone acetyltransferases. Annu Rev Biochem 70 : 81 120.
52. Rozen S Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology (Krawetz S Misener S, eds), pp. 365 386. Humana Press, Totowa, NJ.
53. Rundlett SE, Carmen AA, Kobayashi R, Bavykin S, Turner BM Grunstein M (1996) HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci USA 93 : 14503 14508.
54. Sakchaisri K, Asano S, Yu LR, Shulewitz MJ, Park CJ, Cho YW, Veenstra TD, Thorner J Lee KS (2004) Coupling morphogenesis to mitotic entry. Proc Natl Acad Sci USA 101 : 4124 4129.
55. Sambrook J, Fritsch EF Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Sanglard D, Ischer F, Marchetti O, Entenza J Bille J (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48 : 959 976.
57. Schmidt A, Bickle M, Beck T Hall MN (1997) The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell 88 : 531 542.
58. Sharma VM, Tomar RS, Dempsey AE Reese JC (2007) Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage-induced genes. Mol Cell Biol 27 : 3199 3210.
59. Sertil O, Vemula A, Salmon SL, Morse RH Lowry CV (2007) Direct role for the Rpd3 complex in transcriptional induction of the anaerobic DAN/TIR genes in yeast. Mol Cell Biol 27 : 2037 2047.
60. Sidorova M, Drobna E, Dzugasova V, Hikkel I Subik J (2007) Loss-of-function pdr3 mutations convert the Pdr3p transcription activator to a protein suppressing multidrug resistance in Saccharomyces cerevisiae. FEMS Yeast Lett 7 : 254 264.
61. Simonetti G, Passariello C, Rotili D, Mai A, Garici E Plamara AT (2007) Histone deacetylase inhibitors may reduce pathogenicity and virulence Candida albicans. FEMS Yeast Res 8 : 1 10.
62. Simonics T, Kozovska Z, Michalkova-Papajova D, Delahodde A, Jacq C Subik J (2000) Isolation and molecular characterization of the carboxy-terminal pdr3 mutants in Saccharomyces cerevisiae. Curr Genet 38 : 248 255.
63. Smith WL Edlind TD (2002) Histine deacetylase inhibitors enhance Candida albicans sensitivity to azoles and related antifungals: correlation with reduction in CDR and ERG upregulation. Antimicrob Agents Chemother 46 : 3532 3539.
64. Souid AK, Gao C, Wang L, Milgrom E Shen WC (2006) ELM1 is required for multidrug resistance in Saccharomyces cerevisiae. Genetics 173 : 1919 1937.
65. Struhl K (1998) Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12 : 599 606.
66. Subik J, Ulaszewski S Goffeau A (1986) Genetic mapping of nuclear mucidin resistance mutations in Saccharomyces cerevisiae. A new PDR locus on chromosome II. Curr Genet 10 : 665 670.
67. Thompson JR, Register E, Curotto J, Kurtz M Kelly R (1998) An improved protocol for the preparation of yeast cells for transformation by electroporation. Yeast 14 : 565 571.
68. Vannier D, Balderes D Shore D (1996) Evidence that the transcriptional regulators SIN3 and RPD3, and a novel gene (SDS3) with similar functions, are involved in transcriptional silencing in S. cerevisiae. Genetics 144 : 1343 1353.
69. Vannier D, Damay P Shore D (2001) A role for Sds3p, a component of the Rpd3p/Sin3p deacetylase complex, in maintaining cellular integrity in Saccharomyces cerevisiae. Mol Genet Genomics 265 : 560 568.
70. Vay HA, Philip B Levin DE (2004) Mutational analysis of the cytoplasmic domain of the Wsc1 cell wall stress sensor. Microbiol 150 : 3281 3288.
71. Vilella F, Herrero E, Torres J de al Torre-Ruiz MA (2005) Pkc1 and the upstream elements of the cell integrity pathway in Saccharomyces cerevisiae, Rom2 and Mtl1, are required for cellular responses to oxidative stress. J Biol Chem 280 : 9149 9159.
72. Wang A, Kurdistani SK Grunstein M (2002) Requirement of Hos2 histone deacetylases for gene activity in yeast. Science 298 : 1412 1414.
73. Ward AC (1990) Single step purification of shuttle vectors from yeast for high frequency back-transformation into E. coli. Nucleic Acid Res 18 : 5319.
74. Workman JL Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67 : 545 579.
75. Workman CT, Mak HC, McCuine S, Tagne JB, Agarwal M, Ozier O, Begley TJ, Samson AD Ideker T (2006) A systems approach to mapping DNA damage response pathways. Science 312 : 1054 1059.
76. Ye P, Peyser BD, Pan X, Boeke JD, Spencer FA Bader JS (2005) Gene function prediction from congruent synthetic lethal interactions in yeast. Mol Syst Biol 1 : 2005.0026.