Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-23T23:10:24.446Z Has data issue: false hasContentIssue false

10 - Metal stress and the single yeast cell: Berkeley Award Lecture

from IV - Fungal bioremediation

Published online by Cambridge University Press:  05 October 2013

By
S. V. Avery
Edited by
G. D. Robson ,
Pieter van West  and
Geoffrey Gadd
S. V. Avery
Affiliation:
School of Biology University of Nottingham University Park Nottingham NG7 2RD UK
G. D. Robson
Affiliation:
University of Manchester
Pieter van West
Affiliation:
University of Aberdeen
Geoffrey Gadd
Affiliation:
University of Dundee
Get access

Summary

Introduction

Overview

This paper explores the mechanisms of metal toxicity towards cells, specifically some advances being made in this area through work with the unicellular fungus, Saccharomyces cerevisiae. The two principal questions addressed here are:

  1. Is oxidative damage the cause of cellular metal toxicity?

  2. Why do individual cells exhibit widely differing metal resistances?

Several powerful experimental tools are unique to S. cerevisiae among eukaryotes, and are being exploited to help elucidate the mechanism(s) of metal toxicity. Furthermore, in conjunction with its unicellular morphology, S. cerevisiae provides an ideal system with which to explore the topical problem of cell individuality, applied here to metal toxicity. This chapter provides an overview of these fields, illustrated with key findings from the author's laboratory.

Metals in the environment and relevance to fungi

A wide range of industrial activities give rise to metal pollutants, which continue to be released into the environment at potentially harmful levels. Localized concentration of certain metals may also arise naturally. For example, toxic levels of the biologically essential metal copper are often associated with certain mineral ores as well as industrial or agricultural discharges. Cadmium is used widely in electroplating and galvanizing industries, as a colour pigment in paints and in batteries, and as a by-product of zinc and lead mining and smelting. Zinc, lead and other metals also may be released from similar types of sources.

