The alcohol dehydrogenases of Saccharomyces cerevisiae: A comprehensive review

FEMS Yeast Research

Volumn 8, Issue 7, 2008, Pages 967-978

  De Smidt, Olga ^a,b   Du Preez, James C ^a   Albertyn, Jacobus ^a  

^a UNIVERSITY OF THE FREE STATE   (South Africa)

^b CENTRAL UNIVERSITY OF TECHNOLOGY   (South Africa)

Author keywords

Alcohol dehydrogenase; Function; Kinetics; Localization; Molecular regulation; Saccharomyces cerevisiae

Indexed keywords

ALCOHOL DEHYDROGENASE;

ADH1 GENE; ADH2 GENE; ADH3 GENE; ADH4 GENE; ADH5 GENE; ADH6 GENE; ADH7 GENE; AMINO ACID SEQUENCE; BINDING SITE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COENZYME; CONFERENCE PAPER; ENZYME LOCALIZATION; GENE; GENE CONTROL; GENE EXPRESSION; KINETICS; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

ALCOHOL DEHYDROGENASE; ALCOHOLS; GENE EXPRESSION REGULATION, FUNGAL; KINETICS; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 54049146291     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2008.00387.x     Document Type: Conference Paper

References (107)

1. Bakker BM, Bro C, Kotter P, Luttik MA, van Dijken JP Pronk JT (2000) The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae. J Bacteriol 182 : 4730 4737.
2. Beier DR Young ET (1982) Characterization of a regulatory region upstream of the ADR2 locus of S. cerevisiae. Nature 300 : 724 728.
3. Beier DR, Sledziewski A Young ET (1985) Deletion analysis identifies a region, upstream of the ADH2 gene of Saccharomyces cerevisiae, which is required for ADR1-mediated derepression. Mol Cell Biol 5 : 1743 1749.
4. Bennetzen JL Hall BD (1982) The primary structure of the Saccharomyces cerevisiae gene for alcohol dehydrogenase. J Biol Chem 257 : 3018 3025.
5. Bird AJ, Gordon M, Eide DJ Winge DR (2006) Repression of ADH1 and ADH3 during zinc deficiency by Zap1-induced intergenic RNA transcripts. EMBO J 25 : 5726 5734.
6. Blumberg H, Eisen A, Sledziewski A, Bader D Young ET (1987) Two zinc fingers of a yeast regulatory protein shown by genetic evidence to be essential for its function. Nature 328 : 443 445.
7. Branden CI, Jornvall H, Eklund H Furugren B (1975) Alcohol dehydrogenases. The Enzymes (Boyer PD, eds), pp. 104 190. Academic Press, New York.
8. Bro C, Regenberg B, Lagniel G, Labarre J, Montero-Lomeli M Nielsen J (2003) Transcriptional, proteomic, and metabolic responses to lithium in galactose-grown yeast cells. J Biol Chem 278 : 32141 32149.
9. Cheng LY Lek LH (1992) Inhibition of alcohol dehydrogenases by thiol compounds. FEBS Lett 300 : 251 253.
10. Ciriacy M (1975a) Genetics of alcohol dehydrogenase in Saccharomyces cerevisiae: I. Isolation and genetic analysis of adh mutants. Mutat Res 29 : 315 325.
11. Ciriacy M (1975b) Genetics of alcohol dehydrogenase in Saccharomyces cerevisiae. II. Two loci controlling synthesis of the glucose-repressible ADH II. Mol Gen Genet 138 : 157 164.
12. Ciriacy M (1976) Cis-dominant regulatory mutations affecting the formation of glucose-repressible alcohol dehydrogenase (ADHII) in Saccharomyces cerevisiae. Mol Gen Genet 145 : 327 333.
13. Ciriacy M (1979) Isolation and characterization of further cis- and trans-acting regulatory elements involved in the synthesis of glucose-repressible alcohol dehydrogenase (ADHII) in Saccharomyces cerevisiae. Mol Gen Genet 176 : 427 431.
14. Ciriacy M (1997) Alcohol dehydrogenases. Yeast Sugar Metabolism (Zimmermann FK Entian KD, eds), pp. 213 223. Technomic Publishing Co. Inc., Lancaster.
