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References

  1. Wong CM, Siu KL, Jin DY. 2004. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279: 23207-23213.
  2. Wan XY, Zhou Y, Yan ZY, Wang HL, Hou YD, Jin DY. 1997. Scav engase p 20: a n ovel f amily of b acterial a ntioxidant enzymes. FEBS Lett. 407: 32-36.
  3. Hall A, Nelson K, Poole LB, Karplus PA. 2011. Structurebased insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 15: 795815.
  4. Dietz KJ. 2003. Plant peroxiredoxins. Annu. Rev. Plant Biol. 54: 93-107.
  5. Park SG, Cha MK, Jeong W, Kim IH. 2000. Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275: 5723-5732.
  6. Rhee SG. 2016. Overview on peroxiredoxin. Mol. Cells 39: 1-5.
  7. Latimer HR, Veal EA. 2016. Peroxiredoxins in regulation of MAPK signalling pathways; sensors and barriers to signal transduction. Mol. Cells 39: 40-45.
  8. Netto LES, Antunes F. 2016. The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction. Mol. Cells 39: 65-71.
  9. Perkins A, Nelson KJ, Parsonage D, Poole LB, Karplus PA. 2015. Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40:435-445.
  10. Ralat LA, Manevich Y, Fisher AB, Colman RF. 2006. Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase pi with activity changes in both enzymes. Biochemistry 45: 360-372.
  11. Manevich Y, Feinstein SI, Fisher AB. 2004. Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. USA 101: 3780-3785.
  12. Wood ZA, Schroder E, Robin Harris J, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28: 32-40.
  13. Lian FM, Yu J, Ma XX, Yu XJ, Chen YX, Zhou CZ. 2012. Structural snapshots of yeast alkyl hydroperoxide reductase Ahp1 peroxiredoxin reveal a novel two-cysteine mechanism of electron transfer to eliminate reactive oxygen species. J. Biol. Chem. 287: 17077-17087.
  14. Rhee SG, Kang SW, Chang TS, Jeong W, Kim K. 2001. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52: 35-41.
  15. Lu J, Holmgren A. 2014. The thioredoxin antioxidant system. Free Radic. Biol. Med. 66: 75-87.
  16. Thon M, Al-Abdallah Q, Hortschansky P, Brakhage AA. 2007. The thioredoxin system of the filamentous fungus Aspergillus nidulans - impact on development and oxidative stress response. J. Biol. Chem. 282: 27259-27269.
  17. Yang KS, Kang SW, Woo HA, Hwang SC, Chae HZ, Kim K, et al. 2002. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277: 3802938036.
  18. Chae HZ, Chung SJ, Rhee SG. 1994. Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 269: 27670-27678.
  19. Konig J, Galliardt H, Jutte P, Schaper S, Dittmann L, Dietz KJ. 2013. The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. J. Exp. Bot. 64: 3483-3497.
  20. Peskin AV, Dickerhof N, Poynton RA, Paton LN, Pace PE, Hampton MB, et al. 2013. Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine. J. Biol. Chem. 288: 14170-14177.
  21. Haynes AC, Qian J, Reisz JA, Furdui CM, Lowther WT. 2013. Molecular basis for the resistance of human mitochondrial 2-Cys peroxiredoxin 3 to hyperoxidation. J. Biol. Chem. 288:29714-29723.
  22. Cox AG, Pearson AG, Pullar JM, Jonsson TJ, Lowther WT, Winterbourn CC, et al. 2009. Mitochondrial peroxiredoxin 3 is more resilient to hyperoxidation than cytoplasmic
  23. Salsbury FR, Knutson ST, Poole LB, Fetrow JS. 2008. Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid. Protein Sci. 17: 299-312.
  24. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653.
  25. Sun QA, Wu YL, Zappacosta F, Jeang KT, Lee BJ, Hatfield DL, et al. 1999. Redox regulation of cell signaling by selenocysteine in mammalian thioredoxin reductases. J. Biol. Chem. 274:24522-24530.
  26. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. 2007. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8: 722-728.