Type
Chapter
Information
Exploitation of Fungi , pp. 161 - 186
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, J., Davey, H. M., Broadhurst, D., Heald, J. K., Rowland, J. J., Oliver, S. G. & Kell, D. B. (2003). High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nature Biotechnology, 21, 692–6.CrossRefGoogle ScholarPubMed
Assmann, S., Sigler, K. & Hofer, M. (1996). Cd2 +-induced damage to yeast plasma membrane and its alleviation by Zn2 +: studies on Schizosaccharomyces pombe cells and reconstituted plasma membrane vesicles. Archives of Microbiology, 165, 279–84.Google Scholar
Avery, S. V. (1995). Caesium accumulation by microorganisms: uptake mechanisms, cation competition, compartmentalization and toxicity. Journal of Industrial Microbiology, 14, 76–84.CrossRefGoogle ScholarPubMed
Avery, S. V. (2001). Metal toxicity in yeasts and the role of oxidative stress. Advances in Applied Microbiology, 49, 111–42.CrossRefGoogle ScholarPubMed
Avery, S. V. (2005a). Cell individuality: the bistability of competence development. Trends in Microbiology, 13, 459–62.CrossRefGoogle Scholar
Avery, S. V. (2005b). Phenotypic diversity and fungal fitness. The Mycologist, 19, 74–80.CrossRefGoogle Scholar
Avery, S. V. & Tobin, J. M. (1993). Mechanism of adsorption of hard and soft metal ions to Saccharomyces cerevisiae and influence of hard and soft anions. Applied and Environmental Microbiology, 59, 2851–6.Google ScholarPubMed
Avery, A. M. & Avery, S. V. (2001). Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. Journal of Biological Chemistry, 276, 33730–5.CrossRefGoogle ScholarPubMed
Avery, S. V., Howlett, N. G. & Radice, S. (1996). Copper toxicity towards Saccharomyces cerevisiae: dependence on plasma-membrane fatty acid composition. Applied and Environmental Microbiology, 62, 3960–6.Google ScholarPubMed
Avery, A. M., Willetts, S. A. & Avery, S. V. (2004). Genetic dissection of the phospholipid hydroperoxidase activity of yeast Gpx3 reveals its functional importance. Journal of Biological Chemistry, 279, 46652–8.CrossRefGoogle ScholarPubMed
Baryla, A., Laborde, C., Montillet, J. L., Triantaphylides, C. & Chagvardieff, P. (2000). Evaluation of lipid peroxidation as a toxicity bioassay for plants exposed to copper. Environmental Pollution, 109, 131–5.CrossRefGoogle Scholar
Basu, U., Southron, J. L., Stephens, J. L. & Taylor, G. J. (2004). Reverse genetic analysis of the glutathione metabolic pathway suggests a novel role of PHGPX and URE2 genes in aluminum resistance in Saccharomyces cerevisiae. Molecular Genetics and Genomics, 271, 627–37.CrossRefGoogle ScholarPubMed
Beckman, K. B. & Ames, B. N. (1997). Oxidative decay of DNA. Journal of Biological Chemistry, 272, 19633–66.CrossRefGoogle ScholarPubMed
Bergman, A. & Siegal, M. L. (2003). Evolutionary capacitance as a general feature of complex gene networks. Nature, 424, 549–52.CrossRefGoogle ScholarPubMed
Blake, W. J., Kaern, M., Cantor, C. R. & Collins, J. J. (2003). Noise in eukaryotic gene expression. Nature, 10, 633–7.CrossRefGoogle Scholar
Brennan, R. J. & Schiestl, R. H. (1996). Cadmium is an inducer of oxidative stress in yeast. Mutation Research – Fundamental Molecular Mechanisms of Mutagenesis, 356, 171–8.CrossRefGoogle Scholar
Cabiscol, E., Piulats, E., Echave, P., Herrero, E. & Ros, J. (2000). Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. Journal of Biological Chemistry, 275, 27393–8.Google ScholarPubMed
Cakmak, I. (2000). Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist, 146, 185–205.CrossRefGoogle Scholar
Casalino, E., Sblano, C. & Landriscina, C. (1997). Enzyme activity alteration by cadmium administration to rats – the possibility of iron involvement in lipid peroxidation. Archives of Biochemistry and Biophysics, 346, 171–9.CrossRefGoogle ScholarPubMed
