Fungal ABC proteins: Pleiotropic drug resistance, stress response and cellular detoxification

Research in Microbiology

Volumn 152, Issue 3-4, 2001, Pages 375-389

  Wolfger, Hubert ^a   Mamnun, Yasmine M ^a   Kuchler, Karl ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

ABC protein; Antifungal resistance; Detoxification; Pathogen; Stress response; Yeast

Indexed keywords

ABC TRANSPORTER; ANTIBIOTIC AGENT; BILIRUBIN; BREFELDIN A; CILOFUNGIN; CYCLOHEXIMIDE; FLUCONAZOLE; FLUORESCEIN; GLUTATHIONE; GLYCOPROTEIN P; HEAVY METAL; ITRACONAZOLE; KETOCONAZOLE; LONG CHAIN FATTY ACID; MULTIDRUG RESISTANCE PROTEIN; MUTAGENIC AGENT; OLIGOMYCIN; PLANT TOXIN; PROTEIN KINASE (CALCIUM,CALMODULIN); RHODAMINE; STEROID; TACROLIMUS; TAUROCHOLIC ACID; TRANSCRIPTION FACTOR; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNINDEXED DRUG; VALINOMYCIN; VANADIC ACID; VINBLASTINE; ZINC FINGER PROTEIN;

ARTICLE; DETOXIFICATION; DRUG RESISTANCE; GENE; MULTIDRUG RESISTANCE; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; STRESS; TRANSCRIPTION REGULATION;

ANTIFUNGAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CANDIDA ALBICANS; DNA-BINDING PROTEINS; DRUG RESISTANCE, FUNGAL; HUMANS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ASPERGILLUS; BACTERIA (MICROORGANISMS); CANDIDA; EUKARYOTA; FUNGI; MAMMALIA; PROTISTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 0035019470     PISSN: 09232508     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0923-2508(01)01209-8     Document Type: Article

References (137)

1. Alarco A.M., Raymond M. The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J. Bacteriol. 181:1999;700-708.
2. Ambudkar S.V., Gottesmann M.M. ABC Transporters: Biochemical, Cellular, and Molecular Aspects. 292:1998;Academic Press, San Diego, CA, USA.
3. Andrade A.C., Del Sorbo G., Van Nistelrooy J.G., Waard M.A. The ABC transporter atrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds. Microbiology. 146:2000;1987-1997.
4. Andrade A.C., Van Nistelrooy J.G., Peery R.B., Skatrud P.L., De Waard M.A. The role of ABC transporters from Aspergillus nidulans in protection against cytotoxic agents and in antibiotic production. Mol. Gen. Genet. 263:2000;966-977.
5. Balan I., Alarco A.M., Raymond M. The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter. J. Bacteriol. 179:1997;7210-7218.
6. Balzi E., Chen W., Ulaszewski S., Capieaux E., Goffeau A. The multidrug resistance gene PDR1 from Saccharomyces cerevisiae. J. Biol. Chem. 262:1987;16871-16879.
7. Balzi E., Wang M., Léterme S., Van Dyck L., Goffeau A. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:1994;2206-2214.
8. Barchiesi F., Calabrese D., Sanglard D., Falconi Di Francesco L., Caselli F., et al. Experimental induction of fluconazole resistance in Candida tropicalis ATCC 750. Antimicrob. Agents Chemother. 44:2000;1578-1584.
9. Bauer B.E., Wolfger H., Kuchler K. Inventory and function of yeast ABC proteins: About sex, stress, pleiotropic drug and heavy metal resistance. Biochim. Biophys. Acta. 1461:1999;217-236.
10. Belfield G.P., Ross-Smith N.J., Tuite M.F. Translation elongation factor-3 (EF-3): An evolving eukaryotic ribosomal protein? J. Mol. Evol. 41:1995;376-387.
11. Bissinger P.H., Kuchler K. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:1994;4180-4186.
12. Bobrowicz P., Wysocki R., Owsianik G., Goffeau A., Ulaszewski S. Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast. 13:1997;819-828.
13. Brandl C.J., Furlanetto A.M., Martens J.A., Hamilton K.S. Characterization of NGG1, a novel yeast gene required for glucose repression of GAL4p-regulated transcription. EMBO J. 12:1993;5255-5265.
