Roles of the Yap1 transcription factor and antioxidants in Saccharomyces cerevisiae's tolerance to furfural and 5-Hydroxymethylfurfural, which function as Thiol-Reactive electrophiles generating oxidative stress

Applied and Environmental Microbiology

Volumn 79, Issue 16, 2013, Pages 5069-5077

  Kim, Daehee ^a   Hahn, Ji Sook ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYL FURFURALS; CONSTITUTIVELY ACTIVES; CULTURE MEDIUM; ELECTROPHILES; OVER-EXPRESSION; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE STRAINS; TARGET GENES;

BIOCHEMISTRY; CELLULOSIC ETHANOL; FURFURAL; GENES; REACTION KINETICS; TRANSCRIPTION FACTORS; YEAST;

ALDEHYDES;

5 HYDROXYMETHYLFURFURAL; 5-HYDROXYMETHYLFURFURAL; ALCOHOL; BIOFUEL; CATALASE; DRUG DERIVATIVE; FURFURAL; GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SACCHAROMYCES CEREVISIAE PROTEIN; THIOL DERIVATIVE; TRANSCRIPTION FACTOR; YAP1 PROTEIN, S CEREVISIAE;

ANTIOXIDANT; CELLULOSE; ETHANOL; GENE EXPRESSION; GENETIC ALGORITHM; OIL PRODUCTION; OXIDATION; SPECIES DIVERSITY; YEAST;

ARTICLE; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE;

BIOFUELS; CATALASE; ETHANOL; FURALDEHYDE; GLUTATHIONE; HYDROGEN PEROXIDE; INDUSTRIAL MICROBIOLOGY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFHYDRYL COMPOUNDS; TRANSCRIPTION FACTORS;

EID: 84880978562     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00643-13     Document Type: Article

References (40)

