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Characterization of several members of the thiol oxidoreductase family

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Abstract

There is no doubt as to the important role that free radicals and reactive oxygen species play in the cell. Disturbances in intracellular redox proteins are often accompanied by common pathologies, including diabetes, myocardial infarction, neurodegeneration, bronchopulmonary diseases, cancer, etc. Numerous antioxidant enzymes are related to various redox biology systems, the thiol oxidoreductase superfamily playing a key role. The superfamily includes thioredoxin, glutaredoxin, peroxiredoxin, protein disulfide isomerase, and glutathione peroxidase families and a number of other proteins. Apart from their antioxidant function, thiol oxidoreductases are capable of recycling hydroperoxyde to produce specific disulfide bonds within and between proteins, which significantly expands their functional range. In view of this, it is a topical problem of redox biology to characterize the superfamily members biochemically and to study their functional mechanisms.

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Abbreviations

AhpC:

alkyl hydroperoxyreductase

Cys:

cysteine

GSH:

reduced glutathione

GSSG:

oxidized glutathione

GPx:

glutathione peroxidase

Grx:

glutathione reductase

GST:

glutathione S-transferase

NPHGPx:

nonselenium phospholipid hydroperoxide glutathione peroxidase

NS-GPx:

nonselenium glutathione peroxidase

PHGPx:

phospholipid hydroperoxide glutathione peroxidase

Prx:

peroxiredoxin

ROS:

reactive oxygen species

Sec:

selenocysteine

Tpx:

thiol peroxidase

References

  1. Eklund H., Cambillau C., Sjöberg B.M., Holmgren A., Jöbnvall H., Höög J.O., Brändén C.I. 1984. Conformational and functional similarities between glutaredoxin and thioredoxins. EMBO J. 3, 1443–1449

    PubMed  CAS  Google Scholar 

  2. Arnér E.S., Holmgren A. 2000. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102–6109.

    Article  PubMed  Google Scholar 

  3. Qi Y., Grishin N.V. 2005. Structural classification of thioredoxin-like fold proteins. Proteins. 58, 376–388.

    Article  PubMed  CAS  Google Scholar 

  4. Holmgren A., Soderberg B.O., Eklund H., Branden C.I. 1975. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.7 Proc. Natl. Acad. Sci. U. S. A. 72, 2305–2309.

    Article  PubMed  CAS  Google Scholar 

  5. Katti S.K., LeMaster D.M., Eklund H. 1990. Crystal structure of thioredoxin from Escherichia coil at 1.68 Å resolution. J. Mol. Biol. 212, 167–184.

    Article  PubMed  CAS  Google Scholar 

  6. Bushweller J.H., Billeter M., Holmgren A., Wuthrich K. 1994. The nuclear magnetic resonance solution structure of the mixed disulfide between Escherichia coli glutaredoxin (C14S) and glutathione. J. Mol. Biol. 235, 1585–1597.

    Article  PubMed  CAS  Google Scholar 

  7. Eklund H., Ingelman M., Söberberg B.O., Uhlin T., Nordlund P., Nikkola M., Sonnerstam U., Joelson T., Petratos K. 1992. Structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin): refinement of native and mutant proteins. J. Mol. Biol. 228, 596–618.

    Article  PubMed  CAS  Google Scholar 

  8. Sodano P., Xia T.H., Bushweller J.H., Björnberg O., Holmgren A., Billeter M., Wüthrich K. 1991. Sequence specific 1H NMR assignments and determination of the three-dimensional structure of reduced Escherichia coli glutaredoxin. J. Mol. Biol. 221, 1311–1324.

    Article  PubMed  CAS  Google Scholar 

  9. Xia T.H., Bushweller J.H., Sodano P., Billeter M., Björnberg O., Holmgren A., Wüthrich K. 1992. NMR structure of oxidized Escherichia coli glutaredoxin: Comparison with reduced E. coli glutaredoxin and functionally related proteins. J. Protein Sci. 1, 310–321.