Chen, C. Y., Su, Y. J., Wu, P. F. & Shyu, M. M. (2002). Nickel-induced plasma lipid peroxidation and effect of antioxidants in human blood: involvement of hydroxyl radical formation and depletion of alpha-tocopherol. Journal of Toxicology and Environmental Health, Part A, 65, 843–52.CrossRefGoogle ScholarPubMed
Chiang, K. T., Shinyashiki, M., Switzer, C. H., Valentine, J. S., Gralla, E. B., Thiele, D. J. & Fukuto, J. M. (2000). Effects of nitric oxide on the copper-responsive transcription factor Ace1 in Saccharomyces cerevisiae: cytotoxic and cytoprotective actions of nitric oxide. Archives of Biochemistry and Biophysics, 377, 296–303.CrossRefGoogle ScholarPubMed
Cooke, M. S., Evans, M. D., Dizdaroglu, M. & Lunec, J. (2003). Oxidative DNA damage: mechanisms, mutation, and disease. FASEB Journal, 17, 1195–214.CrossRefGoogle ScholarPubMed
Costa, W. M. V., Amorim, M. A., Quintanilha, A. & Moradas-Ferreira, P. (2002). Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Radical Biology and Medicine, 33, 1507–15.CrossRefGoogle ScholarPubMed
Culotta, V. C., Joh, H.-D., Lin, S.-J., Slekar, K. H. & Strain, J. (1995). A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. Journal of Biological Chemistry, 270, 29991–7.Google ScholarPubMed
Davey, H. M. & Kell, D. B. (1996). Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiological Reviews, 60, 641–96.Google ScholarPubMed
Deutschbauer, A. M., Jaramillo, D. F., Proctor, M., Kumm, J., Hillenmeyer, M. E., Davis, R. W., Nislow, C. & Giaever, G. (2005). Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics, 169, 1915–25.CrossRefGoogle Scholar
Delaunay, A., Pflieger, D., Barrault, M. B., Vinh, J. & Toledano, M. B. (2002). A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell, 111, 471–81.CrossRefGoogle ScholarPubMed
Vos, C. H. R., Bookum, W. M. Y., Vooijs, R., Schat, H. & Kok, L. J. (1993). Effects of copper on fatty acid composition and peroxidation of lipids in the roots of copper tolerant and sensitive Silene cucabalus. Plant Physiology and Biochemistry, 31, 151–8.Google Scholar
Dix, T. A. & Aikens, J. (1993). Mechanisms and biological relevance of lipid peroxidation initiation. Chemical Research in Toxicology, 6, 2–18.CrossRefGoogle ScholarPubMed
Drakulic, T., Temple, M. D., Guido, R., Jarolim, S., Breitenbach, M., Attfield, P. V. & Dawes, I. W. (2005). Involvement of oxidative stress response genes in redox homeostasis, the level of reactive oxygen species, and ageing in Saccharomyces cerevisiae. FEMS Yeast Research, 5, 1215–28.CrossRefGoogle ScholarPubMed
Dunning, J. C., Ma, Y. & Marquis, R. E. (1998). Anaerobic killing of oral streptococci by reduced, transition metal cations. Applied and Environmental Microbiology, 64, 27–33.Google ScholarPubMed
Elowitz, M. B., Levine, A. J., Siggia, E. D. & Swain, P. S. (2002). Stochastic gene expression in a single cell. Science, 297, 1183–6.CrossRefGoogle Scholar
Fortuniak, A., Zadzinski, R., Bilinski, T. & Bartosz, G. (1996). Glutathione depletion in the yeast Saccharomyces cerevisiae. Biochemistry and Molecular Biology International, 38, 901–10.Google ScholarPubMed
Fraser, H. B., Hirsh, A. E., Giaever, G., Kumm, J. & Eisen, M. B. (2004). Noise minimization in eukaryotic gene expression. PLOS Biology, 2, 834–8.CrossRefGoogle ScholarPubMed
Gadd, G. M. (1993). Interactions of fungi with toxic metals. New Phytologist, 124, 25–60.CrossRefGoogle Scholar
Gadd, G. M. (2000). Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Current Opinion in Biotechnology, 11, 271–9.CrossRefGoogle ScholarPubMed
Gadd, G. M. & Mowll, J. L. (1983). The relationship between cadmium uptake, potassium release and viability in Saccharomyces cerevisiae. FEMS Microbiology Letters, 16, 45–8.CrossRefGoogle Scholar