1. Yang B, Wyman CE. 2008. Pretreatment: the key to unlocking low-cost cellulosic ethanol. Biofuels Bioproducts Biorefining 2:26-40.
2. Laluce C, Schenberg ACG, Gallardo JCM, Coradello LFC, Pombeiro-Sponchiado SR. 2012. Advances and developments in strategies to improve strains of Saccharomyces cerevisiae and processes to obtain the lignocellulosic ethanol-a review. Appl. Biochem. Biotechnol. 166:1908-1926.
3. Chheda JN, Roman-Leshkov Y, Dumesic JA. 2007. Production of 5-hydroxymethylfurfural and furfural by dehydration of biomass-derived mono-and poly-saccharides. Green Chem. 9:342-350.
4. Almeida JR, Bertilsson M, Gorwa-Grauslund MF, Gorsich S, Liden G. 2009. Metabolic effects of furaldehydes and impacts on biotechnological processes. Appl. Microbiol. Biotechnol. 82:625-638.
5. Taherzadeh MJ, Gustafsson L, Niklasson C, Liden G. 2000. Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 53:701-708.
6. Almeida JRM, Roder A, Modig T, Laadan B, Liden G, Gorwa-Grauslund MF. 2008. NADH-vs NADPH-coupled reduction of 5-hydroxymethyl furfural (HMF) and its implications on product distribution in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 78:939-945.
7. Petersson A, Almeida JR, Modig T, Karhumaa K, Hahn-Hagerdal B, Gorwa-Grauslund MF, Liden G. 2006. A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23:455-464.
8. Liu ZL, Moon J, Andersh BJ, Slininger PJ, Weber S. 2008. Multiple gene-mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxymethylfurfural by Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 81:743-753.
9. Liu ZL, Moon J. 2009. A novel NADPH-dependent aldehyde reductase gene from Saccharomyces cerevisiae NRRL Y-12632 involved in the detoxification of aldehyde inhibitors derived from lignocellulosic biomass conversion. Gene 446:1-10.
10. Heer D, Heine D, Sauer U. 2009. Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl. Environ. Microbiol. 75:7631-7638.
11. Moon J, Liu ZL. 2012. Engineered NADH-dependent GRE2 from Saccharomyces cerevisiae by directed enzyme evolution enhancesHMFreduction using additional cofactor NADPH. Enzyme Microbiol. Technol. 50: 115-120.
12. Liu ZL. 2011. Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl. Microbiol. Biotechnol. 90: 809-825.
13. Park SE, Koo HM, Park YK, Park SM, Park JC, Lee OK, Park YC, Seo JH. 2011. Expression of aldehyde dehydrogenase 6 reduces inhibitory effect of furan derivatives on cell growth and ethanol production in Saccharomyces cerevisiae. Bioresour. Technol. 102:6033-6038.
14. Miller EN, Jarboe LR, Yomano LP, York SW, Shanmugam KT, Ingram LO. 2009. Silencing of NADPH-dependent oxidoreductase genes (yqhD and dkgA) in furfural-resistant ethanologenic Escherichia coli. Appl. Environ. Microbiol. 75:4315-4323.
15. Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD. 2006. Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 71:339-349.
16. Li BZ, Yuan YJ. 2010. Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 86: 1915-1924.
17. Ma M, Liu ZL. 2010. Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 11:660. doi:10.1186/1471-2164-11-660.
18. Alriksson B, Horvath IS, Jonsson LJ. 2010. Overexpression of Saccharomyces cerevisiae transcription factor and multidrug resistance genes conveys enhanced resistance to lignocellulose-derived fermentation inhibitors. Process Biochem. 45:264-271.
19. Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, Slininger PJ, Liu ZL, Gorsich SW. 2010. Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol. Biofuels 3:2-11.
20. Miller EN, Jarboe LR, Turner PC, Pharkya P, Yomano LP, York SW, Nunn D, Shanmugam KT, Ingram LO. 2009. Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180. Appl. Environ. Microbiol. 75:6132-6141.
21. Keating JD, Panganiban C, Mansfield SD. 2006. Tolerance and adaptation of ethanologenic yeasts to lignocellulosic inhibitory compounds. Biotechnol. Bioeng. 93:1196-1206.
22. Liu ZL, Slininger PJ, Dien BS, Berhow MA, Kurtzman CP, Gorsich SW. 2004. Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2,5-bishydroxymethylfuran. J. Ind. Microbiol. Biotechnol. 31:345-352.
23. Nolan T, Hands RE, Bustin SA. 2006. Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 1:1559-1582.
24. Myhre O, Andersen JM, Aarnes H, Fonnum F. 2003. Evaluation of the probes 2=,7=-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem. Pharmacol. 65:1575-1582.
25. Sedlak J, Lindsay RH. 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal. Biochem. 25:192-205.
26. Rahman I, Kode A, Biswas SK. 2006. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 1:3159-3165.
27. Herrero E, Ros J, Belli G, Cabiscol E. 2008. Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta 1780:1217-1235.
28. Azevedo D, Tacnet F, Delaunay A, Rodrigues-Pousada C, Toledano MB. 2003. Two redox centers within Yap1 for H2O2 and thiol-reactive chemicals signaling. Free Radic. Biol. Med. 35:889-900.
29. Ouyang X, Tran QT, Goodwin S, Wible RS, Sutter CH, Sutter TR. 2011. Yap1 activation by H2O2 or thiol-reactive chemicals elicits distinct adaptive gene responses. Free Radic. Biol. Med. 50:1-13.
30. Grant CM, MacIver FH, Dawes IW. 1996. Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 29:511-515.
31. Lee J, Godon C, Lagniel G, Spector D, Garin J, Labarre J, Toledano MB. 1999. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274:16040-16046.
32. Jungwirth H, Wendler F, Platzer B, Bergler H, Hogenauer G. 2000. Diazaborine resistance in yeast involves the efflux pumps Ycf1p and Flr1p and is enhanced by a gain-of-function allele of gene YAP1. Eur. J. Biochem. 267:4809-4816.
33. Grant CM. 2001. Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol. Microbiol. 39:533-541.
34. Sugiyama K, Izawa S, Inoue Y. 2000. The Yap1p-dependent induction of glutathione synthesis in heat shock response of Saccharomyces cerevisiae. J. Biol. Chem. 275:15535-15540.
35. Grant CM, Collinson LP, Roe JH, Dawes IW. 1996. Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol. Microbiol. 21:171-179.
36. Getz EB, Xiao M, Chakrabarty T, Cooke R, Selvin PR. 1999. A comparison between the sulfhydryl reductants tris(2-carboxyethyl)phosphine and dithiothreitol for use in protein biochemistry. Anal. Biochem. 273: 73-80.
37. Trotter EW, Grant CM. 2002. Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 46:869-878.
38. Bourbouloux A, Shahi P, Chakladar A, Delrot S, Bachhawat AH. 2000. Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275:13259-13265.
39. Penninckx MJ. 2002. An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res. 2:295-305.
40. Li ZS, Szczypka M, Lu YP, Thiele DJ, Rea PA. 1996. The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem. 271:6509-6517.