Abstract
The genome of fission yeast Schizosaccharomyces pombe harbors two genes for thioredoxins, trx1 + and trx2 +, which encode cytosolic and mitochondrial thioredoxins, respectively. The Δtrx1 mutant was found sensitive to diverse external stressors such as various oxidants, heat, and salt, whereas Δtrx2 mutant was not sensitive except to paraquat, a superoxide generator. Both Δtrx1 and Δtrx2 mutants were more resistant to diamide, a thiol-specific oxidant, than the wild type. The trx1 + gene expression was induced by H2O2 and menadione, being mediated through a stress-responsive transcription factor Papl. In Δtrx1 cells, the basal expression of Pap1-regulated genes were elevated, suggesting a role for Trxl as a reducer for oxidized (activated) Papl. The Δtrx1 mutant exhibited cysteine auxotrophy, which can be overcome by adding sulfite. This suggests that Trxl serves as a primary electron donor for 3′-phosphoadenosine-5′-phosphosulfate (PAPS) reductase and thus is an essential protein for sulfur assimilation in S. pombe. These results suggest that, in contrast to Trx2 whose role is more confined to mitochondrial functions, Trxl plays a major role in protecting S. pombe against various stressful conditions and enables proper sulfur metabolism.
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References
Alfa, C., P. Fantes, J. Hyams, M. Mcleod, and E. Warbrick. 1993. Experiments with fission yeast: a laboratory course manual. Cold Spring Harbor Laboratory Press, New York, N.Y., USA.
Bozonet, S., V. Findlay, A. Day, J. Cameron, E. Veal, and B. Morgan. 2005. Oxidation of a eukaryotic 2-cys proxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide. J. Biol. Chem. 280, 23319–23327.
Carmel-Harel, O. and G. Storz. 2000. Roles of the glutathione-and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 54, 439–461.
Delaunay, A., D. Pflieger, M. Barrault, J. Vinh, and M.B. Toledano. 2002. A thiol peroxide is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471–481.
Fujii, Y., T. Simizu, T. Toda, M. Yanagida, and T. Hakoshima. 2000. Structural basis for the diversity of DNA recognition by bZIP transcription factors. Nat. Struct. Biol. 7, 889–893.
Greenberg, J.T. and B. Demple. 1986. Glutathione in Escherichia coli is dispensable for resistance to H2O2 and gamma radiation. J. Bacteriol. 168, 1026–1029.
Herrero, E. and J. Ros. 2002. Glutaredoxins and oxidative stress defense in yeast. Methods Enzymol. 348, 136–146.
Hirota, K., M. Murata, Y. Sachi, H. Nakamura, J. Takeuchi, K. Mori, and J. Yodoi. 1999. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-κB. J. Biol. Chem. 274, 27891–27897.
Holmgren, A. 1984. Enzymatic reduction-oxidation of protein disulfides by thioredoxin. Methods Enzymol. 107, 295–300.
Izawa, S., K. Maeda, K. Sugiyama, J. Mano, and Y. Inoue. 1999. Thioredoxin deficiency causes the constitutive activation of Yap1, an AP-1-like transcription factor in Saccharomyces cerevisiae. J. Biol. Chem. 274, 28459–28465.
Jara, M., A.P. Vivancos, I.A. Calvo, A. Moldon, M. Sanso, and E. Hidalgo. 2007. The peroxiredoxin Tpx1 is essential as a H2O2 scavenger during aerobic growth in fission yeast. Mol. Biol. Cell. 18, 2288–2295.
Kang, H.J., S.M. Hong, B.C. Kim, K. Kim, E.H. Park, and C.J. Lim. 2006. Transcriptional analysis and Pap1-dependence of the unique gene encoding thioredoxin reductase from fission yeast. J. Microbiol. 44, 35–41.
Kim, S.J., E.M. Jung, H.J. Jung, Y.S. Song, E.H. Park, and C.J. Lim. 2007. Celluar functions and transcriptional regulation of a third thioredoxin from Schizosaccharomyces pombe. Can. J. Microbiol. 53, 775–783.
Kudo, N., H. Taoka, T. Toda, M. Yoshida, and S. Horinouchi. 1999. A novel nuclear export signal sensitive to oxidative stress in the fission yeast transcription factor Pap1. J. Biol. Chem. 274, 15151–15158.