Galiazzo, F., Cirilio, M. R., Carri, M. T., Civitareale, P., Marcocci, L., Marmocchi, F. & Rotilio, G. (1991). Activation and induction by copper of Cu/Zn superoxide dismutase in Saccharomyces cerevisiae – presence of an inactive proenzyme in anaerobic yeast. European Journal of Biochemistry, 196, 545–9.CrossRefGoogle ScholarPubMed
Gralla, E. B. (1997). Superoxide dismutase: studies in the yeast Saccharomyces cerevisiae. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses, ed. Scandialos, J. G.. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, pp. 495–525.Google Scholar
Greco, M. A., Hrab, D. I., Magner, W. & Kosman, D. J. (1990). Cu, Zn superoxide-dismutase and copper deprivation and toxicity in Saccharomyces cerevisiae. Journal of Bacteriology, 172, 317–25.CrossRefGoogle ScholarPubMed
Halliwell, B. & Gutteridge, J. M. C. (1990). Role of free radicals and catalytic metal ions in human disease: an overview. Methods in Enzymology, 186, 1–88.CrossRefGoogle ScholarPubMed
Halliwell, B. & Gutteridge, J. M. C. (1999). Free Radicals in Biology and Medicine, 3rd edn. Oxford, UK: Oxford University Press.Google Scholar
Harris, Z. L. & Gitlin, J. D. (1996). Genetic and molecular basis for copper toxicity. American Journal of Clinical Nutrition, 63, S836–S841.CrossRefGoogle ScholarPubMed
Hepburn, D. D. D., Burney, J. M., Woski, S. A. & Vincent, J. B. (2003). The nutritional supplement chromium picolinate generates oxidative DNA damage and peroxidized lipids in vivo. Polyhedron, 22, 455–63.CrossRefGoogle Scholar
Hippeli, S. & Elstner, E. F. (1999). Transition metal ion-catalyzed oxygen activation during pathogenic processes. FEBS Letters, 443, 1–7.CrossRefGoogle ScholarPubMed
Howlett, N. G. & Avery, S. V. (1997a). Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Applied and Environmental Microbiology, 63, 2971–6.Google Scholar
Howlett, N. G. & Avery, S. V. (1997b). Relationship between cadmium sensitivity and degree of plasma membrane fatty acid unsaturation in Saccharomyces cerevisiae. Applied Microbiology and Biotechnology, 48, 539–45.CrossRefGoogle Scholar
Howlett, N. G. & Avery, S. V. (1999). Flow cytometric investigation of heterogeneous copper sensitivity in asynchronously-grown Saccharomyces cerevisiae. FEMS Microbiology Letters, 176, 379–86.CrossRefGoogle ScholarPubMed
Hughes, M. N. & Poole, R. K. (1991). Metal speciation and microbial growth – the hard (and soft) facts. Journal of General Microbiology, 137, 725–34.CrossRefGoogle Scholar
Hughes, T. R., Marton, M. J., Jones, A. R., Roberts, C. J., Stoughton, R., Armour, C. D., Bennett, H. A., Coffey, E., Dai, H. Y., He, Y. D. D., Kidd, M. J., King, A. M., Meyer, M. R., Slade, D., Lum, P. Y., Stepaniants, S. B., Shoemaker, D. D., Gachotte, D., Chakraburtty, K., Simon, J., Bard, M. & Friend, S. H. (2000). Functional discovery via a compendium of expression profiles. Cell, 102, 109–26.CrossRefGoogle Scholar
Inoue, Y., Matsuda, T., Sugiyama, K.-I., Izawa, S. & Kimura, A. (1999). Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. Journal of Biological Chemistry, 274, 27002–9.CrossRefGoogle ScholarPubMed
Jin, Y. H., Clark, A. B., Slebos, R. J. C., Al-Refai, H., Taylor, J. A., Kunkel, T. A., Resnick, M. A. & Gordenin, D. A. (2003). Cadmium is a mutagen that acts by inhibiting mismatch repair. Nature Genetics, 34, 326–9.CrossRefGoogle ScholarPubMed
Jungmann, J., Reins, H. A., Schobert, C. & Jentsch, S. (1993). Resistance to cadmium mediated by ubiquitin-dependent proteolysis. Nature, 361, 369–71.CrossRefGoogle ScholarPubMed
Kaern, M., Elston, T. C., Blake, W. J. & Collins, J. J. (2005). Stochasticity in gene expression: from theories to phenotypes. Nature Reviews Genetics, 6, 451–64.CrossRefGoogle ScholarPubMed
Kale, S. P. & Jazwinski, S. M. (1996). Differential response to UV stress and DNA damage during the yeast replicative life span. Developmental Genetics, 18, 154–60.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Karlstrom, A. R. & Levine, R. L. (1991). Copper inhibits the protease from human immunodeficiency virus-1 by both cysteine-dependent and cysteine-independent mechanisms. Proceedings of the National Academy of Sciences of the USA, 88, 5552–6.CrossRefGoogle ScholarPubMed