15. Collart MA Struhl K (1994) NOT1(CDC39), NOT2(CDC36), NOT3, and NOT4 encode a global-negative regulator of transcription that differentially affects TATA-element utilization. Genes Dev 8 : 525 537.
16. Cook WJ Denis CL (1993) Identification of three genes required for the glucose-dependent transcription of the yeast transcriptional activator ADR1. Curr Genet 23 : 192 200.
17. de Bolle X, Vinals C, Fastrez J Feytmans E (1997) Bivalent cations stabilize yeast alcohol dehydrogenase I. Biochem J 323 : 409 413.
18. Denis CL (1984) Identification of new genes involved in the regulation of yeast alcohol dehydrogenase II. Genetics 108 : 833 844.
19. Denis CL Audino DC (1991) The CCR1 (SNF1) and SCH9 protein kinases act independently of cAMP-dependent protein kinase and the transcriptional activator ADR1 in controlling yeast ADH2 expression. Mol Gen Genet 229 : 395 399.
20. Denis CL Gallo C (1986) Constitutive RNA synthesis for the yeast activator ADR1 and identification of the ADR1-5c mutation: implications in posttranslational control of ADR1. Mol Cell Biol 6 : 4026 4030.
21. Denis CL Malvar T (1990) The CCR4 gene from Saccharomyces cerevisiae is required for both nonfermentative and spt-mediated gene expression. Genetics 124 : 283 291.
22. Denis CL, Ciriacy M Young ET (1981) A positive regulatory gene is required for accumulation of the functional messenger RNA for the glucose-repressible alcohol dehydrogenase from Saccharomyces cerevisiae. J Mol Biol 148 : 355 368.
23. Denis CL, Ferguson J Young ET (1983) mRNA levels for the fermentative alcohol dehydrogenase of Saccharomyces cerevisiae decrease upon growth on a nonfermentable carbon source. J Biol Chem 258 : 1165 1171.
24. Denis CL, Fontaine SC, Chase D, Kemp BE Bemis LT (1992) ADR1c mutations enhance the ability of ADR1 to activate transcription by a mechanism that is independent of effects on cyclic AMP-dependent protein kinase phosphorylation of Ser-230. Mol Cell Biol 12 : 1507 1514.
25. Dickinson FM Dack S (2001) The activity of yeast ADH I and ADH II with long-chain alcohols and diols. Chem Biol Interact 130-132 : 417 423.
26. Dickinson JR, Lanterman MM, Danner DJ, Pearson BM, Sanz P, Harrison SJ Hewlins MJ (1997) A 13C nuclear magnetic resonance investigation of the metabolism of leucine to isoamyl alcohol in Saccharomyces cerevisiae. J Biol Chem 272 : 26871 26878.
27. Dickinson JR, Harrison SJ Hewlins MJ (1998) An investigation of the metabolism of valine to isobutyl alcohol in Saccharomyces cerevisiae. J Biol Chem 273 : 25751 25756.
28. Dickinson JR, Harrison SJ, Dickinson JA Hewlins MJ (2000) An investigation of the metabolism of isoleucine to active Amyl alcohol in Saccharomyces cerevisiae. J Biol Chem 275 : 10937 10942.
29. Dickinson JR, Salgado LE Hewlins MJ (2003) The catabolism of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J Biol Chem 278 : 8028 8034.
30. Di Mauro E, Kendrew SG Caserta M (2000) Two distinct nucleosome alterations characterize chromatin remodeling at the Saccharomyces cerevisiae ADH2 promoter. J Biol Chem 275 : 7612 7618.
31. Donoviel MS, Kacherovsky N Young ET (1995) Synergistic activation of ADH2 expression is sensitive to upstream activation sequence 2 (UAS2) orientation, copy number and UAS1-UAS2 helical phasing. Mol Cell Biol 15 : 3442 3449.
32. Dorsey MJ, Hoeh P Paquin CE (1993) Phenotypic identification of amplifications of the ADH4 and CUP1 genes of Saccharomyces cerevisiae. Curr Genet 23 : 392 396.
