Pdr5-mediated multidrug resistance requires the CPY-vacuolar sorting protein Vps3: Are xenobiotic compounds routed from the vacuole to plasma membrane transporters for efflux?

Molecular Genetics and Genomics

Volumn 279, Issue 6, 2008, Pages 573-583

  Rutledge, Robert M ^a   Ghislain, Michel ^b   Mullins, J Michael ^a   De Thozée, Cedric Pety ^b   Golin, John ^a  

^a CATHOLIC UNIVERSITY OF AMERICA   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Cycloheximide resistance; Multidrug resistance; Pdr5; Vacuolar sorting proteins; Vps3

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; CARBOXYPEPTIDASE C; CLOTRIMAZOLE; CYCLOHEXIMIDE; IMIDAZOLE DERIVATIVE; PROTEIN PDR5; RHODAMINE 6G; SACCHAROMYCES CEREVISIAE PROTEIN; SULFOMETURON METHYL; TRITYLIMIDAZOLE; VACUOLAR SORTING PROTEIN 3; XENOBIOTIC AGENT;

ARTICLE; CELL FRACTIONATION; CELL MEMBRANE TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE MUTATION; MEMBRANE VESICLE; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STRAIN DIFFERENCE;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CLOTRIMAZOLE; CYCLOHEXIMIDE; DRUG RESISTANCE, MULTIPLE, FUNGAL; GENE DELETION; PHENOTYPE; RHODAMINES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSPORT VESICLES; VACUOLES; VESICULAR TRANSPORT PROTEINS; XENOBIOTICS;

SACCHAROMYCES CEREVISIAE;

EID: 44149122152     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-008-0334-5     Document Type: Article

References (32)

