The Saccharomyces cerevisiae weak-acid-inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy- dependent mechanism

Journal of Bacteriology

Volumn 181, Issue 15, 1999, Pages 4644-4652

  Holyoak, Caroline D ^a   Bracey, Danielle ^a   Piper, Peter W ^b   Kuchler, Karl ^c   Coote, Peter J ^a  

^a UNILEVER RESEARCH   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c University and Biocenter of Vienna   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ACETIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANION; BENZOIC ACID; BUTYRIC ACID; CARBOXYLIC ACID; DECANOIC ACID; FLUORESCEIN; FORMIC ACID; HEPTANOIC ACID DERIVATIVE; HEXANOIC ACID; NONANOIC ACID; OCTANOIC ACID; PDR 12; PROPIONIC ACID; SORBIC ACID; UNCLASSIFIED DRUG; VALERIC ACID; VANADIC ACID;

ARTICLE; BINDING SITE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FUNGUS GROWTH; GROWTH INHIBITION; GROWTH RATE; ION TRANSPORT; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INDUCTION; SACCHAROMYCES CEREVISIAE;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0032766243     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.15.4644-4652.1999     Document Type: Article

References (42)

1. Balzi, E., and A. Goffeau. 1994. Genetics and biochemistry of yeast multidrug resistance. Biochim. Biophys. Acta 1187:152-162.
2. Bissinger, P. H., and K. Kuchler. 1994. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:4180-4186.
3. Bolhuis, H., H. W. van Veen, D. Molenaar, B. Poolman, A. J. M. Driessen, and W. N. Konings. 1996. Multidrug resistance in Lactococcus lactis: evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J. 15:4239-4245.
4. Bolhuis, H., H. W. van Veen, B. Poolman, A. J. M. Driessen, and W. N. Konings. 1997. Mechanisms of multidrug transporters. FEMS Microbiol. Rev. 21:55-84.
5. Breeuwer, P., J.-L. Drocourt, F. M. Rombouts, and T. Abee. 1994. Energy-dependent, carrier-mediated extrusion of carboxyfluorescein from Saccharomyces cerevisiae allows rapid assessment of cell viability by flow cytometry. Appl. Environ. Microbiol. 60:1467-1472.
6. Breeuwer, P., J.-L. Drocourt, N. Bunschoten, M. H. Zwietering, F. M. Rombouts, and T. Abee. 1995. Characterization of uptake and hydrolysis of fluorescein diacetate and carboxyfluorescein diacetate by intracellular esterases in Saccharomyces cerevisiae, which result in accumulation of fluorescent product. Appl. Environ. Microbiol. 61:1614-1619.
7. +-ATPase. J. Microbiol. Methods 31:113-125.
8. Bracey, D., C. D. Holyoak, and P. J. Coote. 1998. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: is growth inhibition dependent on reduced intracellular pH? J. Appl. Microbiol. 85:1056-1066.
9. +-ATPase is essential for the regulation of this enzyme by heat shock protein Hsp30, but not for stress activation. FEBS Lett. 418:123-126.
10. Chapman, A. G., L. Fall, and D. E. Atkinson. 1971. Adenylate energy charge in Escherichia coli during growth and starvation. J. Bacteriol. 108:1072-1086.
11. Cherrington, C. A., M. Hinton, G. C. Mead, and I. Chopra. 1991. Organic acids: chemistry, antibacterial activity and practical applications. Adv. Microb. Physiol. 32:87-108.
12. Cole, M. B., and M. H. J. Keenan. 1987. Effects of weak acids and external pH on the intracellular pH of Zygosaccharomyces bailii, and its implications in weak-acid resistance. Yeast 3:23-32.
13. Deak, T. 1991. Food borne yeasts. Adv. Appl. Microbiol. 36:179-278.
14. Decottignies, A., M. Kolaczkowski, E. Balzi, and A. Goffeau. 1994. Solubilisation and characterisation of the overexpressed PDR5 multidrug resistance nucleotide triphosphatase of yeast. J. Biol. Chem. 269:12797-12803.
15. 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.
16. Diez-Gonzalez, F., and J. B. Russell. 1997. Effects of carbonylcyanide-m-chlorophenylhydrazone (CCCP) and acetate on Escherichia coli O157:H7 and K-12: uncoupling versus anion accumulation. FEMS Microbiol. Lett. 151:71-76.