Kasprzak, K. S. (2002). Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radical Biology and Medicine, 32, 958–67.CrossRefGoogle ScholarPubMed
Kryukov, G. V., Kumar, R. A., Koc, A., Sun, Z. H. & Gladyshev, V. N. (2002). Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proceedings of the National Academy of Sciences of the USA, 99, 4245–50.CrossRefGoogle ScholarPubMed
Larison, J. R., Likens, G. E., Fitzpatrick, J. W. & Crock, J. G. (2000). Cadmium toxicity among wildlife in the Colorado Rocky Mountains. Nature, 406, 181–3.CrossRefGoogle ScholarPubMed
Lee, J. K., Kim, J. M., Kim, S. W., Nam, D. H., Yong, C. S. & Huh, K. (1996). Effect of copper-ion damage in superoxide dismutase-deficient Saccharomyces cerevisiae. Archives of Pharmaceutical Research, 19, 178–82.CrossRefGoogle Scholar
Lehmann, M., Reidel, K., Adler, K. & Kunze, G. (2000). Amperometric measurement of copper ions with a deputy substrate using a novel Saccharomyces cerevisiae sensor. Biosensors and Bioelectronics, 15, 211–19.CrossRefGoogle ScholarPubMed
Leonard, S. S., Bower, J. J. & Shi, X. L. (2004). Metal-induced toxicity, carcinogenesis, mechanisms and cellular responses. Molecular and Cellular Biochemistry, 255, 3–10.CrossRefGoogle ScholarPubMed
Li, Z. S., Lu, Y. P., Zhen, R. G., Szczypka, M., Thiele, D. J. & Rea, P. A. (1997). A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proceedings of the National Academy of Sciences USA, 94, 42–7.CrossRefGoogle ScholarPubMed
Lin, C.-M., Crawford, B. F. & Kosman, D. J. (1993). Distribution of Cu64 in Saccharomyces cerevisiae: cellular locale and metabolism. Journal of General Microbiology, 139, 1605–15.CrossRefGoogle Scholar
Liochev, S. I. & Fridovich, I. (1999). Superoxide and iron: partners in crime. IUBMB Life, 48, 157–61.CrossRefGoogle ScholarPubMed
Llanos, R. M. & Mercer, J. F. B. (2002). The molecular basis of copper homeostasis and copper-related disorders. DNA and Cell Biology, 21, 259–70.CrossRefGoogle ScholarPubMed
Lloyd, D. R., Phillips, D. H. & Carmichael, P. L. (1997). Generation of putative intrastrand cross-links and strand breaks in DNA by transition metal ion-mediated oxygen radical attack. Chemical Research in Toxicology, 10, 393–400.CrossRefGoogle ScholarPubMed
Lu, Y., Roe, J. A., Bender, C. J., Peisach, J., Banci, L., Bertini, I., Gralla, E. B. & Valentine, J. S. (1996). New type 2 copper-cysteinate proteins. Copper site histidine-to-cysteine mutants of yeast copper-zinc superoxide dismutase. Inorganic Chemistry, 35, 1692–700.CrossRefGoogle ScholarPubMed
Lum, P. Y., Armour, C. D., Stepaniants, S. B., Cavet, G., Wolf, M. K., Butler, J. S., Hinshaw, J. C., Garnier, P., Prestwich, G. D., Leonardson, A., Garrett-Engele, P., Rush, C. M., Bard, M., Schimmack, G., Phillips, J. W., Roberts, C. J. & Shoemaker, D. D. (2004). Discovering modes of action for therapeutic compounds using a genome-wide screen of yeast heterozygotes. Cell, 116, 121–37.CrossRefGoogle ScholarPubMed
Malik, A. (2004). Metal bioremediation through growing cells. Environment International, 30, 261–78.CrossRefGoogle ScholarPubMed
Mastrolorenzo, A., Scozzafava, A. & Supuran, C. T. (2000). Antifungal activity of silver and zinc complexes of sulfadrug derivatives incorporating arylsulfonylureido moieties. European Journal of Pharmaceutical Sciences, 11, 99–107.CrossRefGoogle ScholarPubMed
Mukhopadhyay, R., Shi, J. & Rosen, B. P. (2000). Purification and characterization of Acr2p, the Saccharomyces cerevisiae arsenate reductase. Journal of Biological Chemistry, 275, 21149–57.CrossRefGoogle ScholarPubMed