Kuge, S., M. Arita, A. Murayama, K. Maeta, S. Izawa, Y. Inoue, and A. Nomoto. 2001. Regulation of the yeast Yap1p nuclear export signal is mediated by redox signal-induced reversible disulfide bond formation. Mol. Cell. Biol. 21, 6139–6150.
Lee, J., I.W. Dawes, and J.H. Roe. 1995. Adaptive response of Schizosaccharomyces pombe to hydrogen peroxide and menadione. Microbiology 141, 3127–3132.
Lee, J., I.W. Dawes, and J.H. Roe. 1997. Isolation, expression, and regulation of the pgr1 + gene encoding glutathione reductase absolutely required for the growth of Schizosaccharomyces pombe. J. Biol. Chem. 272, 23042–23049.
Masutani, H. and J. Yodoi. 2002. Thioredoxin. Methods Enzymol. 347, 279–286.
Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795–823.
Muller, E.G. 1996. A glutathione reductase mutant of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol. Biol. Cell. 7, 1805–1813.
Nakagawa, C.W., K. Yamada, and N. Mutoh. 2000. Role of Atf1 and Pap1 in the induction of the catalase gene of fission yeast Schizosaccharomyces pombe. J. Biochem. (Tokyo) 127, 233–238.
Okamoto, T., K. Asamitsu, and T. Tetsuka. 2002. Thioredoxin and mechanism of inflammatory response. Methods Enzymol. 347, 349–360.
Pedrajas, J.R., E. Kosmidou, A. Miranda-Vizuete, J.A. Gustafsson, A.P. Wright, and G. Spyrou. 1999. Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J. Biol. Chem. 274, 6366–6373.
Quinn, J., V.J. Findlay, K. Dawson, J.B.A. Miller, N. Jones, B.A. Morgan, and W.M. Toone. 2002. Distinct regulatory protein control the graded transcriptional response to increase H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell 13, 805–816.
Russel, M. and A. Holmgren. 1988. Construction and characterization of glutaredoxin-negative mutants of Escherichia coli. Proc. Natl. Acad. Sci. USA 85, 990–994.
Russel, M., P. Model, and A. Holmgern. 1990. Thioredoxin or glutaredoxin in Escherichia coli is essential for sulfate reductase but not for deoxyribonucleotide synthesis. J. Bacteriol. 172, 1923–1929.
Saitoh, M., H. Nishitoh, M. Fujii, K. Takeda, K. Tobiume, Y. Sawada, M. Kawabata, K. Miyazono, and H. Ichijo. 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596–2606.
Schmitt, M.E., T.A. Brown, and B.L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18, 3091–3092.
Song, J.Y. 2006. The role of glutathione reductase and thioredoxin in the fission yeast Schizosaccharomyces pombe. Ph. D. thesis, Seoul National University, Seoul, Korea.
Song, J.Y., J. Cha, J. Lee, and J.H. Roe. 2006. Glutathione reductase and a mitochondrial thioredoxin play an overlapping role for maintaining iron-sulfur enzymes in fission yeast. Eukaryot. Cell. 5, 1857–1865.
Toone, W.M. and N. Jones. 1998. Stress-activated signalling pathways in yeast. Genes Cells 3, 485–498.
Tuggle, C.K. and J.A. Fuchs. 1985. Glutathione reductase is not required for maintenance of reduced glutathione in Escherichia coli K-12. J. Bacteriol. 162, 448–450.
Vivancos, A., E. Castillo, E. Biteau, C. Nicot, J. Ayté, M. Toledano, and E. Hidalgo. 2005. A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc. Natl. Acad. Sci. USA 102, 8875–8880.
Vlamis-Gardikas, A. and A. Holmgren. 2002 Thioredoxin and glutaredoxin isoforms. Methods Enzymol. 347, 286–296.
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Song, JY., Roe, JH. The role and regulation of Trxl, a cytosolic thioredoxin in Schizosaccharomyces pombe . J Microbiol. 46, 408–414 (2008). https://doi.org/10.1007/s12275-008-0076-4
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DOI: https://doi.org/10.1007/s12275-008-0076-4