1. Boeke JD, Fink GR (1984) A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast. Mol Gen Genet 197:345-346
2. Brown JD (2004) Protein trafficking. In: Dickinson JR, Schweizer M (eds) The metabolism and molecular physiology of Saccharomyces cerevisiae, 2nd edn. CRC Press, Boca Raton
3. Burd CG, Mustol PA, Schu PV, Emr SD (1996) A yeast protein related to mammalian Ras-binding protein is required for localization of vacuolar proteins. Mol Cell Biol 16:2369-2377
4. +-ATPase. J Biol Chem 268:21895-21900
5. Cui Z, Shiraki T, Hirata D, Miyakawa T (1998) Yeast gene YRR1, which is required for resistance to 4-nitroquinoline N-oxide, mediates transcriptional activation of the multidrug resistance transporter SNQ2. Mol Microbiol 29(5):1307-1315
6. Decottignies A, Kolaczkowski M, Balzi E, Goffeau A (1994) Solubilization and characterization of the overexpressed Pdr5 multidrug-resistance nucleotide triphosphatase of yeast. J Biol Chem 269:12797-12803
7. Decottignies A, Owsianik G, Ghislain M (1999) Casein kinase I-dependent phosphorylation and stability of the yeast multidrug transporter Pdr5p. J Biol Chem 274:37139-37146
8. Gietz RD, Woods RA (1998) Transformation of yeast by the lithium acetate/single-stranded carrier DNA/PEG method. In: Brown A.J.P. Tuite M.F. (eds) Methods in microbiology vol 26: yeast gene analysis, Academic Press, San Diego
9. Golin J, Ambudkar SV, Gottesman MM, Habib AD, Sezepanski J, Ziccardi W, May L (2003) Studies of novel Pdr5p substrates demonstrate a strong size dependence for xenobiotic efflux. J Biol Chem 278(8):5963-5969
10. Golin J, Kon ZN, Wu CP, Martello J, Hanson L, Supernavage S, Ambudkar SV, Sauna ZE (2007) Complete inhibition of the Pdr5p multidrug efflux pump ATPase by its transport substrate clotrimazole suggests that GTP as well as ATP may be used as an energy source. Biochem 46(45):13109-13119
11. Hanson L, May L, Tuma P, Keeven J, Mehl P, Ferenz M, Ambudkar SV, Golin J (2005) The role of hydrogen bond acceptor groups in the interaction of substrates with Pdr5p, a major yeast drug transporter. Biochem 44(28):9703-9713
12. Hellauer K, Akache BS, MacPherson E, Sirard E, Turcotte B (2002) Zinc cluster protein Rdr1p is a transcriptional repressor of the PDR5 gene encoding a multidrug transporter. J Biol Chem 277(20):17671-17676
13. Katzmann DP, Burnett P, 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
14. Keeven J, Ko D, Shallom J, Uccellini B, Golin J (2002) PDR2-mediated resistance to translational inhibitors requires the UBP6 product. Curr Genet 41(1):11-19
15. Kihara A, Noda T, Ishihara N, Ohsumi Y (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152(3):519-530
16. Klionsky DJ (2005) The molecular machinery of autophagy: unanswered questions. J Cell Sci 118:7-18
17. Kolaczkowski M, van der Rest M, Cybularz-Kolaczkowski A, Soumillon JP, Konings WN, Goffeau A (1996) Anticancer drugs, ionic peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J Biol Chem 271:31543-31548
18. Kumar A, Cheung KH, Ross-Macdonald P, Coelho PSR, Miller P, Snyder M (2000) TRIPLES: a database of gene function in S. cerevisiae. Nucleic Acids Res 28:81-84
19. Meyers S, Schauer W, Balzi E, Wagner M, Goffeau A, Golin J (1992) Interaction of the yeast pleiotropic drug resistance genes-PDR1 and PDR5. Curr Genet 21:431-436
20. Ouar Z, Bens M, Vignes C, Paulais M, Pringel C, Fleury J, Cluzeaud F, Lacave R, Vandewalle A (2003) Inhibitors of vacuolar H+ ATPase impair the preferential accumulation of daunomycin in lysosomes and reverse the resistance to anthracyclines in drug-resistant epithelial cells. Biochem J 370:185-193
21. Parsons AB, Brost RL, Ding, Li Z, Zhang C, Sheikh B, Brown GW, Kane PM, Hughes TR, Boone C (2004) Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat Biotech 22(1):62-69
22. Pelham HRB (2002) Insights from yeast endosomes. Curr Opin Cell Biol 14:454-462
23. Pety de Thozée C, Cronin S, Goj A, Golin J, Ghislain M (2007) Subcellular trafficking of the yeast-plasma membrane ABC transporter Pdr5 is impaired by a mutation in the N-terminal nucleotide binding fold. Mol Microbiol 63:811-825
24. Piper RC, Bryant NJ, Stevens TH (1997) The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway. J Cell Biol 138(3):531-545
25. Raymond CK, O'Hara PJ, Eichinger G, Rothman J, Stevens TH (1990) Molecular analysis of the yeast VPS3 gene and the role of its product in vacuolar protein sorting and vacuolar segregation during the cell cycle. J Cell Biol 111:877-892
26. Rogers B, Decottignies A, Kolaczkowski M, Caravajal E, Moye-Rowley WS, Goffeau A (2001) The pleiotropic drug ABC transporters from Saccharomyces cerevisiae. J Mol Microbiol Biotech 3:207-214
27. +-ATPase are deficient in two yeast mutants that fail to sort vacuolar proteins. J Cell Biol 109:93-100
28. Servos J, Haase E, Brendel M (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 Genom 236(2/3):214-218
29. Shukla S, Sani P, Jha S, Ambukar SV, Prasad R (2003) Functional characterization of Candida albicans ABC transporter Cdr1p. Eukary Cell 2:1361-1375
30. Stepp JD, Huang K, Lemmon SK (1997) The yeast adaptor protein complex, AP-3, is essential for efficient delivery of alkaline phosphatase by the alternative pathway to the vacuole. J Cell Biol 139(7):1761-1774
31. Wach A, Brachat A, Rebischung C, Steiner S, Pokorni K, te Heesen S, Philippsen P (1998) PCR-based gene targeting in Saccharomyces cerevisiae. In: Brown AJP, Tuite MF (eds) Methods in microbiology vol 26: yeast gene analysis, Academic Press, San Diego
32. Wurmser AE, Emr SD (2002) Novel PtdIns(3) P-binding protein Etf1 functions as an effector of the Vps34 PtdIns 3-kinase in autophagy. J Cell Sci 158(4):761-772