33. Drewke C Ciriacy M (1988) Overexpression, purification and properties of alcohol dehydrogenase IV from Saccharomyces cerevisiae. Biochim Biophys Acta 950 : 54 60.
34. Drewke C, Thielen J Ciriacy M (1990) Ethanol formation in adh0 mutants reveals the existence of a novel acetaldehyde-reducing activity in Saccharomyces cerevisiae. J Bacteriol 172 : 3909 3917.
35. Feldmann H, Aigle M, Aljinovic G, Andre B, Baclet MC, Barthe C, Baur A, Becam AM, Biteau N Boles E (1994) Complete DNA sequence of yeast chromosome II. EMBO J 13 : 5795 5809.
36. Ganzhorn AJ, Green DW, Hershey AD, Gould RM Plapp BV (1987) Kinetic characterization of yeast alcohol dehydrogenases. Amino acid residue. 294 and substrate specificity. J Biol Chem 262 : 3754 3761.
37. Gonzalez E, Fernandez MR, Larroy C, Sola L, Pericas MA, Pares X Biosca JA (2000) Characterization of a (2R,3R)-2,3-butanediol dehydrogenase as the Saccharomyces cerevisiae YAL060W gene product. Disruption and induction of the gene. J Biol Chem 275 : 35876 35885.
38. Green DW, Sun HW Plapp BV (1993) Inversion of the substrate specificity of yeast alcohol dehydrogenase. J Biol Chem 268 : 7792 7798.
39. Grey M, Schmidt M Brendel M (1996) Overexpression of ADH1 confers hyper-resistance to formaldehyde in Saccharomyces cerevisiae. Curr Genet 29 : 437 440.
40. Harris JI (1964) The Structure and catalytic activity of thiol dehydrogenases. Structure and activity of enzymes (Goodwin TW, Harris JI Hartley BS, eds), pp. 97 109. Academic Press, New York.
41. Haurie V, Perrot M, Mini T, Jeno P, Sagliocco F Boucherie H (2001) The transcriptional activator Cat8p provides a major contribution to the reprogramming of carbon metabolism during the diauxic shift in Saccharomyces cerevisiae. J Biol Chem 276 : 76 85.
42. Heick HMC, Willemot J Begin-heick N (1969) The subcellular localization of alcohol dehydrogenase activity in baker's yeast. Biochim Biophys Acta 191 : 493 501.
43. Hope IA Struhl K (1985) GCN4 protein, synthesized in vitro, binds HIS3 regulatory sequences: implications for general control of amino acid biosynthetic genes in yeast. Cell 43 : 177 188.
44. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS O'Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425 : 686 691.
45. Irani M, Taylor WE Young ET (1987) Transcription of the ADH2 gene in Saccharomyces cerevisiae is limited by positive factors that bind competitively to its intact promoter region on multicopy plasmids. Mol Cell Biol 7 : 1233 1241.
46. Jornvall H (1977) The primary structure of yeast alcohol dehydrogenase. Eur J Biochem 72 : 425 442.
47. Jornvall H, Shafqat J Persson B (2001) Variations and constant patterns in eukaryotic MDR enzymes. Conclusions from novel structures and characterized genomes. Chem Biol Interact 130-132 : 491 498.
48. Kallberg Y, Oppermann U, Jornvall H Persson B (2002) Short-chain dehydrogenases/reductases (SDRs). Eur J Biochem 269 : 4409 4417.
49. Karlovic D, Amiguet P, Bonner FJ Luisi PL (1976) Spectroscopic investigation of binary and ternary coenzyme complexes of yeast alcohol dehydrogenase. Eur J Biochem 66 : 277 284.
50. Karnitz L, Morrison M Young ET (1992) Identification and characterization of three genes that affect expression of ADH2 in Saccharomyces cerevisiae. Genetics 132 : 351 359.
51. Ladriere JM, Georis I, Guerineau M Vandenhaute J (2000) Kluyveromyces marxianus exhibits an ancestral Saccharomyces cerevisiae genome organization downstream of ADH2. Gene 255 : 83 91.
