Zinc pyrithione inhibits yeast growth through copper influx and inactivation of iron-sulfur proteins

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 12, 2011, Pages 5753-5760

  Reeder, Nancy L ^a   Kaplan, Jerry ^b   Xu, Jun ^a   Youngquist, R Scott ^a   Wallace, Jared ^b   Hu, Ping ^a   Juhlin, Kenton D ^a   Schwartz, James R ^a   Grant, Raymond A ^a   Fieno, Angela ^a   Nemeth, Suzanne ^a   Reichling, Tim ^a   Tiesman, Jay P ^a   Mills, Tim ^a   Steinke, Mark ^a   Wang, Shuo L ^a   Saunders, Charles W ^a  

^a PROCTER AND GAMBLE COMPANY   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; IRON SULFUR PROTEIN; PYRITHIONE ZINC;

ANTIFUNGAL ACTIVITY; ARTICLE; ATOMIC EMISSION SPECTROMETRY; CELL LEVEL; CONTROLLED STUDY; DANDRUFF; FUNGUS GROWTH; GENETIC ASSOCIATION; GROWTH INHIBITION; INTRACELLULAR MEMBRANE; MALASSEZIA GLOBOSA; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE;

ANTIFUNGAL AGENTS; COPPER; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; IRON-SULFUR PROTEINS; MALASSEZIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGANOMETALLIC COMPOUNDS; PYRIDINES; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION;

EID: 81555201980     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00724-11     Document Type: Article

References (45)