  27. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. USA 104: 11772-11777.
  28. Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J. 2008. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot. Cell 7: 1352-1361.
  29. Vargas-Perez I, Sanchez O, Kawasaki L, Georgellis D, Aguirre J. 2007. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryot. Cell 6: 1570-1583.
  30. Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, Diamond RD, et al. 2003. Catalases of Aspergillus fumigatus. Infect. Immun. 71: 3551-3562.
  31. Hillmann F, Bagramyan K, Strassburger M, Heinekamp T, Hong TB, Bzymek KP, et al. 2016. The crystal structure of peroxiredoxin Asp f3 provides mechanistic insight into oxidative stress resistance and virulence of Aspergillus fumigatus. Sci. Rep. 6: 33996.
  32. Thon M, Al Abdallah Q, Hortschansky P, Scharf DH, Eisendle M, Haas H, et al. 2010. The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Res. 38: 1098-1113.
  33. Zhou SM, Narukami T, Nameki M, Ozawa T, Kamimura Y, Hoshino T, et al. 2012. Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl. Environ. Microbiol. 78: 103-109.
  34. Zhou Y, Zhou SM, Yu HJ, Li JY, Xia Y, Li BY, et al. 2016. Cloning and characterization of filamentous fungal Snitrosoglutathione reductase from Aspergillus nidulans. J. Microbiol. Biotechnol. 26: 928-937.
  35. Zhou SM, Narukami T, Masuo S, Shimizu M, Fujita T, Doi Y, et al. 2013. NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin. Nat. Chem. Biol. 9: 657-663.
  36. Takasaki K, Shoun H, Yamaguchi M, Takeo K, Nakamura A, Hoshino T, et al. 2004. Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol role of acetyl CoA synthetase in anaerobic ATP synthesis. J. Biol. Chem. 279: 12414-12420.
  37. Nakamura T, Kado Y, Yamaguchi T, Matsumura H, Ishikawa K, Inoue T. 2010. Crystal structure of peroxiredoxin from Aeropyrum pernix K1 complexed with its substrate, hydrogen peroxide. J. Biochem. 147: 109-115.
  38. Kang SW, Baines IC, Rhee SG. 1998. Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J. Biol. Chem. 273: 6303-6311.
  39. Prouzet-Mauleon V, Monribot-Espagne C, Boucherie H, Lagniel G, Lopez S, Labarre J, et al. 2002. Identification in Saccharomyces cerevisiae of a new stable variant of alkyl hydroperoxide reductase 1 (Ahp1) induced by oxidative stress. J. Biol. Chem. 277: 4823-4830.
  40. Chauhan N, Latge JP, Calderone R. 2006. Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat. Rev. Microbiol. 4: 435-444.
  41. Li Q, Bai Z, O’Donnell A, Harvey LM, Hoskisson PA, McNeil B. 2011. Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol. Lett. 33: 457-467.
  42. Paulo E, Garcia-Santamarina S, Calvo IA, Carmona M, Boronat S, Domenech A, et al. 2014. A genetic approach to study H2O2 scavenging in fission yeast - distinct roles of peroxiredoxin and catalase. Mol. Microbiol. 92: 246-257.
  43. Michan S, Lledias F, Baldwin JD, Natvig DO, Hansberg W. 2002. Regulation and oxidation of two large monofunctional catalases. Free Radic. Biol. Med. 33: 521-532.
  44. Michiels C, Raes M, Toussaint O, Remacle J. 1994. Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic. Biol. Med. 17: 235-248.
  45. Lee J, Spector D, Godon C, Labarre J, Toledano MB. 1999. A new antioxidant with alkyl hydroperoxide defense properties in yeast. J. Biol. Chem. 274: 4537-4544.
  46. Jeong JS, Kwon SJ, Kang SW, Rhee SG, Kim K. 1999. Purification and characterization of a second type thioredoxin peroxidase (type II TPx) from Saccharomyces cerevisiae. Biochemistry 38: 776-783.
  47. Stadtman ER. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metalcatalyzed reactions. Annu. Rev. Biochem. 62: 797-821.
  48. Becker K, Gromer S, Schirmer RH, Muller S. 2000. Thioredoxin reductase as a pathophysiological factor and drug target. Eur. J. Biochem. 267: 6118-6125.

