全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Impact of Acute Metal Stress in Saccharomyces cerevisiae

DOI: 10.1371/journal.pone.0083330

Full-Text   Cite this paper   Add to My Lib

Abstract:

Although considered as essential cofactors for a variety of enzymatic reactions and for important structural and functional roles in cell metabolism, metals at high concentrations are potent toxic pollutants and pose complex biochemical problems for cells. We report results of single dose acute toxicity testing in the model organism S. cerevisiae. The effects of moderate toxic concentrations of 10 different human health relevant metals, Ag+, Al3+, As3+, Cd2+, Co2+, Hg2+, Mn2+, Ni2+, V3+, and Zn2+, following short-term exposure were analyzed by transcription profiling to provide the identification of early-on target genes or pathways. In contrast to common acute toxicity tests where defined endpoints are monitored we focused on the entire genomic response. We provide evidence that the induction of central elements of the oxidative stress response by the majority of investigated metals is the basic detoxification process against short-term metal exposure. General detoxification mechanisms also comprised the induction of genes coding for chaperones and those for chelation of metal ions via siderophores and amino acids. Hierarchical clustering, transcription factor analyses, and gene ontology data further revealed activation of genes involved in metal-specific protein catabolism along with repression of growth-related processes such as protein synthesis. Metal ion group specific differences in the expression responses with shared transcriptional regulators for both, up-regulation and repression were also observed. Additionally, some processes unique for individual metals were evident as well. In view of current concerns regarding environmental pollution our results may support ongoing attempts to develop methods to monitor potentially hazardous areas or liquids and to establish standardized tests using suitable eukaryotic a model organism.