    Article  CAS  Google Scholar 

  10. Ji X., Zhang P., Armstrong R.N., Gilliland G.L. 1992. The three-dimensional structure of a glutathione S-transferase from the pi gene class: Structural analysis of the binary complex of isozyme 3-3 and glutathione at 2.2 J. Biochem. 31, 10169–10184.

    Article  CAS  Google Scholar 

  11. Reinemer P., Dirr H.W., Ladenstein R., Schäffer J., Gallay O., Huber R. 1991. The three-dimensional structure of class r glutathione S-transferase in complex with glutathione sulfonate at 2.3 EMBO J. 10, 1997–2005.

    PubMed  CAS  Google Scholar 

  12. Reinemer P., Dirr H.W., Ladenstein R., Huber R., Lo Bello M., Federici G., Parker M.W. 1992. Three-dimensional structure of class r glutathione S-transferase from human placenta in complex with S-hexylglutathione at 2.8 J. Mol. Biol. 227, 214–226.

    Article  PubMed  CAS  Google Scholar 

  13. Sinning I., Jones T.A. 1993. Structure determination and refinement of human class glutathione transferase A1-1, and a comparison with the pI and rr class enzymes. J. Mol. Biol. 232, 192–212.

    Article  PubMed  CAS  Google Scholar 

  14. Martin J.L., Bardwell J.C.A., Kuriyan J. 1993. Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature. 365, 464–468.

    Article  PubMed  CAS  Google Scholar 

  15. Fomenko D.E., Gladyshev V.N. 2003. CxxS: Fold-independent redox motif revealed by genome-wide searches for thiol/disulfide oxidoreductase function. J. Biochem. 42, 11214–11225.

    Article  CAS  Google Scholar 

  16. Jacob C., Giles G.I., Giles N.M., Sies H. 2003. Sulfur and selenium: The role of oxidation state in protein structure and function. J. Angew. Chem. Int. Ed. 42, 4742–4758.

    Article  CAS  Google Scholar 

  17. Johansson L., Gafvelin G., Arnér E.S. 2005. Selenocysteine in proteins: Properties and biotechnological use. J. Biochim. Biophys. Acta. 1726, 1–13.

    Article  CAS  Google Scholar 

  18. Mills G.C. 1957. Hemoglobin catabolism: 1. Glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown. J. Biol. Chem. 229, 189–197.

    PubMed  CAS  Google Scholar 

  19. Sunde R.A. 1997. Selenium. In: Handbook of Nutritionally Essential Mineral Elements. Eds. O’Dell B.L., Sunde R.A. NY: Marcel Dekker, pp. 493–556.

    Google Scholar 

  20. Grossmann A., Wendel A. 1983. Non-reactivity of the selenoenzyme glutathione peroxidase with enzymically hydroperoxidised phospholipids. Eur. J. Biochem. 135, 549–552.

    Article  PubMed  CAS  Google Scholar 

  21. Chu F.F., Doroshow J.H., Esworthy R.S. 1993. Expression, characterization and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI. J. Biol. Chem. 268, 2571–2576.

    PubMed  CAS  Google Scholar 

  22. Florian S., Wingler K., Schmehl K., Jacobasch G., Kreuzer O.J., Meyerhof W., Brigelius-Flohe R. 2001. Cellular and subcellular localization of gastrointestinal glutathione peroxidase in normal and malignant human intestinal tissue. Free Radic. Res. 35, 655–663.

    Article  PubMed  CAS  Google Scholar 

  23. Murawaki Y., Tsuchiya H., Kanbe T., Harada K., Yashima K., Nozaka K., Tanida O., Kohno M., Mukoyama T., Nishimuki E., Kojo H., Matsura T., Takahashi K., Osaki M., Ito H., Yodoi J., Murawaki Y., Shiota G. 2008. Aberrant expression of selenoproteins in the progression of colorectal cancer. Cancer Lett. 259, 218–230.

