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Heat Shock Causes Oxidative Stress and Induces a Variety of Cell Rescue Proteins in Saccharomyces cerevisiae KNU5377  

Kim, Il-Sup (Department of Microbiology, Kyungpook National University)
Moon, Hye-Youn (Metabolic Engineering Laboratory, Korea Research Institute of Bioscience and Biotechnology)
Yun, Hae-Sun (Division of Enteric and Hepatitis Viruses, Center for Infectious Diseases, National Institute of Health)
Jin, Ing-Nyol (Department of Microbiology, Kyungpook National University)
Publication Information
Journal of Microbiology / v.44, no.5, 2006 , pp. 492-501 More about this Journal
Abstract
In this study, we attempted to characterize the physiological response to oxidative stress by heat shock in Saccharomyces cerevisiae KNU5377 (KNU5377) that ferments at a temperature of $40^{\circ}C$. The KNU5377 strain evidenced a very similar growth rate at $40^{\circ}C$ as was recorded under normal conditions. Unlike the laboratory strains of S. cerevisiae, the cell viability of KNU5377 was affected slightly under 2 hours of heat stress conditions at $43^{\circ}C$. KNU5377 evidenced a time-dependent increase in hydroperoxide levels, carbonyl contents, and malondialdehyde (MDA), which increased in the expression of a variety of cell rescue proteins containing Hsp104p, Ssap, Hsp30p, Sod1p, catalase, glutathione reductase, G6PDH, thioredoxin, thioredoxin peroxidase (Tsa1p), Adhp, Aldp, trehalose and glycogen at high temperature. Pma1/2p, Hsp90p and $H^+$-ATPase expression levels were reduced as the result of exposure to heat shock. With regard to cellular fatty acid composition, levels of unsaturated fatty acids (USFAs) were increased significantly at high temperatures ($43^{\circ}C$), and this was particularly true of oleic acid (C18:1). The results of this study indicated that oxidative stress as the result of heat shock may induce a more profound stimulation of trehalose, antioxidant enzymes, and heat shock proteins, as well as an increase in the USFAs ratios. This might contribute to cellular protective functions for the maintenance of cellular homeostasis, and may also contribute to membrane fluidity.
Keywords
Saccharomyces cerevisiae KNU5377; heat shock; oxidative stress; antioxidant enzymes; heat shock proteins; trehalose; fatty acid composition;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 16  (Related Records In Web of Science)
Times Cited By SCOPUS : 14
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1 Kim, J.W., I.N. Jin, and J.H. Seu. 1995a. Isolation of Saccharomyces cerevisiae F38-1, a thermotolerant for fuel alcohol production at higher temperature. Kor. J. Appl. Microbiol. Biotechnol. 23, 617-623
2 Majara, M., E.S.C. O'Conner-Cox, and B.C. Axcell. 1996. Trehalose-an osmoprotectant and stress indicator compound in high and very high gravity brewing. J. Am. Soc. Brew. Chem. 54, 149-154   DOI
3 Mehlen, P., X. Preville, P. Chareyron, J. Briolay, R. Klemenz, and A.P. Arrigo. 1995. Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystalline confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J. Immunol. 154, 363-374
4 Serrano, R. 1978. Characterization of the plasma membrane ATPase of Saccharomyces cerevisiae. Mol. Cell Biochem. 22, 51-63
5 Teparic, R., I., Stuparevic, and V. Mrsa. 2004. Increased mortality of Saccharomyces cerevisiae cell wall protein mutants. Microbiology 150, 3145-3150   DOI   ScienceOn
6 Ambesi, A., M. Miranda, V.V. Petrov, and C.W. Slayman. 2000. Biogenesis and function of the yeast plasma membrane H(+)-ATPase. J. Exp. Biol. 203, 155-160
7 Arrigo, A.P., C. Paul, C. Ducasse, O. Sauvageot, and C. Kretz-Remy. 2002. Small stress proteins: modulation of intracellular redox state and protection against oxidative stress. p. 171-184. In A.-P. Arrigo and W.E.G. Muller (eds.), Small stress proteins. Springer-Verlag Berlin, Germany
8 Carmelo, V., P. Bogaerts, and I. Sa-Correia. 1996. Activity of plasma membrane $H^{+}$-ATPase and expression of PMAI and PMA2 genes in Saccharomyces cerevisiae cells grown at optimal and low pH. Arch. Microbiol. 166, 315-320   DOI
9 Cashikar, A.G., M.L. Duennwald, and S.L. Lindquist. 2005. A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp 104. J. Biol. Chem. in Press
10 Chen, E.C. 1981. Relaease of fatty acids as a consequence of yeast autolysis. J. Am. Soc. Brew. Chem. 39, 117-124