References

[1]  Waldron KJ, Rutherford JC, Ford D, Robinson NJ (2009) Metalloproteins and metal sensing. Nature 460: 823–830.
[2]  Ballatori N (2002) Transport of toxic metals by molecular mimicry. Environ Health Perspect 110 Suppl 5: 689–694.
[3]  Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12: 1161–1208.
[4]  Porwol T, Ehleben W, Zierold K, Fandrey J, Acker H (1998) The influence of nickel and cobalt on putative members of the oxygen-sensing pathway of erythropoietin-producing HepG2 cells. Eur J Biochem 256: 16–23.
[5]  Rainbow PS, Black WH (2005) Cadmium, zinc and the uptake of calcium by two crabs, Carcinus maenas and Eriocheir sinensis. Aquat Toxicol 72: 45–65.
[6]  Qiu JW, Xie ZC, Wang WX (2005) Effects of calcium on the uptake and elimination of cadmium and zinc in Asiatic clams. Arch Environ Contam Toxicol 48: 278–287.
[7]  Belcastro M, Marino T, Russo N, Toscano M (2005) Interaction of cysteine with Cu2+ and group IIb (Zn2+, Cd2+, Hg2+) metal cations: a theoretical study. J Mass Spectrom 40: 300–306.
[8]  Stohs SJ (1995) The role of free radicals in toxicity and disease. J Basic Clin Physiol Pharmacol 6: 205–228.
[9]  Chen F, Shi X (2002) Intracellular signal transduction of cells in response to carcinogenic metals. Crit Rev Oncol Hematol 42: 105–121.
[10]  Dandrea T, Hellmold H, Jonsson C, Zhivotovsky B, Hofer T, et al. (2004) The transcriptosomal response of human A549 lung cells to a hydrogen peroxide-generating system: relationship to DNA damage, cell cycle arrest, and caspase activation. Free Radic Biol Med 36: 881–896.
[11]  Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82: 493–512.
[12]  Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51: 730–750.
[13]  Rosen BP (2002) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A Mol Integr Physiol 133: 689–693.
[14]  Mager WH, De Kruijff AJ (1995) Stress-induced transcriptional activation. Microbiol Rev 59: 506–531.
[15]  Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241–4257.
[16]  Jin YH, Dunlap PE, McBride SJ, Al-Refai H, Bushel PR, et al. (2008) Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet 4: e1000053.
[17]  Wysocki R, Tamas MJ (2010) How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiol Rev 34: 925–951.
[18]  Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, et al. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29: 365–371.
[19]  Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
[20]  Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, et al. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700–2707.
[21]  Silver JD, Ritchie ME, Smyth GK (2009) Microarray background correction: maximum likelihood estimation for the normal-exponential convolution. Biostatistics 10: 352–363.
[22]  Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31: 265–273.
[23]  Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–193.
[24]  Smyth GK, Gentleman R, Carey V, Dudoit S, Irizarry R, et al.. (2005) Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor Springer, New York.
[25]  Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863–14868.
[26]  Nadon R, Shoemaker J (2002) Statistical issues with microarrays: processing and analysis. Trends Genet 18: 265–271.
[27]  Saldanha AJ (2004) Java Treeview–extensible visualization of microarray data. Bioinformatics 20: 3246–3248.
[28]  Tavazoie S, Hughes JD, Campbell MJ, Cho RJ, Church GM (1999) Systematic determination of genetic network architecture. Nat Genet 22: 281–285.
[29]  McLachlan GJ, Do K-A, Ambroise C (2004) Analyzing microarray gene expression data. Hoboken, N.J.: Wiley-Interscience. xx, 320 p. p.
[30]  Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99–104.
[31]  Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33: W592–595.
[32]  Haugen AC, Kelley R, Collins JB, Tucker CJ, Deng C, et al. (2004) Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5: R95.
[33]  Dormer UH, Westwater J, McLaren NF, Kent NA, Mellor J, et al. (2000) Cadmium-inducible expression of the yeast GSH1 gene requires a functional sulfur-amino acid regulatory network. J Biol Chem 275: 32611–32616.
[34]  Rep M, Krantz M, Thevelein JM, Hohmann S (2000) The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275: 8290–8300.
[35]  Thorsen M, Di Y, Tangemo C, Morillas M, Ahmadpour D, et al. (2006) The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol Biol Cell 17: 4400–4410.
[36]  Akache B, Turcotte B (2002) New regulators of drug sensitivity in the family of yeast zinc cluster proteins. J Biol Chem 277: 21254–21260.
[37]  Larochelle M, Drouin S, Robert F, Turcotte B (2006) Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. Mol Cell Biol 26: 6690–6701.
[38]  Boeke JD, Sandmeyer SB (1991) Yeast transposable elements. The molecular and cellular biology of the yeast Saccharomyces The molecular and cellular biology of the yeast Saccharomyces Broach J, Jones E, Pringle J, (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY) 1: 193–261.
[39]  Vido K, Spector D, Lagniel G, Lopez S, Toledano MB, et al. (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J Biol Chem 276: 8469–8474.
[40]  Momose Y, Iwahashi H (2001) Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environ Toxicol Chem 20: 2353–2360.
[41]  Thorsen M, Lagniel G, Kristiansson E, Junot C, Nerman O, et al. (2007) Quantitative transcriptome, proteome, and sulfur metabolite profiling of the Saccharomyces cerevisiae response to arsenite. Physiol Genomics 30: 35–43.
[42]  Thorsen M, Perrone GG, Kristiansson E, Traini M, Ye T, et al. (2009) Genetic basis of arsenite and cadmium tolerance in Saccharomyces cerevisiae. BMC Genomics 10: 105.