17. Eklund, T. 1985. The effect of sorbic acid and esters of p-hydroxybenzoic acid on the protonmotive force in Escherichia coli membrane vesicles. J. Gen. Microbiol. 131:73-76.
18. Fleet, G. 1992. Spoilage yeasts. Crit. Rev. Biotechnol. 12:1-44.
19. Freese, E., C. W. Sheu, and E. Galliers. 1973. Function of lipophilic acids as antimicrobial food additives. Nature 241:321-325.
20. Henriques, M., C. Quintas, and M. C. Loureiro-Dias. 1997. Extrusion of benzoic acid in Saccharomyces cerevisiae by an energy-dependent mechanism. Microbiology 143:1877-1833.
21. Higgins, C. F. 1994. Flip-flop: the transmembrane translocation of lipids. Cell 79:393-395.
22. +-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl. Environ. Microbiol. 62:3158-3164.
23. Kaiser, C., S. Michaelis, and A. Mitchell. 1994. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
24. Kolaczkowski, M., M. van der Rest, A. Cybularz-Kolaczkowska, J.-P. Soumillion, W. N. Konings, and A. Goffeau. 1996. Anticancer drugs, ionophoric peptides, and steroid as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem. 271:31543-31548.
25. Krebs, H. A., D. Wiggins, S. Sols, and F. Bedoya. 1983. Studies on the mechanism of the antifungal action of benzoate. Biochem. J. 214:657-663.
26. Leo, A., C. Hansch, and D. Elkins. 1971. Partition coefficients and their uses. Chem. Rev. 71:525-616.
27. Loureiro-Dias, M. C. 1998. Effects of and resistance to weak acids in spoilage yeasts, abstr. L2.4, p. 81. In Abstracts of the 19th International Specialised Symposium on Yeasts 1998: yeast in the production and spoilage of food and beverages. University of Minho, Braga, Portugal.
28. Mahe, Y., Y. Lemoine, and K. Kuchler. 1996. The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J. Biol. Chem. 271:25167-25172.
29. +-ATPase. Cell Stress Chaperones 2:12-24.
30. Piper, P. W., Y. Mahe, S. Thompson, R. Pandjaitan, C. Holyoak, R. Egner, M. Muhlbauer, P. Coote, and K. Kuchler. 1998. The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J. 17:4257-4265.
31. Ruetz, S., M. Raymond, and P. Gros. 1993. Functional expression of P-glycoprotein encoded by the mouse mdr3 gene in yeast cells. Proc. Natl. Acad. Sci. USA 90:11588-11592.
32. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell 77:1071-1081.
33. Russell, J. B. 1992. Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J. Appl. Bacteriol. 73:363-370.
34. Salmond, C. V., R. G. Kroll, and I. R. Booth. 1984. The effect of food preservatives on pH homeostasis in Escherichia coli. J. Gen. Microbiol. 130:2845-2850.
35. Serrano, R. 1991. Transport across yeast vacuolar and plasma membranes, p. 523-585. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces: genome dynamics, protein synthesis, and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
36. 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.
37. Stevens, S., and J.-H. S. Hofmeyr. 1993. Effects of ethanol, octanoic and decanoic acids on fermentation and the passive influx of protons through the plasma membrane of Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 38:656-663.
38. Thevelein, J. M., M. Buellens, F. Honshoven, et al. 1987. Regulation of the cAMP level in the yeast Saccharomyces cerevisiae: the glucose-induced cAMP signal is not mediated by a transient drop in the intracellular pH. J. Gen. Microbiol. 133:2197-2205.
39. Venduyn, C., E. Postma, W. A. Scheffers, and J. P. van Dijken. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501-517.
40. Viegas, C. A., and I. Sa-Correia. 1991. Activation of plasma membrane ATPase of Saccharomyces cerevisiae by octanoic acid. J. Gen. Microbiol. 137:645-651.
41. +-ATPase in the plasma membrane of Saccharomyces cerevisiae is activated during growth latency in octanoic acid-supplemented medium accompanying the decrease in intracellular pH and cell viability. Appl. Environ. Microbiol. 64:779-783.
42. Warth, A. D. 1977. Mechanism of resistance of Saccharomyces bailii to benzoic, sorbic and other weak acids used as food preservatives. J. Appl. Bacteriol. 43:215-230.