    Article  PubMed  CAS  Google Scholar 

  24. Chu F.F., Esworthy R.S., Chu P.G., Longmate J.A., Huycke M.M., Wilczynski S., Doroshow J.H. 2004. Bacteria-induced intestinal cancer in mice with disrupted GPx1 and GPx2 genes. Cancer Res. 64, 962–968.

    Article  PubMed  CAS  Google Scholar 

  25. Esworthy R.S., Yang L., Frankel P.H., Chu F.F. 2005. Epithelium-specific glutathione peroxidase, GPx2, is involved in the prevention of intestinal inflammation in selenium-deficient mice. J. Nutr. 135, 740–745.

    PubMed  CAS  Google Scholar 

  26. Burk R.F., Hill K.E. 2005. Selenoprotein P: An extracellular protein with unique physical characteristics and a role in selenium homeostasis. Annu. Rev. Nutr. 25, 215–235.

    Article  PubMed  CAS  Google Scholar 

  27. Yoshimura S., Watanabe K., Suemizu H., Onozawa T., Mizoguchi J., Tsuda K., Hatta H., Moriuchi T. 1991. Tissue specific expression of the plasma glutathione peroxidase gene in rat kidney. J. Biochem. 109, 918–923.

    PubMed  CAS  Google Scholar 

  28. Schmutzler C., Mentrup B., Schomburg L., Hoang-Vu C., Herzog V., Kohrle J. 2007. Selenoproteins of the thyroid gland: Expression, localization and possible function of glutathione peroxidase 3. Biol. Chem. 388, 1053–1059.

    Article  PubMed  CAS  Google Scholar 

  29. Ottaviano F.G., Tang S.S., Handy D.E., Loscalzo J. 2009. Regulation of the extracellular antioxidant selenoprotein plasma glutathione peroxidase (GPx-3) in mammalian cells. Mol. Cell. Biochem. 327, 111–126.

    Article  PubMed  CAS  Google Scholar 

  30. Bjornstedt M., Xue J., Huang W., Akesson B., Holmgren A. 1994. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269, 29382–29384.

    PubMed  CAS  Google Scholar 

  31. Freedman J.E., Loscalzo J., Benoit S.E., Valeri C.R., Barnard M.R., Michelson A.D. 1996. Decreased platelet inhibition by nitric oxide in two brothers with a history of arterial thrombosis. J. Clin. Invest. 97, 979–987.

    Article  PubMed  CAS  Google Scholar 

  32. Ursini F., Heim S., Kiess M., Maiorino M., Roveri A., Wissing J., Flohe L. 1999. Dual function of the selenoprotein PHGPx during sperm maturation. Science. 277, 1393–1396.

    Article  Google Scholar 

  33. Roveri A., Casasco A., Maiorino M., Dalan P., Calligaro A., Ursini F. 1992. Phospholipid hydroperoxide glutathione peroxidase of rat testis: Gonadotropin dependence and immunocytochemical identification. J. Biol. Chem. 267, 6142–6146.

    PubMed  CAS  Google Scholar 

  34. Brigelius-Flohe R. 1999. Tissue-specific functions of individual glutathione peroxidases: Analysis with the fluorescent labeling agent monobromobimane. Free Radic. Biol. Med. 27. 951-965.

    Google Scholar 

  35. Pushpa Rekha T., Burdsal L.M., Chilsom G.M., Driscoll D.M. 1985. Rat phospholipid-hydroperoxidase glutathione peroxidase: cDNA cloning and identification of multiple transcription and translation start sites. J. Biol. Chem. 270, 26993–26999.

    Google Scholar 

  36. Pfeifer H., Conrad M., Roethlein D., Kyriakopoulos A., Brielmeier M., Bornkamm G. W., Behne D. 2001. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J. 15, 1236–1238.

    Article  PubMed  CAS  Google Scholar 

  37. Conrad S., G. Moreno F., Sinowatz F., Ursini S., Kölle A., Roveri M., Brielmeier W., Wurst M., Maiorino and Bornkamm G. W. 2005. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol. Cell Biol. 25, 7637–7639.