[43]  Chrestensen CA, Starke DW, Mieyal JJ (2000) Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed disulfides, and initiates apoptosis. J Biol Chem 275: 26556–26565.
[44]  Khanna S, Lakhera PC, Khandelwal S (2011) Interplay of early biochemical manifestations by cadmium insult in sertoli-germ coculture: an in vitro study. Toxicology 287: 46–53.
[45]  Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18: 321–336.
[46]  Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1: 529–539.
[47]  Fauchon M, Lagniel G, Aude JC, Lombardia L, Soularue P, et al. (2002) Sulfur sparing in the yeast proteome in response to sulfur demand. Mol Cell 9: 713–723.
[48]  Tamas MJ, Wysocki R (2001) Mechanisms involved in metalloid transport and tolerance acquisition. Curr Genet 40: 2–12.
[49]  Niazi JH, Sang BI, Kim YS, Gu MB (2011) Global gene response in Saccharomyces cerevisiae exposed to silver nanoparticles. Appl Biochem Biotechnol 164: 1278–1291.
[50]  Hassinen VH, Tervahauta AI, Schat H, Karenlampi SO (2011) Plant metallothioneins–metal chelators with ROS scavenging activity? Plant Biol (Stuttg) 13: 225–232.
[51]  Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116: 409–418.
[52]  Stadler JA, Schweyen RJ (2002) The yeast iron regulon is induced upon cobalt stress and crucial for cobalt tolerance. J Biol Chem 277: 39649–39654.
[53]  Chen CY, Wang YF, Lin YH, Yen SF (2003) Nickel-induced oxidative stress and effect of antioxidants in human lymphocytes. Arch Toxicol 77: 123–130.
[54]  Saponja JA, Vogel HJ (1996) Metal-ion binding properties of the transferrins: a vanadium-51 NMR study. J Inorg Biochem 62: 253–270.
[55]  Ward RJ, Zhang Y, Crichton RR (2001) Aluminium toxicity and iron homeostasis. J Inorg Biochem 87: 9–14.
[56]  Chen H, Davidson T, Singleton S, Garrick MD, Costa M (2005) Nickel decreases cellular iron level and converts cytosolic aconitase to iron-regulatory protein 1 in A549 cells. Toxicol Appl Pharmacol 206: 275–287.
[57]  Pagani MA, Casamayor A, Serrano R, Atrian S, Arino J (2007) Disruption of iron homeostasis in Saccharomyces cerevisiae by high zinc levels: a genome-wide study. Mol Microbiol 65: 521–537.
[58]  Ruotolo R, Marchini G, Ottonello S (2008) Membrane transporters and protein traffic networks differentially affecting metal tolerance: a genomic phenotyping study in yeast. Genome Biol 9: R67.
[59]  Cao YR, Zhang XY, Deng JY, Zhao QQ, Xu H (2012) Lead and cadmium-induced oxidative stress impacting mycelial growth of Oudemansiella radicata in liquid medium alleviated by microbial siderophores. World J Microbiol Biotechnol 28: 1727–1737.
[60]  Pearce DA, Sherman F (1999) Toxicity of copper, cobalt, and nickel salts is dependent on histidine metabolism in the yeast Saccharomyces cerevisiae. J Bacteriol 181: 4774–4779.
[61]  Farcasanu IC, Mizunuma M, Nishiyama F, Miyakawa T (2005) Role of L-histidine in conferring tolerance to Ni2+ in Sacchromyces cerevisiae cells. Biosci Biotechnol Biochem 69: 2343–2348.
[62]  Ralph DM, Robinson SR, Campbell MS, Bishop GM (2010) Histidine, cystine, glutamine, and threonine collectively protect astrocytes from the toxicity of zinc. Free Radic Biol Med 49: 649–657.
[63]  Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30: 405–439.
[64]  Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci U S A 94: 12949–12956.
[65]  Kim S, Schilke B, Craig EA, Horwich AL (1998) Folding in vivo of a newly translated yeast cytosolic enzyme is mediated by the SSA class of cytosolic yeast Hsp70 proteins. Proc Natl Acad Sci U S A 95: 12860–12865.
[66]  Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73–82.
[67]  Abbas-Terki T, Donze O, Briand PA, Picard D (2001) Hsp104 interacts with Hsp90 cochaperones in respiring yeast. Mol Cell Biol 21: 7569–7575.
[68]  Lee DH, Sherman MY, Goldberg AL (1996) Involvement of the molecular chaperone Ydj1 in the ubiquitin-dependent degradation of short-lived and abnormal proteins in Saccharomyces cerevisiae. Mol Cell Biol 16: 4773–4781.
[69]  Ezaki B, Sasaki K, Matsumoto H, Nakashima S (2005) Functions of two genes in aluminium (Al) stress resistance: repression of oxidative damage by the AtBCB gene and promotion of efflux of Al ions by the NtGDI1gene. J Exp Bot 56: 2661–2671.
[70]  Wu LF, Hughes TR, Davierwala AP, Robinson MD, Stoughton R, et al. (2002) Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters. Nat Genet 31: 255–265.
[71]  Hosiner D, Lempiainen H, Reiter W, Urban J, Loewith R, et al. (2009) Arsenic toxicity to Saccharomyces cerevisiae is a consequence of inhibition of the TORC1 kinase combined with a chronic stress response. Mol Biol Cell 20: 1048–1057.
[72]  Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717–728.
[73]  Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437–440.
[74]  Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, et al. (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10: 457–468.
[75]  Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124: 471–484.
[76]  Martin DE, Soulard A, Hall MN (2004) TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969–979.
[77]  Lempiainen H, Shore D (2009) Growth control and ribosome biogenesis. Curr Opin Cell Biol 21: 855–863.
[78]  Lempiainen H, Uotila A, Urban J, Dohnal I, Ammerer G, et al. (2009) Sfp1 interaction with TORC1 and Mrs6 reveals feedback regulation on TOR signaling. Mol Cell 33: 704–716.
[79]  Bozhkov A, Padalko V, Dlubovskaya V, Menzianova N (2010) Resistance to heavy metal toxicity in organisms under chronic exposure. Indian J Exp Biol 48: 679–696.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133