Murakami, K. & Yoshino, M. (1999). Dipicolinic acid as an antioxidant: protection of glutathione reductase from the inactivation by copper. Biomedical Research – Tokyo, 20, 321–6.CrossRefGoogle Scholar
Naganuma, A., Miura, N., Kaneko, S., Mishina, T., Hosoya, S., Miyairi, S., Furuchi, T. & Kuge, S. (2000). GFAT as a target molecule of methylmercury toxicity in Saccharomyces cerevisiae. FASEB Journal, 14, 968–72.CrossRefGoogle ScholarPubMed
Nicoletti, G., Domalewska, E. & Borland, R. (1999). Fungitoxicity of oxine and copper oxinate: activity spectrum, development of resistance and synergy. Mycological Research, 103, 1073–84.CrossRefGoogle Scholar
Ohsumi, Y., Kitamoto, K. & Anraku, Y. (1988). Changes induced in the permeability barrier of the yeast plasma membrane by cupric ion. Journal of Bacteriology, 170, 2676–82.CrossRefGoogle ScholarPubMed
Ozbudak, E. M., Thattai, M., Kurtser, I., Grossman, A. D. & Oudenaarden, A. (2002). Regulation of noise in the expression of a single gene. Nature Genetics, 31, 69–73.CrossRefGoogle ScholarPubMed
Park, J. I., Grant, C. M., Davies, M. J. & Dawes, I. W. (1998). The cytoplasmic Cu, Zn superoxide dismutase of Saccharomyces cerevisiae is required for resistance to freeze-thaw stress. Generation of free radicals during freezing and thawing. Journal of Biological Chemistry, 273, 22921–8.CrossRefGoogle ScholarPubMed
Pereira, M. D., Herdeiro, R. S., Fernandes, P. N., Eleutherio, E. C. & Panek, A. D. (2003). Targets of oxidative stress in yeast sod mutants. Biochimica et Biophysica Acta, 1620, 245–51.CrossRefGoogle ScholarPubMed
Pourahmad, J. & O'Brien, P. J. (2000). A comparison of hepatocyte cytotoxic mechanisms for Cu2 + and Cd2 +. Toxicology, 143, 263–73.CrossRefGoogle ScholarPubMed
Predki, P. F. & Sarkar, B. (1992). Effect of replacement of zinc finger zinc on estrogen-receptor DNA interactions. Journal of Biological Chemistry, 267, 5842–6.Google ScholarPubMed
Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C. & O'Halloran, T. V. (1999). Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science, 284, 805–8.CrossRefGoogle ScholarPubMed
Raser, J. M. & O'Shea, E. K. (2004). Control of stochasticity in eukaryotic gene expression. Science, 304, 1811–14.CrossRefGoogle ScholarPubMed
Requena, J. R., Groth, D., Legname, G., Stadtman, E. R., Prusiner, S. B. & Levine, R. L. (2001). Copper-catalyzed oxidation of the recombinant SHa(29–231) prion protein. Proceedings of the National Academy of Sciences of the USA, 98, 7170–5.CrossRefGoogle ScholarPubMed
Rotilio, G., Rossi, L., Demartino, A., Ferreira, A. M. D. S. & Ciriolo, M. R. (1995). Free-radicals, metal-ions and oxidative stress – chemical mechanisms of damage and protection in living systems. Journal of the Brazilian Chemical Society, 6, 221–7.CrossRefGoogle Scholar
Rutherford, J. C. & Bird, A. J. (2004). Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryotic Cell, 3, 1–13.CrossRefGoogle ScholarPubMed
Sarkar, S., Poonam, Y. & Bhatnagar, D. (1997). Cadmium-induced lipid peroxidation and the antioxidant enzymes in rat tissues – role of vitamin E and selenium. Trace Elements and Electrolytes, 14, 41–5.Google Scholar
Shanmuganathan, A., Avery, S. V., Willetts, S. A. & Houghton, J. E. (2004). Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Letters, 556, 253–9.CrossRefGoogle ScholarPubMed
Shenton, D. & Grant, C. M. (2003). Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochemical Journal, 374, 513–19.CrossRefGoogle ScholarPubMed
Shringarpure, R., Grune, T. & Davies, K. J. A. (2001). Protein oxidation and 20S proteasome-dependent proteolysis in mammalian cells. Cellular and Molecular Life Sciences, 58, 1442–50.CrossRefGoogle ScholarPubMed
Srinivasan, C., Liba, A., Imlay, J. A., Valentine, J. S. & Gralla, E. B. (2000). Yeast lacking superoxide dismutase(s) show elevated levels of ‘free iron’ as measured by whole cell electron paramagnetic resonance. Journal of Biological Chemistry, 275, 29187–92.CrossRefGoogle Scholar