    Article  PubMed  CAS  Google Scholar 

  38. Maiorino M.J. B. Wissing R., Brigelius-Flohe F., Calabrese A., Roveri P., Steinert F., Ursini F., Flohe L. 1995. Probing the presumed catalytic triad of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol. Chem. Hoppe Seyler. 376, 651–660.

    Article  PubMed  CAS  Google Scholar 

  39. Roveri A., Ursini F., Flohe L., Maiorino M. 2001. PHGPx and spermatogenesis. Biofactors. 14, 213–222.

    Article  PubMed  CAS  Google Scholar 

  40. Van Heusden G.P.H. 2005. 14-3-3 proteins: Regulators of numerous eukaryotic proteins. J. IUBMB Life. 57, 623–629.

    Article  CAS  Google Scholar 

  41. Maiorino M., Roveri A., Benazzi L., Bosello V., Mauri P., Toppo S., Tosatto S. C., Ursini F. 2005. Functional interaction of phospholipid hydroperoxide glutathione peroxidase with sperm mitochondrion-associated cysteine-rich protein discloses the adjacent cysteine motif as a new substrate of the selenoperoxidase. J. Biol. Chem. 280, 38395–38402.

    Article  PubMed  CAS  Google Scholar 

  42. Peltola V., Huhtaniemi I., Metsa-Ketela T., Ahotupa M. 1996. Induction of lipid peroxidation during steroidogenesis in the rat testis. Endocrinology. 137, 105–112.

    Article  PubMed  CAS  Google Scholar 

  43. Ho Y.-S., Magnenat J.L., Bronson R.T., Cao J., Gargano M., Sugawara M., Funk C.D. 1997. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J. Biol. Chem. 272, 16644–16651.

    Article  PubMed  CAS  Google Scholar 

  44. Ghyselinck N.B., Dufaure J.P. 1990. A mouse cDNA sequence for epididymal androgen-regulated proteins related to glutathione peroxidases. Nucleic Acids Res. 18, 7144.

    Article  PubMed  CAS  Google Scholar 

  45. Jimenez C., Lefrancois A., Ghyselinck N.B., Dufaure J.P. 1992. Characterization and hormonal regulation of 24 kDa protein synthesis by the adult murine epididymis. J. Endocrinol. 133, 197–203.

    Article  PubMed  CAS  Google Scholar 

  46. Vernet P., Faure J., Dufaure J.P. Drevet J.R. 1997. Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPx5, a murine epididymis-specific glutathione peroxidase. Mol. Rep. Dev. 47, 87–98.

    Article  CAS  Google Scholar 

  47. Rejraji H., Vernet P., Drevet J.R. 2002. GPx5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Mol. Rep. Dev. 63, 96–103.

    Article  CAS  Google Scholar 

  48. Thisse C., Degrave A., Kryukov G.V., Gladyshev V.N., Obrecht-Pflumio S., Krol A., Thisse B., Lescure A. 2003. Spatial and temporal expression patterns of sele-noprotein genes during embryogenesis in zebrafish. Gene Exp. Patterns. 3, 525–532.

    Article  CAS  Google Scholar 

  49. Varlamova E.G. 2011. Intracellular localization of mammalian selenoproteins: SelV (Selenoprotein V) and GPx6 (Glutathion Peroxidase 6). Fundamental Res. 9, 326–330.

    Google Scholar 

  50. Utomo A., Jiang X.Z., Furuta S., Yun J., Levin D.S., Wang Y.C.J., Desai K.V., Green J.E., Chen P.L., Lee W.H. 2004. Identification of a novel putative nonselenocysteine containing phospholipid hydroperoxide glutathione peroxidase (NPGPx) essential for alleviating oxidative stress generated from polyunsaturated fatty acids in breast cancer cells. J. Biol. Chem. 279, 43522–43529.

    Article  PubMed  CAS  Google Scholar 

  51. Thomas J.P., Maiorino M., Ursini F., Girotti A.W. 1990. Protective action of phospholipid hydroperoxide glutathione peroxidase against membrane-damaging lipid-peroxidation: In situ reduction of phospholipid and cholesterol hydroperoxides. J. Biol. Chem. 265, 454–461.