14. Browne B.L., McClendon V., Bedwell D.M. Mutations within the first LSGGQ motif of Ste6p cause defects in a-factor transport and mating in Saccharomyces cerevisiae. J. Bacteriol. 178:1996;1712-1719.
15. Christensen P.U., Davey J., Nielsen O. The Schizosaccharomyces pombe mam1 gene encodes an ABC transporter mediating secretion of M-factor. Mol. Gen. Genet. 255:1997;226-236.
16. Christensen P.U., Davis K., Nielsen O., Davey J. Abc1: A new ABC transporter from the fission yeast Schizosaccharomyces pombe. FEMS Microbiol. Lett. 147:1997;97-102.
17. Cole S.P., Deeley R.G. Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays. 20:1998;931-940.
18. Coleman S.T., Epping E.A., Steggerda S.M., Moye-Rowley W.S. Yap1p activates gene transcription in an oxidant-specific fashion. Mol. Cell Biol. 19:1999;8302-8313.
19. Cui Z., Hirata D., Tsuchiya E., Osada H., Miyakawa T. The multidrug resistance-associated protein (MRP) subfamily (Yrs1/Yor1) of Saccharomyces cerevisiae is important for the tolerance to a broad range of organic anions. J. Biol. Chem. 271:1996;14712-14716.
20. Cui Z., Shiraki T., Hirata D., Miyakawa T. Yeast gene YRR1, which is required for resistance to 4-nitroquinoline N-oxide, mediates transcriptional activation of the multidrug resistance transporter gene SNQ2. Mol. Microbiol. 29:1998;1307-1315.
21. Dean M., Allikmets R. Evolution of ATP-binding cassette transporter genes. Curr. Opin. Genet. Dev. 5:1995;779-785.
22. Decottignies A., Goffeau A. Complete inventory of the yeast ABC proteins. Nat. Genet. 15:1997;137-145.
23. Decottignies A., Grant A.M., Nichols J.W., de Wet H., McIntosh D.B., et al. ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273:1998;12612-12622.
24. Decottignies A., Lambert L., Catty P., Degand H., Epping E.A., et al. Identification and characterization of SNQ2, a new multidrug ATP-binding cassette transporter of the yeast plasma membrane. J. Biol. Chem. 270:1995;18150-18157.
25. Decottignies A., Owsianik G., Ghislain M. Casein kinase I-dependent phosphorylation and stability of the yeast multidrug transporter Pdr5p. J. Biol. Chem. 274:1999;37139-37146.
26. Del Sorbo G., Andrade A.C., Van Nistelrooy J.G., Van Kan J.A., Balzi E., et al. Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters. Mol. Gen. Genet. 254:1997;417-426.
27. Delahodde A., Delaveau T., Jacq C. Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol. Cell. Biol. 15:1995;4043-4051.
28. Delaveau T., Delahodde A., Carvajal E., Subik J., Jacq C. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244:1994;501-511.
29. DeRisi J., van den Hazel B., Marc P., Balzi E., Brown P., et al. Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. FEBS Lett. 470:2000;156-160.
30. Dogra S., Krishnamurthy S., Gupta V., Dixit B.L., Gupta C.M., et al. Asymmetric distribution of phosphatidylethanolamine in C. albicans: Possible mediation by CDR1, a multidrug transporter belonging to ATP binding cassette (ABC) superfamily. Yeast. 15:1999;111-121.
31. Egner R., Kuchler K. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett. 378:1996;177-181.
32. Egner R., Mahé Y., Pandjaitan R., Kuchler K. Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:1995;5879-5887.
33. Egner R., Rosenthal F.E., Kralli A., Sanglard D., Kuchler K. Genetic separation of FK506 susceptibility and drug transport in the yeast Pdr5 ATP-binding cassette multidrug resistance transporter. Mol. Biol. Cell. 9:1998;523-543.
34. Falcon-Perez J.M., Mazon M.J., Molano J., Eraso P. Functional domain analysis of the yeast ABC transporter Ycf1p by site-directed mutagenesis. J. Biol. Chem. 274:1999;23584-23590.
35. Fernandes L., Rodrigues-Pousada C., Struhl K. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol. Cell. Biol. 17:1997;6982-6993.