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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(1): 145-156

Published online January 28, 2018 https://doi.org/10.4014/jmb.1707.07024

Copyright © The Korean Society for Microbiology and Biotechnology.

Peroxiredoxin System of Aspergillus nidulans Resists Inactivation by High Concentration of Hydrogen Peroxide-Mediated Oxidative Stress

Yang Xia 1, Haijun Yu 1, Zhemin zhou 2, Naoki Takaya 3, Shengmin Zhou 1* and Ping Wang 1

1State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology, Shanghai 200237, P.R. China, 2School of Biotechnology, Jiangnan University, Wuxi, Jiangsu 214122, P.R. China, 3Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-0006, Japan

Correspondence to:Shengmin  Zhou
zhoushengmin@ecust.edu.cn

Received: July 12, 2017; Accepted: October 30, 2017

Abstract

Most eukaryotic peroxiredoxins (Prxs) are readily inactivated by a high concentration of hydrogen peroxide (H2O2) during catalysis owing to their “GGLG” and “YF” motifs. However, such oxidative stress sensitive motifs were not found in the previously identified filamentous fungal Prxs. Additionally, the information on filamentous fungal Prxs is limited and fragmentary. Herein, we cloned and gained insight into Aspergillus nidulans Prx (An.PrxA) in the aspects of protein properties, catalysis characteristics, and especially H2O2 tolerability. Our results indicated that An.PrxA belongs to the newly defined family of typical 2-Cys Prxs with a marked characteristic that the “resolving” cysteine (CR) is invertedly located preceding the “peroxidatic” cysteine (CP) in amino acid sequences. The inverted arrangement of CR and CP can only be found among some yeast, bacterial, and filamentous fungal deduced Prxs. The most surprising characteristic of An.PrxA is its extraordinary ability to resist inactivation by extremely high concentrations of H2O2, even that approaching 600 mM. By screening the H2O2- inactivation effects on the components of Prx systems, including Trx, Trx reductase (TrxR), and Prx, we ultimately determined that it is the robust filamentous fungal TrxR rather than Trx and Prx that is responsible for the extreme H2O2 tolerence of the An.PrxA system. This is the first investigation on the effect of the electron donor partner in the H2O2 tolerability of the Prx system.

Keywords: Peroxiredoxin, filamentous fungus, thioredoxin, thioredoxin reductase, oxidative stress, hydrogen peroxide