52. Larroy C, Fernandez MR, Gonzalez E, Pares X Biosca JA (2002a) Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J 361 : 163 172.
53. Larroy C, Pares X Biosca JA (2002b) Characterization of a Saccharomyces cerevisiae NADP(H)-dependent alcohol dehydrogenase (ADHVII), a member of the cinnamyl alcohol dehydrogenase family. Eur J Biochem 269 : 5738 5745.
54. Larroy C, Rosario FM, Gonzalez E, Pares X Biosca JA (2003) Properties and functional significance of Saccharomyces cerevisiae ADHVI. Chem Biol Interact 143-144 : 229 238.
55. Leskovac V, Trivic S Anderson BM (1998) Use of competitive dead-end inhibitors to determine the chemical mechanism of action of yeast alcohol dehydrogenase. Mol Cell Biochem 178 : 219 227.
56. Leskovac V, Trivic S Pericin D (2002) The three zinc-containing alcohol dehydrogenases from baker's yeast, Saccharomyces cerevisiae. FEMS Yeast Res 2 : 481 494.
57. Liu HY, Chiang YC, Pan J, Chen J, Salvadore C, Audino DC, Badarinarayana V, Palaniswamy V, Anderson B Denis CL (2001) Characterization of CAF4 and CAF16 reveals a functional connection between the CCR4-NOT complex and a subset of SRB proteins of the RNA polymerase II holoenzyme. J Biol Chem 276 : 7541 7548.
58. Lutstorf U Megnet R (1968) Multiple forms of alcohol dehydrogenase in Saccharomyces cerevisiae. I. Physiological control of ADH-2 and properties of ADH-2 and ADH-4. Arch Biochem Biophys 126 : 933 944.
59. Magonet E, Hayen P, Delforge D, Delaive E Remacle J (1992) Importance of the structural zinc atom for the stability of yeast alcohol dehydrogenase. Biochem J 287 : 361 365.
60. Malvar T, Biron RW, Kaback DB Denis CL (1992) The CCR4 protein from Saccharomyces cerevisiae contains a leucine-rich repeat region which is required for its control of ADH2 gene expression. Genetics 132 : 951 962.
61. Mizuno A, Tabei H Iwahuti M (2006) Characterization of low-acetic acid-producing yeast isolated from 2-deoxyglucose-resistant mutants and its application to high-gravity brewing. J Biosci Bioeng 101 : 31 37.
62. Mooney DT, Pilgrim DB Young ET (1990) Mutant alcohol dehydrogenase (ADH III) presequences that affect both in vitro mitochondrial import and in vitro processing by the matrix protease. Mol Cell Biol 10 : 2801 2808.
63. Mortimer RK Schild D (1985) Genetic map of Saccharomyces cerevisiae, edition 9. Microbiol Rev 49 : 181 213.
64. Niederacher D Entian KD (1991) Characterization of Hex2 protein, a negative regulatory element necessary for glucose repression in yeast. Eur J Biochem 200 : 311 319.
65. O'Hara PJ, Horowitz H, Eichinger G Young ET (1988) The yeast ADR6 gene encodes homopolymeric amino acid sequences and a potential metal-binding domain. Nucleic Acids Res 16 : 10153 10169.
66. Overkamp KM, Bakker BM, Kotter P, van Tuijl A, de Vries S, van Dijken JP Pronk JT (2000) In vivo analysis of the mechanisms for oxidation of cytosolic NADH by Saccharomyces cerevisiae mitochondria. J Bacteriol 182 : 2823 2830.
67. Paquin CE Williamson VM (1986) Ty insertions at two loci account for most of the spontaneous antimycin A resistance mutations during growth at 15 degrees C of Saccharomyces cerevisiae strains lacking ADH1. Mol Cell Biol 6 : 70 79.
68. Persson B, Hallborn J, Walfridsson M, Hahn-Hagerdal B, Keranen S, Penttila M Jornvall H (1993) Dual relationships of xylitol and alcohol dehydrogenases in families of two protein types. FEBS Lett 324 : 9 14.
69. Petersson A, Almeida JRM, Modig T, Karhumaa K, Hahn-Hägerdal B, Gorwa-Grauslund MF Lidén G (2006) A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23 : 455 464.