36. Franz R., Kelly S.L., Lamb D.C., Kelly D.E., Ruhnke M., et al. Multiple molecular mechanisms contribute to a stepwise development of fluconazole resistance in clinical Candida albicans strains. Antimicrob. Agents Chemother. 42:1998;3065-3072.
37. Franz R., Michel S., Morschhauser J. A fourth gene from the Candida albicans CDR family of ABC transporters. Gene. 220:1998;91-98.
38. Gärtner J., Moser H., Valle D. Mutations in the 70K peroxisomal membrane protein gene in Zellweger syndrome. Nat. Genet. 1:1992;16-23.
39. Ghosh M., Shen J., Rosen B.P. Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. (USA). 96:1999;5001-5006.
40. Goodall S.D., Gilkens M.M.C., Stergiopoulos I., Venema K., Zwiers L.-H., De Waard M.A. ABC transporters of Mycosphaerella graminicola, a fungal pathogen of wheat. 2nd FEBS advanced lecture course - ATP-binding cassette transporters: From multidrug resistance to genetic disease. 1999;77 Gosau.
41. Gottesman M.M., Hrycyna C.A., Schoenlein P.V., Germann U.A., Pastan I. Genetic analysis of the multidrug transporter. Annu. Rev. Genet. 29:1995;607-649.
42. Gustin M.C., Albertyn J., Alexander M., Davenport K. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1998;1264-1300.
43. Hallström T.C., Katzmann D.J., Torres R.J., Sharp W.J., Moye-Rowley W.S. Regulation of transcription factor Pdr1p function by an Hsp70 protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1998;1147-1155.
44. Hallström T.C., Moye-Rowley W.S. Divergent transcriptional control of multidrug resistance genes in Saccharomyces cerevisiae. J. Biol. Chem. 273:1998;2098-2104.
45. Hallström T.C., Moye-Rowley W.S. Hyperactive forms of the Pdr1p transcription factor fail to respond to positive regulation by the hsp70 protein Pdr13p. Mol. Microbiol. 36:2000;402-413.
46. Hallström T.C., Moye-Rowley W.S. Multiple signals from dysfunctional mitochondria activate the pleiotropic drug resistance pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275:2000;37347-37356.
47. Hellauer K., Rochon M.H., Turcotte B. A novel DNA binding motif for yeast zinc cluster proteins: The Leu3p and Pdr3p transcriptional activators recognize everted repeats. Mol. Cell. Biol. 16:1996;6096-6102.
48. Hernaez M.L., Gil C., Pla J., Nombela C. Induced expression of the Candida albicans multidrug resistance gene CDR1 in response to fluconazole and other antifungals. Yeast. 14:1998;517-526.
49. Hettema E.H., Tabak H.F. Transport of fatty acids and metabolites across the peroxisomal membrane. Biochim. Biophys. Acta. 1486:2000;18-27.
50. Hettema E.H., van Roermund C.W., Distel B., van den Berg M., Vilela C., et al. The ABC transporter proteins Pat1 and Pat2 are required for import of long-chain fatty acids into peroxisomes of Saccharomyces cerevisiae. EMBO J. 15:1996;3813-3822.
51. Hirata D., Yano K., Miyahara K., Miyakawa T. Saccharomyces cerevisiae YDR1, which encodes a member of the ATP-binding cassette (ABC) superfamily, is required for multidrug resistance. Curr. Genet. 26:1994;285-294.
52. Holyoak C.D., Bracey D., Piper P.W., Kuchler K., Coote P.J. The Saccharomyces cerevisiae weak-acid-inducible ABC transporter Pdr12p transports fluorescein and preservative anions from the cytosol by an energy-dependent mechanism. J. Bacteriol. 181:1999;4644-4652.
53. Holyoak C.D., Thompson S., Ortiz Calderon C., Hatzixanthis K., Bauer B., et al. Loss of Cmk1 Ca(2+)-calmodulin-dependent protein kinase in yeast results in constitutive weak organic acid resistance, associated with a post-transcriptional activation of the Pdr12 ATP-binding cassette transporter. Mol. Microbiol. 37:2000;595-605.