References

  1. Wong CM, Siu KL, Jin DY. 2004. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279: 23207-23213.
  2. Wan XY, Zhou Y, Yan ZY, Wang HL, Hou YD, Jin DY. 1997. Scav engase p 20: a n ovel f amily of b acterial a ntioxidant enzymes. FEBS Lett. 407: 32-36.
  3. Hall A, Nelson K, Poole LB, Karplus PA. 2011. Structurebased insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 15: 795815.
  4. Dietz KJ. 2003. Plant peroxiredoxins. Annu. Rev. Plant Biol. 54: 93-107.
  5. Park SG, Cha MK, Jeong W, Kim IH. 2000. Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275: 5723-5732.
  6. Rhee SG. 2016. Overview on peroxiredoxin. Mol. Cells 39: 1-5.
  7. Latimer HR, Veal EA. 2016. Peroxiredoxins in regulation of MAPK signalling pathways; sensors and barriers to signal transduction. Mol. Cells 39: 40-45.
  8. Netto LES, Antunes F. 2016. The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction. Mol. Cells 39: 65-71.
  9. Perkins A, Nelson KJ, Parsonage D, Poole LB, Karplus PA. 2015. Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40:435-445.
  10. Ralat LA, Manevich Y, Fisher AB, Colman RF. 2006. Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase pi with activity changes in both enzymes. Biochemistry 45: 360-372.
  11. Manevich Y, Feinstein SI, Fisher AB. 2004. Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. USA 101: 3780-3785.
  12. Wood ZA, Schroder E, Robin Harris J, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28: 32-40.
  13. Lian FM, Yu J, Ma XX, Yu XJ, Chen YX, Zhou CZ. 2012. Structural snapshots of yeast alkyl hydroperoxide reductase Ahp1 peroxiredoxin reveal a novel two-cysteine mechanism of electron transfer to eliminate reactive oxygen species. J. Biol. Chem. 287: 17077-17087.
  14. Rhee SG, Kang SW, Chang TS, Jeong W, Kim K. 2001. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52: 35-41.
  15. Lu J, Holmgren A. 2014. The thioredoxin antioxidant system. Free Radic. Biol. Med. 66: 75-87.
  16. Thon M, Al-Abdallah Q, Hortschansky P, Brakhage AA. 2007. The thioredoxin system of the filamentous fungus Aspergillus nidulans - impact on development and oxidative stress response. J. Biol. Chem. 282: 27259-27269.
  17. Yang KS, Kang SW, Woo HA, Hwang SC, Chae HZ, Kim K, et al. 2002. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277: 3802938036.
  18. Chae HZ, Chung SJ, Rhee SG. 1994. Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 269: 27670-27678.
  19. Konig J, Galliardt H, Jutte P, Schaper S, Dittmann L, Dietz KJ. 2013. The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. J. Exp. Bot. 64: 3483-3497.
  20. Peskin AV, Dickerhof N, Poynton RA, Paton LN, Pace PE, Hampton MB, et al. 2013. Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine. J. Biol. Chem. 288: 14170-14177.
  21. Haynes AC, Qian J, Reisz JA, Furdui CM, Lowther WT. 2013. Molecular basis for the resistance of human mitochondrial 2-Cys peroxiredoxin 3 to hyperoxidation. J. Biol. Chem. 288:29714-29723.
  22. Cox AG, Pearson AG, Pullar JM, Jonsson TJ, Lowther WT, Winterbourn CC, et al. 2009. Mitochondrial peroxiredoxin 3 is more resilient to hyperoxidation than cytoplasmic
  23. Salsbury FR, Knutson ST, Poole LB, Fetrow JS. 2008. Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid. Protein Sci. 17: 299-312.
  24. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653.
  25. Sun QA, Wu YL, Zappacosta F, Jeang KT, Lee BJ, Hatfield DL, et al. 1999. Redox regulation of cell signaling by selenocysteine in mammalian thioredoxin reductases. J. Biol. Chem. 274:24522-24530.
  26. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. 2007. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8: 722-728.
  27. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. USA 104: 11772-11777.
  28. Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J. 2008. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot. Cell 7: 1352-1361.
  29. Vargas-Perez I, Sanchez O, Kawasaki L, Georgellis D, Aguirre J. 2007. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryot. Cell 6: 1570-1583.
  30. Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, Diamond RD, et al. 2003. Catalases of Aspergillus fumigatus. Infect. Immun. 71: 3551-3562.
  31. Hillmann F, Bagramyan K, Strassburger M, Heinekamp T, Hong TB, Bzymek KP, et al. 2016. The crystal structure of peroxiredoxin Asp f3 provides mechanistic insight into oxidative stress resistance and virulence of Aspergillus fumigatus. Sci. Rep. 6: 33996.
  32. Thon M, Al Abdallah Q, Hortschansky P, Scharf DH, Eisendle M, Haas H, et al. 2010. The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Res. 38: 1098-1113.
  33. Zhou SM, Narukami T, Nameki M, Ozawa T, Kamimura Y, Hoshino T, et al. 2012. Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl. Environ. Microbiol. 78: 103-109.
  34. Zhou Y, Zhou SM, Yu HJ, Li JY, Xia Y, Li BY, et al. 2016. Cloning and characterization of filamentous fungal Snitrosoglutathione reductase from Aspergillus nidulans. J. Microbiol. Biotechnol. 26: 928-937.
  35. Zhou SM, Narukami T, Masuo S, Shimizu M, Fujita T, Doi Y, et al. 2013. NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin. Nat. Chem. Biol. 9: 657-663.
  36. Takasaki K, Shoun H, Yamaguchi M, Takeo K, Nakamura A, Hoshino T, et al. 2004. Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol role of acetyl CoA synthetase in anaerobic ATP synthesis. J. Biol. Chem. 279: 12414-12420.
  37. Nakamura T, Kado Y, Yamaguchi T, Matsumura H, Ishikawa K, Inoue T. 2010. Crystal structure of peroxiredoxin from Aeropyrum pernix K1 complexed with its substrate, hydrogen peroxide. J. Biochem. 147: 109-115.
  38. Kang SW, Baines IC, Rhee SG. 1998. Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J. Biol. Chem. 273: 6303-6311.
  39. Prouzet-Mauleon V, Monribot-Espagne C, Boucherie H, Lagniel G, Lopez S, Labarre J, et al. 2002. Identification in Saccharomyces cerevisiae of a new stable variant of alkyl hydroperoxide reductase 1 (Ahp1) induced by oxidative stress. J. Biol. Chem. 277: 4823-4830.
  40. Chauhan N, Latge JP, Calderone R. 2006. Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat. Rev. Microbiol. 4: 435-444.
  41. Li Q, Bai Z, O’Donnell A, Harvey LM, Hoskisson PA, McNeil B. 2011. Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol. Lett. 33: 457-467.
  42. Paulo E, Garcia-Santamarina S, Calvo IA, Carmona M, Boronat S, Domenech A, et al. 2014. A genetic approach to study H2O2 scavenging in fission yeast - distinct roles of peroxiredoxin and catalase. Mol. Microbiol. 92: 246-257.
  43. Michan S, Lledias F, Baldwin JD, Natvig DO, Hansberg W. 2002. Regulation and oxidation of two large monofunctional catalases. Free Radic. Biol. Med. 33: 521-532.
  44. Michiels C, Raes M, Toussaint O, Remacle J. 1994. Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic. Biol. Med. 17: 235-248.
  45. Lee J, Spector D, Godon C, Labarre J, Toledano MB. 1999. A new antioxidant with alkyl hydroperoxide defense properties in yeast. J. Biol. Chem. 274: 4537-4544.
  46. Jeong JS, Kwon SJ, Kang SW, Rhee SG, Kim K. 1999. Purification and characterization of a second type thioredoxin peroxidase (type II TPx) from Saccharomyces cerevisiae. Biochemistry 38: 776-783.
  47. Stadtman ER. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metalcatalyzed reactions. Annu. Rev. Biochem. 62: 797-821.
  48. Becker K, Gromer S, Schirmer RH, Muller S. 2000. Thioredoxin reductase as a pathophysiological factor and drug target. Eur. J. Biochem. 267: 6118-6125.