1. 2+. Proc. Natl. Acad. Sci. U. S. A. 106:8374-8379.
2. Askwith, C., et al. 1994. The FET3 gene of S. cerevisiae encodes a multi-copper oxidase required for ferrous iron uptake. Cell 76:403-410. (Pubitemid 24046701)
3. Beinert, H., and M. C. Kennedy. 1989. Engineering of protein bound iron-sulfur clusters. A tool for the study of protein and cluster chemistry and mechanism of iron-sulfur enzymes. Eur. J. Biochem. 186:5-15. (Pubitemid 20015120)
4. Blandino, A., I. Caro, and D. Cantero. 1997. Comparative study of alcohol dehydrogenase activity in flour yeast extracts. Biotechnol. Lett. 19:651-654. (Pubitemid 27321086)
5. Chandler, C. J., and I. H. Segel. 1978. Mechanism of the antimicrobial action of pyrithione: effects on membrane transport, ATP levels, and protein synthesis. Antimicrob. Agents Chemother. 14:60-68. (Pubitemid 8370708)
6. Chen, T. A., and P. B. Hill. 2005. The biology of Malassezia organisms and their ability to induce immune responses and skin disease. Vet. Dermatol. 16:4-26.
7. Chillappagari, S., et al. 2010. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J. Bacteriol. 192:2512-2524.
8. Davis-Kaplan, S. R., C. C. Askwith, A. C. Bengtzen, D. Radisky, and J. Kaplan. 1998. Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p: an unexpected role for intracellular chloride channels. Proc. Natl. Acad. Sci. U. S. A. 95:13641-13645. (Pubitemid 28523025)
9. DeAngelis, Y. M., et al. 2007. Isolation and expression of a Malassezia globosa lipase gene, LIP1. J. Investig. Dermatol. 127:2138-2146.
10. De Freitas, J. M., A. Liba, R. Meneghini, J. S. Valentine, and E. B. Gralla. 2000. Yeast lacking Cu-Zn superoxide dismutase show altered iron homeostasis. Role of oxidative stress in iron metabolism. J. Biol. Chem. 275:11645-11649. (Pubitemid 30237724)
11. Ermolayeva, E., and D. Sanders. 1995. Mechanism of pyrithione-induced membrane depolarization in Neurospora crassa. Appl. Environ. Microbiol. 61:3385-3390.
12. Felice, M. R., et al. 2005. Post-transcriptional regulation of the yeast high affinity iron transport system. J. Biol. Chem. 280:22181-22190. (Pubitemid 40827874)
13. Gaxiola, R. A., D. S. Yuan, R. D. Klausner, and G. R. Fink. 1998. The yeast CLC chloride channel functions in cation homeostasis. Proc. Natl. Acad. Sci. U. S. A. 95:4046-4050. (Pubitemid 28173251)
14. Gelling, C., I. W. Dawes, N. Richhardt, R. Lill, and U. Muhlenhoff. 2008. Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes. Mol. Cell. Biol. 28:1851-1861.
15. Gemmer, C. M., Y. M. DeAngelis, B. Theelen, T. Boekhout, and T. L. Dawson, Jr. 2002. Fast, noninvasive method for molecular detection and differentiation of Malassezia yeast species on human skin and application of the method to dandruff microbiology. J. Clin. Microbiol. 40:3350-3357. (Pubitemid 34977453)
16. Gross, C., M. Kelleher, V. R. Iyer, P. O. Brown, and D. R. Winge. 2000. Identification of the copper regulon in Saccharomyces cerevisiae by DNA microarrays. J. Biol. Chem. 275:32310-32316.
17. Hollander, M., and D. A. Wolfe. 1999. Nonparametric statistical methods, 2nd ed. John Wiley & Sons, New York, NY.
18. Krenn, B. M., et al. 2009. Antiviral activity of the zinc ionophores pyrithione and hinokitiol against picornavirus infections. J. Virol. 83:58-64.
19. Kumánovics, A., et al. 2008. Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J. Biol. Chem. 283:10276-10286.
20. Li, L., and J. Kaplan. 2004. A mitochondrial-vacuolar signaling pathway in yeast that affects iron and copper metabolism. J. Biol. Chem. 279:33653-33661. (Pubitemid 39063015)
21. Lill, R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460:831-838.
22. Lin, H., et al. 2008. A single amino acid change in the yeast vacuolar metal transporters ZRC1 and COT1 alters their substrate specificity. J. Biol. Chem. 283:33865-33873.
23. Lynch, S. M., and B. Frei. 1995. Reduction of copper, but not iron, by human low density lipoprotein (LDL). Implications for metal ion-dependent oxidative modification of LDL. J. Biol. Chem. 270:5158-5163.
24. MacDiarmid, C. W., L. A. Gaither, and D. Eide. 2000. Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J. 19: 2845-2855. (Pubitemid 30386757)
25. MacDiarmid, C. W., M. A. Milanick, and D. J. Eide. 2002. Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae. J. Biol. Chem. 277:39187-39194. (Pubitemid 35190887)
26. Macomber, L., and J. A. Imlay. 2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U. S. A. 106:8344-8349.
27. Magda, D., et al. 2008. Synthesis and anticancer properties of water-soluble zinc ionophores. Cancer Res. 68:5318-5325.
28. Pagani, M. A., A. Casamayor, R. Serrano, S. Atrian, and J. Arino. 2007. Disruption of iron homeostasis in Saccharomyces cerevisiae by high zinc levels: a genome-wide study. Mol. Microbiol. 65:521-537. (Pubitemid 47052732)
29. Peña, M. M. O., K. A. Koch, and D. J. Thiele. 1998. Dynamic regulation of copper uptake and detoxification genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:2514-2523. (Pubitemid 28183421)
30. Pierik, A. J., D. J. Netz, and R. Lill. 2009. Analysis of iron-sulfur protein maturation in eukaryotes. Nat. Protoc. 4:753-766.
31. Pierrel, F., P. A. Cobine, and D. R. Winge. 2007. Metal Ion availability in mitochondria. Biometals 20:675-682. (Pubitemid 46776567)
32. Rae, T. D., P. J. Schmidt, R. A. Pufahl, V. C. Culotta, and T. V. O'Halloran. 1999. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284:805-808. (Pubitemid 29291346)
33. Ramsay, L. M., and G. M. Gadd. 1997. Mutants of Saccharomyces cerevisiae defective in vacuolar function confirm a role for the vacuole in toxic metal ion detoxification. FEMS Microbiol. Lett. 152:293-298. (Pubitemid 27305833)
34. Reisch, A. S., and O. Elpeleg. 2007. Biochemical assays for mitochondrial activity: assays of TCA cycle enzymes and PDHc. Methods Cell Biol. 80: 199-222.
35. Roon, R. J., H. L. Even, and F. Larimore. 1974. Glutamate synthase: properties of the reduced nicotinamide adenine dinucleotide-dependent enzyme from Saccharomyces cerevisiae. J. Bacteriol. 118:89-95.
36. Schwartz, J. R., C. W. Cardin, and T. L. Dawson. 2004. Dandruff and seborrheic dermatitis, p. 259-272. In R. Baran and H. I. Maibach (ed.), Textbook of cosmetic dermatology. Martin Dunitz, Ltd., London, United Kingdom.
37. Thomas, K. V. 1999. Determination of the antifouling agent zinc pyrithione in water samples by copper chelate formation and high-performance liquid chromatography-atmospheric pressure chemical ionisation mass spectrometry. J. Chromatogr. A 833:105-109. (Pubitemid 29076639)
38. Tuttle, M. S., D. Radisky, L. Li, and J. Kaplan. 2003. A dominant allele of PDR1 alters transition metal resistance in yeast. J. Biol. Chem. 278:1273-1280. (Pubitemid 36790811)
39. van Bakel, H., E. Strengman, C. Wijmenga, and F. C. Holstege. 2005. Gene expression profiling and phenotype analyses of S. cerevisiae in response to changing copper reveals six genes with new roles in copper and iron metabolism. Physiol. Genomics 22:356-367. (Pubitemid 41356367)
40. Watts, R. N., C. Hawkins, P. Ponka, and D. R. Richardson. 2006. Nitrogen monoxide (NO)-mediated iron release from cells is linked to NO-induced glutathione efflux via multidrug resistance-associated protein 1. Proc. Natl. Acad. Sci. U. S. A. 103:7670-7675.
41. Wolschendorf, F., et al. 2011. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 108:1621-1626.
42. Xu, J., et al. 2007. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc. Natl. Acad. Sci. U. S. A. 104:18730-18735. (Pubitemid 350210765)
43. Yasokawa, D., et al. 2010. DNA microarray analysis suggests that zinc pyrithione causes iron starvation to the yeast Saccharomyces cerevisiae. J. Biosci. Bioeng. 109:479-486.
44. Yasokawa, D., et al. 2008. Mechanisms of copper toxicity in Saccharomyces cerevisiae determined by microarray analysis. Environ. Toxicol. 23:599-606.
45. Zhao, H., et al. 1998. Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J. Biol. Chem. 273:28713-28720. (Pubitemid 28507558)