70. Pilgrim D Young ET (1987) Primary structure requirements for correct sorting of the yeast mitochondrial protein ADH III to the yeast mitochondrial matrix space. Mol Cell Biol 7 : 294 304.
71. Reid MF Fewson CA (1994) Molecular characterization of microbial alcohol dehydrogenases. Crit Rev Microbiol 20 : 13 56.
72. Rossman MG, Liljas A, Branden CI Banaszak LJ (1975) The enzymes (Boyer P, ed), pp. 61 102. Academic Press, New York.
73. Ruohonen L, Aalto MK Keranen S (1995) Modifications to the ADH1 promoter of Saccharomyces cerevisiae for efficient production of heterologous proteins. J Biotechnol 39 : 193 203.
74. Russell DW, Smith M, Cox D, Williamson VM Young ET (1983a) DNA sequences of two yeast promoter-up mutants. Nature 304 : 652 654.
75. Russell DW, Smith M, Williamson VM Young ET (1983b) Nucleotide sequence of the yeast alcohol dehydrogenase II gene. J Biol Chem 258 : 2674 2682.
76. Santangelo GM Tornow J (1990) Efficient transcription of the glycolytic gene ADH1 and three translational component genes requires the GCR1 product, which can act through TUF/GRF/RAP binding sites. Mol Cell Biol 10 : 859 862.
77. Schopp W Aurich H (1976) Kinetics and reaction mechanism of yeast alcohol dehydrogenase with long-chain primary alcohols. Biochem J 157 : 15 22.
78. Sledziewski A Young ET (1982) Chromatin conformational changes accompany transcriptional activation of a glucose-repressed gene in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 79 : 253 256.
79. Sonderegger M, Jeppsson M, Hahn-Hägerdal B Sauer U (2004) Molecular basis for anaerobic growth of Saccharomyces cerevisiae on xylose, investigated by global gene expression and metabolic flux analysis. Appl Environ Microbiol 70 : 2307 2317.
80. Tachibana C, Yoo JY, Tagne JB, Kacherovsky N, Lee TI Young ET (2005) Combined global localization analysis and transcriptome data identify genes that are directly coregulated by Adr1 and Cat8. Mol Cell Biol 25 : 2138 2146.
81. Taguchi AK Young ET (1987) The identification and characterization of ADR6, a gene required for sporulation and for expression of the alcohol dehydrogenase II isozyme from Saccharomyces cerevisiae. Genetics 116 : 523 530.
82. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP Benner SA (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37 : 630 635.
83. Thukral SK, Eisen A Young ET (1991) Two monomers of yeast transcription factor ADR1 bind a palindromic sequence symmetrically to activate ADH2 expression. Mol Cell Biol 11 : 1566 1577.
84. Valencia E, Rosell A, Larroy C, Farres J, Biosca JA, Fita I, Pares X Ochoa WF (2003) Crystallization and preliminary X-ray analysis of NADP(H)-dependent alcohol dehydrogenases from Saccharomyces cerevisiae and Rana perezi. Acta Crystallogr D Biol Crystallogr 59 : 334 337.
85. Valencia E, Larroy C, Ochoa WF, Pares X, Fita I Biosca JA (2004) Apo and Holo structures of an NADPH-dependent cinnamyl alcohol dehydrogenase from Saccharomyces cerevisiae. J Mol Biol 341 : 1049 1062.
86. Vallee BL Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73 : 79 118.
87. van Iersel MF, Eppink MH, van Berkel WJ, Rombouts FM Abee T (1997) Purification and characterization of a novel NADP-dependent branched-chain alcohol dehydrogenase from Saccharomyces cerevisiae. Appl Environ Microbiol 63 : 4079 4082.