54. Jungwirth H., Wendler F., Platzer B., Bergler H., Högenauer G. Diazaborine resistance in yeast involves the efflux pumps Ycf1p and Flr1p and is enhanced by a gain-of-function allele of gene YAP1. Eur. J. Biochem. 267:2000;4809-4816.
55. Katzmann D.J., Burnett P.E., Golin J., Mahé Y., Moye-Rowley W.S. Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14:1994;4653-4661.
56. Katzmann D.J., Epping E.A., Moye-Rowley W.S. Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Mol. Cell. Biol. 19:1999;2998-3009.
57. Katzmann D.J., Hallström T.C., Mahé Y., Moye-Rowley W.S. Multiple Pdr1p/Pdr3p binding sites are essential for normal expression of the ATP-binding cassette transporter protein-encoding gene PDR5. J. Biol. Chem. 271:1996;23049-23054.
58. Katzmann D.J., Hallström T.C., Voet M., Wysock W., Golin J., et al. Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:1995;6875-6883.
59. Kispal G., Csere P., Guiard B., Lill R. The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett. 418:1997;346-350.
60. Kispal G., Csere P., Prohl C., Lill R. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J. 18:1999;3981-3989.
61. Kolaczkowska A., Goffeau, A. Regulation of Pleiotropic Drug Resistance in Yeast. Drug Resistance Updates. 2:1999;403-414.
62. Kolaczkowski M., Kolaczowska A., Luczynski J., Witek S., Goffeau A. 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. 4:1998;143-158.
63. Kölling R., Hollenberg C.P. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:1994;3261-3271.
64. Kölling R., Losko S. The linker region of the ABC-transporter Ste6 mediates ubiquitination and fast turnover of the protein. EMBO J. 16:1997;2251-2261.
65. Kontoyiannis D.P. Genetic analysis of azole resistance by transposon mutagenesis in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 43:1999;2731-2735.
66. Kralli A., Bohen S.P., Yamamoto K.R. LEM1, an ATP-binding-cassette transporter, selectively modulates the biological potency of steroid hormones. Proc. Natl. Acad. Sci. (USA). 92:1995;4701-4705.
67. Kralli A., Yamamoto K.R. An FK506-sensitive transporter selectively decreases intracellular levels and potency of steroid hormones. J. Biol. Chem. 271:1996;17152-17156.
68. Krishnamurthy S., Gupta V., Snehlata P., Prasad R. Characterisation of human steroid hormone transport mediated by Cdr1p, a multidrug transporter of Candida albicans, belonging to the ATP binding cassette super family. FEMS Microbiol. Lett. 158:1998;69-74.
69. Kuchler K. Unusual routes of protein secretion: The easy way out. Trends Cell Biol. 3:1993;421-426.
70. Kuchler K., Sterne R.E., Thorner J. Saccharomyces cerevisiae STE6 gene product: A novel pathway for protein export in eukaryotic cells. EMBO J. 8:1989;3973-3984.
71. Kuge S., Jones N., Nomoto A. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J. 16:1997;1710-1720.
72. Leighton J., Schatz G. An ABC transporter in the mitochondrial inner membrane is required for normal growth of yeast. EMBO J. 14:1995;188-195.
73. Li Z.S., Lu Y.P., Zhen R.G., Szczypka M., Thiele D.J., et al. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc. Natl. Acad. Sci. (USA). 94:1997;42-47.
74. Loayza D., Michaelis S. Role for the ubiquitin-proteasome system in the vacuolar degradation of Ste6p, the a-factor transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1998;779-789.
75. Loayza D., Tam A., Schmidt W.K., Michaelis S. Ste6p mutants defective in exit from the endoplasmic reticulum (ER) reveal aspects of an ER quality control pathway in Saccharomyces cerevisiae. Mol. Biol. Cell. 9:1998;2767-2784.
76. Lyons C.N., White T.C. Transcriptional analyses of antifungal drug resistance in Candida albicans. Antimicrob. Agents Chemother. 44:2000;2296-2303.
77. Maesaki S., Marichal P., Vanden Bossche H., Sanglard D., Kohno S. Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains. J. Antimicrob. Chemother. 44:1999;27-31.
78. Mahé Y., Lemoine Y., Kuchler K. The ATP-binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J. Biol. Chem. 271:1996;25167-25172.