11 Christian, G., L. Gilles, L. Jaekwon, J.M. Buhler, K. Sylvie, P. Michel, B. Helian, B.T. Michael, and L. Jean. 1998. The $H_{2}O_{2}$ stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273, 22480-22489   DOI   ScienceOn
12 Davidson, J.F., B. Whyte, P.H. Bissinger, and R.H. Schiestl. 1996. Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93, 5116-5121
13 Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol. Rev. 24, 469-486   DOI
14 Davidson, J.F. and R.H. Schiestl. 2001a. Cytotoxic and genotoxic consequences of heat stress are dependent on the presence of oxygen in Saccharomyces cerevisiae. J. Bacteriol. 183, 4580-4587   DOI   ScienceOn
15 Fernandes, A.R., F.P. Peixoto, and I. Sa-Correia. 1998. Activation of the $H^{+}$-ATPase in the plasma membrane of cells of Saccharomyces cerevisiae grown under mild copper stress. Arch. Microbiol. 171, 6-12   DOI
16 Walker, G.M. 1998. Yeast physiology and biotechnology. John Wiley & Sons Ltd. Chichester, England
17 Lee, S.M. and J.W. Park. 1998. Thermosensitive phenotype of yeast mutant lacking thioredoxin peroxidase. Arch. Biochem. Biophys. 359, 99-106   DOI   ScienceOn
18 Piper, P.W., C. Ortiz-Calderon, C. Holyoak, P. Coote, and M. Cole. 1997. Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevtstae, is a stress-inducible regulator of plasma membrane H(+)-ATP ase. Cell Stress Chaperones 2, 12-24   DOI
19 Wenzel, T.J., A. Teunissen, and H. Steensma. 1995. PDAI mRNA: a standard for quantitation of mRNA in Saccharomyces cerevisiae superior to ACTI mRNA. Nucleic Acids Res. 23, 883-884   DOI
20 Elisa, C., P. Eva, E. Pedro, H. Enrique, and R. Joaquim. 2000. Oxidative damage stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 275, 27393-27398
21 Navarro-Avino, J.P., R. Prasad, V.J. Miralles, R.M. Bentino, and R. Serrano. 1999. A proposal of nomenclature of aldehyde dehydrogenase in Saccharomyces cerevisiae and characterization of the stress-inducible ALD2 and ALD3 genes. Yeast 15, 829-842   DOI   ScienceOn
22 Ogawa, Y., A. Nitta, H. Uchitama, T. Imamura, H. Shimoi, and K. Ito. 2000. Tolerance mechanism of the tolerant the ethanol-tolerant mutant of sake yeast. J. Biosci. Bioeng. 90, 313-320   DOI
23 Lentini, A., M. Mariani, and S. Takis. 1998. An overview of the physiological changes to the structure and activity of the yeast cell during fermentation, storage and when subjected to successive repitchings. Proc. 25th Conv. Inst. Brew. Asia Pacific Sect., Perth
24 Reznick, A.Z. and L. Packer. 1994. Oxidative damage to proteins: spectrometric method for carbonyl assay. Methods Enzymol. 233, 357-363   DOI
25 Steels, E.L., R.P. Learmonth, and K. Waston. 1994. Stress tolerance and membrane lipid unsaturation in Saccharomyces cerevisiae grown aerobically or anaerobically. Microbiology 140, 569-576   DOI
26 Coote, PJ., M.V. Jones, U. Seymour, D.L. Rowe, D.P. Ferdinando, A.J. McArthur, and M.B. Cole. 1994. Activity of the membrane H(+)-ATPase is a key physiological. determinant of thermotolerance in Saccharromyces cerevisiae. Microbiology 140, 1881-1890   DOI
27 Voit, E.O. 2003. Biochemical and genomic regulation of the trehalose cycle in yeast: review of observation and canonical model analysis. J. Theor. Biol. 223, 55-78   DOI   ScienceOn
28 Brosnan, M.P., D. Donnelly, T.C. James, and U. Bond. 2000. The stress response is repressed during fermentation in brewery strains of yeast. Appl. Microbiol. 88, 746-755   DOI   ScienceOn
29 Fernanda rosa, M. and I. Sa-correia, 1991. In vivo activation by ethanol of plasma membrane ATPase of Saccharomyces cerevisiae. Am. Soc. Microbiol. 57, 830-835
30 Davidson, J.F. and R.H. Schiestl. 2001b. Mitochondrial respiratory electron carriers are involved in oxidative stress during heat stress in Saccharomyces cerevisiae. Mol. Cell. BioI. 21, 8483-8489   DOI   ScienceOn
31 Elutherio, E., M. Ribeiro, M. Pereira, F.M. Maia, and A.D. Panek. 1995. Effect of trehalose during stress in a heat-shock resistant mutant of Saccharomyces cerevisiae. Biochem. Mol. Biol. Int. 36, 1217-1223
32 Pereira Ede, J., A.D. Panek, and E.C. Eleutherio. 2003. Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8, 120-124   DOI
33 Brokovich, K.A., F.W. Farrelly, D.B. Finkelstein, J. Taulien, and S. Lindquist. 1989. Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 9, 3919-3930   DOI
34 Kim, I.S., H.S. Yun, H. Shimisu, E. Kitakawa, H. Iwahashi, and I.N. Jin. 2005. Elucidation of copper and asparagine transport systems in Saccharomyces cerevisiae KNU5377 through genome-wide transcriptional analysis. J. Microbiol. Biotechnol. 15, 1240-1249   과학기술학회마을