    PubMed  CAS  Google Scholar 

  52. Ursini F., Maiorino M., Gregolin C. 1985. The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim. Biophys. Acta. 839, 62–70.

    Article  PubMed  CAS  Google Scholar 

  53. Nguyen V.D., Saaranen M.J., Karala A.R., Lappi A.K., Wang L., Raykhel I.B., Alanen H.I., Salo K.E., Wang C.C., Ruddock L.W. 2011.Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J. Mol. Biol. 406, 503–515.

    Article  PubMed  CAS  Google Scholar 

  54. Rocher C., Lalanne J.L., Chaudière J. 1992. Purification and properties of a recombinant sulfur analog of murine selenium-glutathione peroxidase. Eur. J. Biochem. 205, 955–960.

    Article  PubMed  CAS  Google Scholar 

  55. Maiorino M., Aumann K.D., Brigelius-Flohé R., Doria D., van den Heuvel J., McCarthy J., Roveri A., Ursini F., Flohé L. 1995. Probing the presumed catalytic triad of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol. Chem. 376, 651–660.

    CAS  Google Scholar 

  56. Flohe L., Gunzler W.A., Schock H.H. 1973. Glutathione peroxidase: A selenoenzyme. FEBS Lett. 32, 132–134.

    Article  PubMed  CAS  Google Scholar 

  57. Flohe L., Loschen G., Gunzler W.A., Eichele E. 1972. Glutathione peroxidase: 5. The kinetic mechanism. Physiol. Chem. 353, 987–999.

    Article  CAS  Google Scholar 

  58. Kraus R.J., Prohaska J.R., Ganther H.E. 1980. Oxidized forms of ovine erythrocyte glutathione peroxidase. Cyanide inhibition of a 4-glutathione: 4-selenoenzyme. Biochim. Biophys. Acta. 615, 19–26.

    Article  PubMed  CAS  Google Scholar 

  59. Takebe G., Yarimizu J., Saito Y., Hayashi T., Nakamura H., Yodoi J., Nagasawa S., and Takahashi K. 2002. A comparative study on the hydroperoxide and thiol specificity of the glutathione peroxidase family and selenoprotein P. J. Biol. Chem. 277, 41254–41258.

    Article  PubMed  CAS  Google Scholar 

  60. Ursini F., Maiorino M., Brigelius-Flohe R., Aumann K.D., Roveri A., Schomburg D., Flohe L. 1995. Diversity of glutathione peroxidases. Methods Enzymol. 252, 38–53.

    Article  PubMed  CAS  Google Scholar 

  61. Martinez J.I., Garcia R.D., Galarza A.M. 1982. The kinetic mechanism of glutathione peroxidase from human platelets. Thromb. Res. 27, 197–203.

    Article  PubMed  CAS  Google Scholar 

  62. Herbette S., Roeckel-Drevet P., Drevet J.R. 2007. Selenoindependent glutathione peroxidases: More than simple antioxidant scavengers. FEBS J. 274 (9), 2163–80.

    Article  PubMed  CAS  Google Scholar 

  63. Lubos E., Loscalzo J., Handy D.E. 2011. Glutathione peroxidase-1 in health and disease: From molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 7, 1957–1998.

    Article  CAS  Google Scholar 

  64. Lillig C.H., Berndt C., Holmgren A. 2008. Glutaredoxin systems. Biochim. Biophys. Acta. 1980, 1304–1317.

    Article  CAS  Google Scholar 

  65. Mieyal J.J., Gallogly M.M., Qanungo S., Sabens E.A., Shelton M.D. 2008. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid. Redox Signal. 10, 1941–1988

    Article  PubMed  CAS  Google Scholar 

  66. Wang J., Boja E.S., Tan W., Tekle E., Fales H.M., English S., Mieyal J.J., Chock P.B. 2001. Reversible glutathionylation regulates actin polymerization in A431 cells. J. Biol. Chem. 276, 47763–47766.