79. Mahé Y., Parle-McDermott A., Nourani A., Delahodde A., Lamprecht A., et al. The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: A novel target for the transcription factors Pdr1 and Pdr3. Mol. Microbiol. 20:1996;109-117.
80. Marichal P., Koymans L., Willemsens S., Bellens D., Verhasselt P., et al. Contribution of mutations in the cytochrome P450 14alpha-demethylase (Erg11p, Cyp51p) to azole resistance in Candida albicans. Microbiology. 145:1999;2701-2713.
81. Marr K.A., Lyons C.N., Rustad T., Bowden R.A., White T.C. Rapid, transient fluconazole resistance in Candida albicans is associated with increased mRNA levels of CDR. Antimicrob. Agents Chemother. 42:1998;2584-2589.
82. Martens J.A., Genereaux J., Saleh A., Brandl C.J. Transcriptional activation by yeast PDR1p is inhibited by its association with NGG1p/ADA3p. J. Biol. Chem. 271:1996;15884-15890.
83. Martinez-Pastor M.T., Marchler G., Schüller C., Marchler-Bauer A., Ruis H., et al. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15:1996;2227-2235.
84. Marton M.J., Vazquez de Aldana C.R., Qiu H., Chakraburtty K., Hinnebusch A.G. Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol. Cell. Biol. 17:1997;4474-4489.
85. Maurice T.C., Mazzucco C.E., Ramanathan C.S., Ryan B.M., Warr G.A., et al. A highly conserved intraspecies homolog of the Saccharomyces cerevisiae elongation factor-3 encoded by the HEF3 gene. Yeast. 14:1998;1105-1113.
86. McGrath J.P., Varshavsky A. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature. 340:1989;400-404.
87. Michalkova-Papajova D., Obernauerova M., Subik J. Role of the PDR gene network in yeast susceptibility to the antifungal antibiotic mucidin. Antimicrob. Agents Chemother. 44:2000;418-420.
88. Miyahara K., Mizunuma M., Hirata D., Tsuchiya E., Miyakawa T. The involvement of the Saccharomyces cerevisiae multidrug resistance transporters Pdr5p and Snq2p in cation resistance. FEBS Lett. 399:1996;317-320.
89. Miyazaki H., Miyazaki Y., Geber A., Parkinson T., Hitchcock C., et al. Fluconazole resistance associated with drug efflux and increased transcription of a drug transporter gene, PDH1, in Candida glabrata. Antimicrob. Agents Chemother. 42:1998;1695-1701.
90. Moran G.P., Sanglard D., Donnelly S.M., Shanley D.B., Sullivan D.J., et al. Identification and expression of multidrug transporters responsible for fluconazole resistance in Candida dubliniensis. Antimicrob. Agents Chemother. 42:1998;1819-1830.
91. Mosser J., Douar A.M., Sarde C.O., Kioschis P., Feil R., et al. Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature. 361:1993;726-730.
92. Moye-Rowley W.S., Harshman K.D., Parker C.S. Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev. 3:1989;283-292.
93. Nagao K., Taguchi Y., Arioka M., Kadokura H., Takatsuki A., et al. bfr1+, a novel gene of Schizosaccharomyces pombe which confers brefeldin A resistance, is structurally related to the ATP-binding cassette superfamily. J. Bacteriol. 177:1995;1536-1543.
94. Nakaune R., Adachi K., Nawata O., Tomiyama M., Akutsu K., et al. A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Appl. Environ. Microbiol. 64:1998;3983-3988.
95. Nikaido H. Multiple antibiotic resistance and efflux. Curr. Opin. Microbiol. 1:1998;516-523.
96. Nishi K., Yoshida M., Nishimura M., Nishikawa M., Nishiyama M., et al. A leptomycin B resistance gene of Schizosaccharomyces pombe encodes a protein similar to the mammalian P-glycoproteins. Mol. Microbiol. 6:1992;761-769.
97. Nourani A., Papajova D., Delahodde A., Jacq C., Subik J. Clustered amino acid substitutions in the yeast transcription regulator Pdr3p increase pleiotropic drug resistance and identify a new central regulatory domain. Mol. Gen. Genet. 256:1997;397-405.