Stohs, S. J. & Bagchi, D. (1995). Oxidative mechanisms in the toxicity of metal ions. Free Radical Biology and Medicine, 18, 321–36.CrossRefGoogle ScholarPubMed
Strain, J. & Culotta, V. C. (1996). Copper ions and the regulation of Saccharomyces cerevisiae metallothionein genes under aerobic and anaerobic conditions. Molecular and General Genetics, 251, 139–45.Google ScholarPubMed
Sumner, E. R. & Avery, S. V. (2002). Phenotypic heterogeneity: differential stress resistance among individual cells of the yeast Saccharomyces cerevisiae. Microbiology, 148, 345–51.CrossRefGoogle ScholarPubMed
Sumner, E. R., Avery, A. M., Houghton, J. E., Robins, R. A. & Avery, S. V. (2003). Cell cycle- and age-dependent activation of Sod1p drives the formation of stress-resistant cell subpopulations within clonal yeast cultures. Molecular Microbiology, 50, 857–70.CrossRefGoogle ScholarPubMed
Sumner, E. R., Shanmuganathan, A., Sideri, T. C., Willetts, S. A., Houghton, J. E. & Avery, S. V. (2005). Oxidative protein damage causes chromium toxicity in yeast. Microbiology, 151, 1939–48.CrossRefGoogle Scholar
Szuster-Ciesielska, A., Stachura, A., Slotwinska, M., Kaminska, T., Sniezko, R., Paduch, R., Abramczyk, D., Filar, J. & Kandefer-Szerszen, M. (2000). The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology, 145, 159–71.CrossRefGoogle ScholarPubMed
Tamai, K. T., Gralla, E. B., Ellerby, L. M., Valentine, J. S. & Thiele, D. J. (1993). Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proceedings of the National Academy of Sciences of the USA, 90, 8013–17.CrossRefGoogle ScholarPubMed
Thattai, M. & Oudenaarden, A. (2004). Stochastic gene expression in fluctuating environments. Genetics, 167, 523–30.CrossRefGoogle ScholarPubMed
Tolker-Nielsen, T., Holmstrom, K., Boe, L. & Molin, S. (1998). Non-genetic population heterogeneity studied by in situ polymerase chain reaction. Molecular Microbiology, 27, 1099–105.CrossRefGoogle ScholarPubMed
Uetz, P., Giot, L., Cagney, G., Mansfield, T. A., Judson, R. S., Knight, J. R., Lockshon, D., Narayan, V., Srinivasan, M., Pochart, P., Qureshi-Emili, A., Li, Y., Godwin, B., Conover, D., Kalbfleisch, T., Vijayadamodar, G., Yang, M. J., Johnston, M., Fields, S. & Rothberg, J. M. (2000). A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature, 403, 623–7.CrossRefGoogle ScholarPubMed
Ginkel, G. & Sevanian, A. (1994). Lipid peroxidation-induced membrane structural alterations. Methods in Enzymology, 233, 273–88.CrossRefGoogle ScholarPubMed
Verma, N. & Singh, M. (2005). Biosensors for heavy metals. Biometals, 18, 121–9.CrossRefGoogle ScholarPubMed
Viarengo, A., Burlando, B., Ceratto, N. & Panfoli, I. (2000). Antioxidant role of metallothioneins: A comparative review. Cellular and Molecular Biology, 46, 407–17.Google Scholar
Watabe, S., Hasegawa, H., Takimoto, K., Yamamoto, Y. & Takahashi, S. Y. (1995). Possible function of SP-22, a substrate of mitochondrial ATP-dependent protease, as radical scavenger. Biochemical and Biophysical Research Communications, 213, 1010–16.CrossRefGoogle ScholarPubMed
Wei, J. P. J., Srinivasan, C., Han, H., Valentine, J. S. & Gralla, E. B. (2001). Evidence for a novel role of copper-zinc superoxide dismutase in zinc metabolism. Journal of Biological Chemistry, 276, 44798–803.CrossRefGoogle ScholarPubMed
Wemmie, J. A., Szczypka, M. S., Thiele, D. J. & Moye-Rowley, W. S. (1994). Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. Journal of Biological Chemistry, 269, 32592–7.Google ScholarPubMed
White, C., Sharman, A. K. & Gadd, G. M. (1998). An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nature Biotechnology, 16, 572–5.CrossRefGoogle ScholarPubMed
Winzeler, E. A.et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285, 901–6.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×