35 Seymour, I.J. and P.W. Piper. 1999. Stress induction of HSP30, the plasma membrane heat shock protein gene of Saccharomyces cerevisiae, appears not to use known stress-regulated transcription factors. Microbiology 145, 231-239   DOI   ScienceOn
36 Rogalla, T., M. Ehrnsperger, X. Preville, A Kotlyarov, G. Lustsch, C. Ducasse, C. Paul, M. Wieske, A.P. Arrigo, J. Buchner, and M. Gaestel. 1999. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J. Biol. Chem. 274, 18947-18956   DOI
37 Aguilera, A, R.A. Peinado, C. Millan, J.M. Ortega, and J.C. Mauicio. 2006. Relationship between ethanol tolerance, H+-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. Int. J. Food Microbiol. 110, 34-42   DOI   ScienceOn
38 Chatterjee, M.T., S.A. Khalawan, and B.P. Curran. 2000. Cellular lipid composition influences stress activation of the yeast general stress response element (STRE). Microbiology 146, 877-884   DOI
39 Hohnman, S. and E.H. Mager. 2003. Yeast stress responses. Springer-Verlag Berlin, German
40 Preville, X., F. Salvemini, S. Giraud, S. Chaufour, C. Paul, G. Stepien, M.Y. Ursini, and AP. Arrigo. 1999. Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp. Cell Res. 247, 61-78   DOI   ScienceOn
41 Echave, P., J. Tamarit, E. Cabiscol, and J. Ros. 2003. Novel antioxidant role of alcohol dehydrogenase E from Escherichia coli. J. BioI. Chem. 278, 30193-30198   DOI   ScienceOn
42 Laemmli, U.K. 1979. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685   DOI   ScienceOn
43 Lushchak, V.I. and T.V. Bagnyukova. 2006b. Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comp. Biochem. Physiol. C Toxiol. Pharmacol. 143, 36-41   DOI   ScienceOn
44 Beaven, M.J., C. Charpentier, and A.H. Rose. 1982. Production and tolerance of ethanol in relation to phospholipid fatty acyl composition of Saccharomyces cerevisiae. J. Gen. Microbiol. 128, 1447-1455
45 Swan, T.M. and K. Watson. 1997. Membrane fatty acid composition and membrane fluidity as parameters of stress tolerance in yeast. Can. J. Microbiol. 43, 70-77   DOI   ScienceOn
46 Walker, G.M. and P.V. Dijck. 2006. Physiological and molecular responses of yeasts to the environment, p. 111-152. In Querol, A and G. Fleet (eds.), Yeasts in food and beverages, Springer-Verlag Berlin, Germany
47 Wolff, S.P. 1994. Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxide. Methods Enzymol. 233, 182-189   DOI
48 Herdeiro, R.S., M.D. Pereira, A.D. Panek, and E.C. Eleutherio. 2006. Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochem. Biophys. Acta 1760, 340-346   DOI   ScienceOn
49 Miller, L.T. 1982. Single deriviation method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxyl acid. J. Clin. Microbiol. 18, 861-867
50 Benaroudj, N., D.H. Lee, and A.L. Goldberg. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276, 24261-24267   DOI   ScienceOn
51 Panaretou, B. and P.W. Piper. 1992. The plasma membrane of yeast acquires a novel heat shock protein (hsp30) and displays a decline in proton-pumping ATPase levels in response to both heat shock and the entry to stationary phase. Eur. J. Biochem. 206, 635-640   DOI   ScienceOn
52 Piper, P.W., K. Talreja, B. Panaretou, P. Moradas-Ferreira, K. Byrne, U.M. Praekelt, P. Meacock, M. Recnacq, and H. Boucherie. 1994. Induction of major heat shock proteins of Saccharomyces cerevisiae, including plasma membrane Hsp30, by ethanol levels above a critical threshold. Microbiology 140, 3031-3038   DOI
53 Patrica, M., B. Fernandes, T. Domitrovic, C.M. Kao, and E. Kurtenach. 2004. Genomic expression pattern in Saccharomyces cerevisiae cells in response to high hydrostatic pressure. FEMS Lett. 556, 153-160
54 Fillinger, S., M.K. Chaveroche, P. van Dijck, R. de Vries, G. Ruijter, J. Thevelein, and C. d'Enfert. 2001. Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147, 1851-1862   DOI
55 Kim, J.W., S.H. Kim, and I.N. Jin. 1995b. The fermentation characteristics of Saccharomyces cerevisiae F38-1, a thermotolerant yeast isolated for fuel alcohol production at elevated temperature. Kor. J. Appl. Microbiol. Biotechn. 23, 624-631
56 Lushchak, V.I. and T.V. Bagnyukova. 2006a. Temperature increase results in oxidative stress in goldfish tissues. 1. Indices of oxidative stress. Comp. Biochem. Physiol. C Toxiol. Pharmacol. 143, 30-35   DOI   ScienceOn
57 Beuge, J.A. and S.D. Aust. 1978. Microsomal lipid peroxidation. Methods Enzymol. 52, 302-310   DOI