98. Nourani A., Wesolowski-Louvel M., Delaveau T., Jacq C., Delahodde A. Multiple-drug-resistance phenomenon in the yeast Saccharomyces cerevisiae: Involvement of two hexose transporters. Mol. Cell. Biol. 17:1997;5453-5460.
99. Ogawa A., Hashida-Okado T., Endo M., Yoshioka H., Tsuruo T., et al. Role of ABC transporters in aureobasidin A resistance. Antimicrob. Agents Chemother. 42:1998;755-761.
100. Ortiz D.F., Ruscitti T., McCue K.F., Ow D.W. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 270:1995;4721-4728.
101. Ortiz D.F., St. Pierre M.V., Abdulmessih A., Arias I.M. A yeast ATP-binding cassette-type protein mediating ATP-dependent bile acid transport. J. Biol. Chem. 272:1997;15358-15365.
102. Petrovic S., Pascolo L., Gallo R., Cupelli F., Ostrow J.D., et al. The products of YCF1 and YLL015w (BPT1) cooperate for the ATP-dependent vacuolar transport of unconjugated bilirubin in Saccharomyces cerevisiae. Yeast. 16:2000;561-571.
103. Piper P., Mahé Y., Thompson S., Pandjaitan R., Holyoak C., et al. The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J. 17:1998;4257-4265.
104. Plemper R.K., Egner R., Kuchler K., Wolf D.H. Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J. Biol. Chem. 273:1998;32848-32856.
105. Prasad R., De Wergifosse P., Goffeau A., Balzi E. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet. 27:1995;320-329.
106. Rebbeor J.F., Connolly G.C., Dumont M.E., Ballatori N. ATP-dependent transport of reduced glutathione on YCF1, the yeast orthologue of mammalian multidrug resistance associated proteins. J. Biol. Chem. 273:1998;33449-33454.
107. Reid R.J., Kauh E.A., Bjornsti M.A. Camptothecin sensitivity is mediated by the pleiotropic drug resistance network in yeast. J. Biol. Chem. 272:1997;12091-12099.
108. Riordan J.R. Cystic fibrosis as a disease of misprocessing of the cystic fibrosis transmembrane conductance regulator glycoprotein. Am. J. Hum. Genet. 64:1999;1499-1504.
109. Sandbaken M., Lupisella J.A., DiDomenico B., Chakraburtty K. Isolation and characterization of the structural gene encoding elongation factor 3. Biochim. Biophys. Acta. 1050:1990;230-234.
110. Sanglard D., Ischer F., Calabrese D., Majcherczyk P.A., Bille J. The ATP binding cassette transporter gene CgCDR1 from Candida glabrata is involved in the resistance of clinical isolates to azole antifungal agents. Antimicrob. Agents Chemother. 43:1999;2753-2765.
111. Sanglard D., Ischer F., Monod M., Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: Characterization of CDR2, a new multidrug ABC transporter gene. Microbiology. 143:1997;405-416.
112. Sanglard D., Kuchler K., Ischer F., Pagani J.L., Monod M., et al. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob. Agents Chemother. 39:1995;2378-2386.
113. Sarthy A.V., McGonigal T., Capobianco J.O., Schmidt M., Green S.R., et al. Identification and kinetic analysis of a functional homolog of elongation factor 3, YEF3 in Saccharomyces cerevisiae. Yeast. 14:1998;239-253.
114. Servos J., Haase E., Brendel M. Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol. Gen. Genet. 236:1993;214-218.
115. Shani N., Vallé D. A Saccharomyces cerevisiae homolog of the human adrenoleukodystrophy transporter is a heterodimer of two half ATP-binding cassette transporters. Proc. Natl. Acad. Sci. (USA). 93:1996;11901-11906.
116. Stieger B., Meier P.J. Bile acid and xenobiotic transporters in liver. Curr. Opin. Cell. Biol. 10:1998;462-467.
117. Swartzman E.E., Viswanathan M.N., Thorner J. The PAL1 gene product is a peroxisomal ATP-binding cassette transporter in the yeast Saccharomyces cerevisiae. J. Cell Biol. 132:1996;549-563.
118. Szczypka M.S., Wemmie J.A., Moye-Rowley W.S., Thiele D.J. A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem. 269:1994;22853-22857.
