Multiple-drug-resistance phenomenon in the yeast Saccharomyces cerevisiae: Involvement of two hexose transporters

Molecular and Cellular Biology

Volumn 17, Issue 9, 1997, Pages 5453-5460

  Nourani, Amine ^a   Wesolowski Louvel, Micheline ^b   Delaveau, Thierry ^a   Jacq, Claude ^a   Delahodde, Agnès ^a,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; ABC TRANSPORTER; CYCLOHEXIMIDE; GALACTOSE; GENE PRODUCT; GLUCOSE;

ARTICLE; DRUG SENSITIVITY; FUNGUS MUTANT; GENE EXPRESSION; GENETIC TRANSCRIPTION; KLUYVEROMYCES; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; YEAST;

FUNGI; KLUYVEROMYCES; KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

EID: 0030837532     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.9.5453     Document Type: Article

References (46)

1. Andre, B. 1995. An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575-1611.
2. Balzi, E., W. Chen, S. Ulaszewski, E. Capieaux, and A. Goffeau. 1987. The multidrug resistance gene PDR1 from Saccharomyces cerevisiae. J. Biol. Chem. 262:16871-16879.
3. Balzi, E., and A. Goffeau. 1994. Genetics and biochemistry of yeast multidrug resistance. Biochim. Biophys. Acta 1187:152-162.
4. Balzi, E., and A. Goffeau. 1995. Yeast multidrug resistance: the PDR network. J. Bioenerg. Biomemhr. 27:71-76.
5. Balzi, E., M. Wang, S. Leterme, L. Van Dyck, and A. Goffeau. 1994. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:2206-2214.
6. Banroques, J., A. Delahodde, and C. Jacq. 1986. A mitochondrial RNA-maturase gene control mitochondrial mRNA splicing. Cell 46:837-844.
7. Bissinger, P. H., and K. Kuchler. 1994. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. J. Biol. Chem. 269:4180-4186.
8. Bisson, L. F., and D. M. Coons. 1993. Yeast sugar transporters. Crit. Rev. Biochem. Mol. Biol. 28:259-308.
9. Bonneaud, N., O. Ozier-Kalogeropoulos, G. Li, M. Labouesse, L. Minvielle-Sebastia, and F. Lacroute. 1991. A family of low copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7:609-615.
10. Chardin, P., J. H. Camonis, N. W. Gale, L. Van Aelst, J. Schlessinger, M. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to Grb2. Science 260:1338-1343.
11. Conklin, D. S., C. Kung, and M. R. Culbertson. 1993. The COT2 gene is required for glucose-dependent divalent cation transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:2041-2049.
12. Dang, V. D., M. Valens, M. Bolotin-Fukuhara, and B. Daignan-Fornier. 1994. A genetic screen to isolate genes regulated by the yeast CCAAT-box binding protein Hap2p. Yeast 10:1273-1283.
13. Decottignies, A., and A. Goffeau. 1997. Complete inventory of the yeast ABC proteins. Nat. Genet. 15:137-145.
14. Decottignies, A., L. Lambert, P. Catty, H. Degand, E. A. Epping, W. S. Moye-Rowley, E. Balzi, and A. Goffeau. 1995. Identification and characterization of SNQ2, a new multidrug ATP binding cassette transporter of the yeast plasma membrane. J. Biol. Chem. 270:18150-18157.
15. Delahodde, A., T. Delaveau, and C. Jacq. 1995. Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol. Cell. Biol. 15:4043-4051.
16. Delaveau, T., A. Delahodde, E. Carvajal, J. Subik, and C. Jacq. 1994. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244:501-511.
17. Dexter, D., S. Moye-Rowley, S. Wu, and J. Golin. 1994. Mutations in yeast PDR3, PDR4, PDR7 and PDR9 pleiotropic (multiple) drug resistance loci affect the transcript level of an ATP binding cassette transporter encoding gene, PDR5. Genetics 136:505-515.
18. Endicott, J. A., and V. Ling. 1989. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu. Rev. Biochem. 58:137-171.
19. Gartner, J., H. Moser, and D. Valle. 1992. Mutations in the 70K peroxisomal membrane protein gene in Zellweger syndrome. Nat. Genet. 1:16-23.
20. Gould, G. W., and G. L. Bell. 1990. Facilitative glucose transporters: an expanding family. Trends Biochem. Sci. 15:18-23.
21. Henderson, P. J. F. 1990. The homologous glucose transport proteins of prokaryotes and eukaryotes. Res. Microbiol. 141:316.
22. Katzmann, D. J., P. E. Burnett, J. Golin, Y. Mahé, and W. S. Moye-Rowley. 1994. Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14:4653-4661.