88. van Loon AP Young ET (1986) Intracellular sorting of alcohol dehydrogenase isoenzymes in yeast: a cytosolic location reflects absence of an amino-terminal targeting sequence for the mitochondrion. EMBO J 5 : 161 165.
89. Verdone L, Cesari F, Denis CL, Di Mauro E Caserta M (1997) Factors affecting Saccharomyces cerevisiae ADH2 chromatin remodelling and transcription. J Biol Chem 272 : 30828 30834.
90. Verdone L, Wu J, Van Riper K, Kacherovsky N, Vogelauer M, Young ET, Grunstein M, Di Mauro E Caserta M (2002) Hyperacetylation of chromatin at the ADH2 promoter allows Adr1 to bind in repressed conditions. EMBO J 21 : 1101 1111.
91. Voronkova V, Kacherovsky N, Tachibana C, Yu D Young ET (2006) Snf1-dependent and Snf1-independent pathways of constitutive ADH2 expression in Saccharomyces cerevisiae. Genetics 172 : 2123 2138.
92. Walther K Schuller HJ (2001) Adr1 and Cat8 synergistically activate the glucose-regulated alcohol dehydrogenase gene ADH2 of the yeast Saccharomyces cerevisiae. Microbiol 147 : 2037 2044.
93. Walton JD, Paquin CE, Kaneko K Williamson VM (1986) Resistance to antimycin A in yeast by amplification of ADH4 on a linear, 42 kb palindromic plasmid. Cell 46 : 857 863.
94. Wehner EP, Rao E Brendel M (1993) Molecular structure and genetic regulation of SFA, a gene responsible for resistance to formaldehyde in Saccharomyces cerevisiae, and characterization of its protein product. Mol Gen Genet 237 : 351 358.
95. Wenger JI Bernofsky C (1971) Mitochondrial alcohol dehydrogenase from Saccharomyces cerevisiae. Biochim Biophys Acta 227 : 479 490.
96. Wiesenfeld M, Schimpfessel L Crokaert R (1975) Multiple forms of mitochondrial alcohol dehydrogenase in Saccharomyces cerevisiae. Biochim Biophys Acta 405 : 500 512.
97. Williamson VM Paquin CE (1987) Homology of Saccharomyces cerevisiae ADH4 to an iron-activated alcohol dehydrogenase from Zymomonas mobilis. Mol Gen Genet 209 : 374 381.
98. Williamson VM, Bennetzen J, Young ET, Nasmyth K Hall BD (1980) Isolation of the structural gene for alcohol dehydrogenase by genetic complementation in yeast. Nature 283 : 214 216.
99. Williamson VM, Young ET Ciriacy M (1981) Transposable elements associated with constitutive expression of yeast alcohol dehydrogenase II. Cell 23 : 605 614.
100. Wills C (1976) Production of yeast alcohol dehydrogenase isoenzymes by selection. Nature 261 : 26 29.
101. Wills C, Kratofil P Martin T (1982) Functional mutants of yeast alcohol dehydrogenase. Basic Life Sci 19 : 305 329.
102. Xella B, Goding C, Agricola E, Di Mauro E Caserta M (2006) The ISWI and CHD1 chromatin remodelling activities influence ADH2 expression and chromatin organization. Mol Microbiol 59 : 1531 1541.
103. Young ET Pilgrim D (1985) Isolation and DNA sequence of ADH3, a nuclear gene encoding the mitochondrial isozyme of alcohol dehydrogenase in Saccharomyces cerevisiae. Mol Cell Biol 5 : 3024 3034.
104. Yu J, Donoviel MS Young ET (1989) Adjacent upstream activation sequence elements synergistically regulate transcription of ADH2 in Saccharomyces cerevisiae. Mol Cell Biol 9 : 34 42.
105. Yu W, Macreadie IG Winge DR (1991) Protection against cadmium toxicity in yeast by alcohol dehydrogenase. J Inorg Biochem 44 : 155 161.
106. Yuan DS (2000) Zinc-regulated genes in Saccharomyces cerevisiae revealed by transposon tagging. Genetics 156 : 45 58.
107. Zhang W, Needham DL, Coffin M, Rooker A, Hurban P, Tanzer MM Shuster JR (2003) Microarray analyses of the metabolic responses of Saccharomyces cerevisiae to organic solvent dimethyl sulfoxide. J Ind Microbiol Biotechnol 30 : 57 69.