119. Taglicht D., Michaelis S. Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol. 292:1998;130-162.
120. Talibi D., Raymond M. Isolation of a putative Candida albicans transcriptional regulator involved in pleiotropic drug resistance by functional complementation of a pdr1 pdr3 mutation in Saccharomyces cerevisiae. J. Bacteriol. 181:1999;231-240.
121. Thornewell S.J., Peery R.B., Skatrud P.L. Cloning and characterization of CneMDR1: A Cryptococcus neoformans gene encoding a protein related to multidrug resistance proteins. Gene. 201:1997;21-29.
122. Tobin M.B., Peery R.B., Skatrud P.L. Genes encoding multiple drug resistance-like proteins in Aspergillus fumigatus and Aspergillus flavus. Gene. 200:1997;11-23.
123. Tommasini R., Evers R., Vogt E., Mornet C., Zaman G.J., et al. The human multidrug resistance-associated protein functionally complements the yeast cadmium resistance factor 1. Proc. Natl. Acad. Sci. (USA). 93:1996;6743-6748.
124. Toone W.M., Kuge S., Samuels M., Morgan B.A., Toda T., et al. Regulation of the fission yeast transcription factor Pap1 by oxidative stress: Requirement for the nuclear export factor Crm1 (Exportin) and the stress-activated MAP kinase Sty1/Spc1. Genes Dev. 12:1998;1453-1463.
125. Turi T.G., Rose J.K. Characterization of a novel Schizosaccharomyces pombe multidrug resistance transporter conferring brefeldin A resistance. Biochem. Biophys. Res. Commun. 213:1995;410-418.
126. Urban M., Bhargava T., Hamer J.E. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J. 18:1999;512-521.
127. Vanden Bossche H., Dromer F., Improvisi I., Lozano-Chiu M., Rex J.H., et al. Antifungal drug resistance in pathogenic fungi. Med. Mycol. 36:1998;119-128.
128. Vazquez de Aldana C.R., Marton M.J., Hinnebusch A.G. GCN20, a novel ATP binding cassette protein, and GCN1 reside in a complex that mediates activation of the eIF-2 alpha kinase GCN2 in amino acid-starved cells. EMBO J. 14:1995;3184-3199.
129. Verleur N., Hettema E.H., van Roermund C.W., Tabak H.F., Wanders R.J. Transport of activated fatty acids by the peroxisomal ATP-binding-cassette transporter Pxa2 in a semi-intact yeast cell system. Eur. J. Biochem. 249:1997;657-661.
130. Wemmie J.A., Moye-Rowley W.S. Mutational analysis of the Saccharomyces cerevisiae ATP-binding cassette transporter protein Ycf1p. Mol. Microbiol. 25:1997;683-694.
131. Wemmie J.A., Szczypka M.S., Thiele D.J., Moye-Rowley W.S. Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J. Biol. Chem. 269:1994;32592-32597.
132. Wemmie J.A., Wu A.L., Harshman K.D., Parker C.S., Moye-Rowley W.S. Transcriptional activation mediated by the yeast AP-1 protein is required for normal cadmium tolerance. J. Biol. Chem. 269:1994;14690-14697.
133. Wendler F., Bergler H., Prutej K., Jungwirth H., Zisser G., et al. Diazaborine resistance in the yeast Saccharomyces cerevisiae reveals a link between YAP1 and the pleiotropic drug resistance genes PDR1 and PDR3. J. Biol. Chem. 272:1997;27091-27098.
134. White T.C. 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. Antimicrob. Agents Chemother. 41:1997;1482-1487.
135. Wolfger H., Mahé Y., Parle-McDermott A., Delahodde A., Kuchler K. The yeast ATP-binding cassette (ABC) protein genes PDR10 and PDR15 are novel targets for the Pdr1 and Pdr3 transcriptional regulators. FEBS Lett. 418:1997;269-274.
136. Wu A., Wemmie J.A., Edgington N.P., Goebl M., Guevara J.L., et al. Yeast bZip proteins mediate pleiotropic drug and metal resistance. J. Biol. Chem. 268:1993;18850-18858.
137. Yan C., Lee L.H., Davis L.I. Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J. 17:1998;7416-7429.