23. Katzmann, D. J., T. C. Hallstrom, Y. Mahé, and W. S. Moye-Rowley. 1996. Multiple Pdr1p/Pdr3p binding sites are essential for normal expression of the ATP binding cassette transporter protein-encoding gene PDR5. J. Biol. Chem. 271:23049-23054.
24. Katzmann, D. J., T. C. Hallstrom, M. Voet, W. Wysock, J. Golin, G. Volckaert, and W. S. Moye-Rowley. 1995. Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6875-6883.
25. Ko, C. H., H. Liang, and R. F. Gaber. 1993. Roles of multiple glucose transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:638-648.
26. Kruckeberg, A. L. 1996. The hexose transporter family of Saccharomyces cerevisiae. Arch. Microbiol. 166:283-292.
27. Leonard, P. J., P. K. Rathod, and J. Golin. 1994. Loss of function mutation in the yeast multiple drug resistance gene PDR5 causes a reduction in chloramphenicol efflux. Antimicrob. Agents Chemother. 38:2492-2494.
28. Mahé, Y., A. Parle-McDermott, A. Nourani, A. Delahodde, A. Lamprecht, and K. Kuchler. 1996. The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: a novel target for the transcription factors Pdr1 and Pdr3. Mol. Microbiol. 20:109-117.
29. Miller, J. H. 1972. Experiments in molecular genetics, p. 352-355. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
30. Mosser, J., A. M. Douar, C. O. Sarde, P. Hioschis, R. Feil, H. Moser, A. M. Poustka, J. L. Mandel, and P. Aubourg. 1993. Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361:726-730.
31. Nehlin, J. O., M. Carlberg, and H. Ronne. 1989. Yeast galactose permease is related to yeast and mammalian glucose transporters. Gene 85:313-319.
32. Nelissen, B., P. Mordant, J. L. Jonniaux, R. De Wachter, and A. Goffeau. 1995. Phylogenetic classification of the major superfamily of membrane transport facilitators, as deduced from yeast genome sequencing. FEBS Lett. 377:232-236.
33. Nourani, A., D. Papajova, A. Delahodde, C. Jacq, and J. Subik. 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., in press.
34. Nourani, A., et al. Unpublished data.
35. Özcan, S., and M. Johnston. 1995. Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose. Mol. Cell. Biol. 15:1564-1572.
36. Prior, C., H. Fukuhara, J. Blaisonneau, and M. Wésolowski-Louvel. 1993. Low-affinity glucose carrier gene LGT1 of Saccharomyces cerevisiae, a homolog of Kluyveromyces lactis RAG1 gene. Yeast 9:1373-1377.
37. Reifenberger, E., K. Freidel, and M. Ciriacy. 1995. Identification of novel HXT genes in Saccharomyces cerevisiae reveals the impact of individual hexose transporters on glycolytic flux. Mol. Microbiol. 16:157-167.
38. Riordan, J. R., J. M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, and J. L. Chou. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073.
39. Schmitt, M. E., T. A. Brown, and B. L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 19:3091-3092.
40. Servos, J., E. Haase, and M. Brendel. 1993. 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. 236:214-218.
41. Tschopp, J. F., S. D. Emr, C. Field, and R. Schekman. 1986. GAL2 codes for a membrane-bound subunit of the galactose permease in Saccharomyces cerevisiae. J. Bacteriol. 166:313-318.
42. Vera, J. C., G. R. Castillo, and O. M. Rosen. 1991. A possible role for a mammalian facilitative hexose transporter in the development of resistance to drugs. Mol. Cell. Biol. 11:3407-3418.
43. Walsh, M. C., H. P. Smits, M. Scholte, and K. van Dam. 1994. Affinity of glucose transport in Saccharomyces cerevisiae is modulated during growth on glucose. J. Bacteriol. 176:953-958.
44. Wertheimer, E., S. Sasson, E. Cerasi, and Y. Ben-Neriah. 1991. The ubiquitous glucose transporter GLUT-1 belongs to the glucose-regulated protein family of stress-inducible proteins. Proc. Natl. Acad. Sci. USA 88:2525-2529.
45. Wésolowski-Louvel, M., P. Goffrini, I. Ferrero, and H. Fukuhara. 1992. Glucose transport in the yeast Kluyveromyces lactis. I. Properties of an inducible low-affinity glucose transporter gene. Mol. Gen. Genet. 33:89-96.
46. Yamamoto, T., Y. Seino, H. Fukumoto, G. Koh, H. Yano, N. Inagaki, Y. Yamada, K. Inoue, T. Manabe, and H. Imura. 1990. Over-expression of facilitative glucose transporter genes in human cancer. Biochem. Biophys. Res. Commun. 170:223-230.