    PubMed  CAS  Google Scholar 

  67. Chen Y.R., Chen C.L., Pfeiffer D.R., Zweier J.L. 2007. Mitochondrial complex II in the post-ischemic heart: Oxidative injury and the role of protein S-glutathionylation. J. Biol. Chem. 282, 32640–32654.

    Article  PubMed  CAS  Google Scholar 

  68. Chen F.C., Ogut O. 2006. Decline of contractility during ischemia reperfusion injury: Actin glutathionylation and its effect on allosteric interaction with tropomyosin. Am. J. Physiol. Cell Physiol. 290, C719–C727.

    Article  PubMed  CAS  Google Scholar 

  69. Eaton P., Wright N., Hearse D.J., Shattock M.J. 2002. Glyceraldehyde phosphate dehydrogenase oxidation during cardiac ischemia and reperfusion. J. Mol. Cell Cardiol. 34, 1549–1560.

    Article  PubMed  CAS  Google Scholar 

  70. Hurd T.R., Requejo R., Filipovska A., Brown S., Prime T.A., Robinson A.J., Fearnley I.M., Murphy M.P. 2008. Complex I within oxidatively stressed bovine heart mitochondria is glutathionylated on Cys-531 and Cys-704 of the 75-kDa subunit: Potential role of CYS residues in decreasing oxi-dative damage. J. Biol. Chem. 283, 24801–24815.

    Article  PubMed  CAS  Google Scholar 

  71. Holmgren A. 1976. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc. Natl. Acad. Sci. U. S. A. 73, 2275–2279.

    Article  PubMed  CAS  Google Scholar 

  72. Vlamis-Gardikas A., Holmgren A. 2002. Thioredoxin and glutaredoxin isoforms. Methods Enzymol. 347, 286–296.

    Article  PubMed  CAS  Google Scholar 

  73. Xia B., Vlamis-Gardikas A., Holmgren A., Wright P.E., Dyson H.J. 2001. Solution structure of Escherichia coli glutaredoxin-2 shows similarity to mammalian glutathione-S-transferases. J. Mol. Biol. 310, 907–918.

    Article  PubMed  CAS  Google Scholar 

  74. Rodriguez-Manzaneque M.T., Ros J., Cabiscol E., Sorribas A., Herrero E. 1999. Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol. Cell Biol. 19, 8180–8190.

    PubMed  CAS  Google Scholar 

  75. Witte S., Villalba M., Bi K., Liu Y., Isakov N., Altman A. 2000. Inhibition of the c-Jun N-terminal kinase/AP-1 and NF-kappaB pathways by PICOT, a novel protein kinase E. coli glutaredoxins 73 C-interacting protein with a thioredoxin homology domain. J. Biol. Chem. 275, 1902–1909.

    Article  PubMed  CAS  Google Scholar 

  76. Takashima Y., Hirota K., Nakamura H., Nakamura T., Akiyama K., Cheng F. S., Maeda M., Yodoi J. 1999. Differential expression of glutaredoxin and thioredoxin during monocytic differentiation. Immunol. Lett. 68, 397–401.

    Article  PubMed  CAS  Google Scholar 

  77. Bandyopadhyay S., Starke D.W., Mieyal J.J., Gronostajski R.M. 1998. Thioltransferase (glutaredoxin) reactivates the DNA-binding activity of oxidation-inactivated nuclear factor I. J. Biol. Chem. 273, 392–397.

    Article  PubMed  CAS  Google Scholar 

  78. Hirota K., Matsui M., Murata M., Takashima Y., Cheng F.S., Itoh T., Fukuda K., Yodoi J. 2000. Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem. Biophys. Res. Commun. 274, 177–182.

    Article  PubMed  CAS  Google Scholar 

  79. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., Murphy M.P. 2004. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: Implications for mitochondrial redox regulation and antioxidant defense. J. Biol. Chem. 279, 47939–47951.

    Article  PubMed  CAS  Google Scholar 

  80. Lillig C.H., Lonn M.E., Enoksson M., Fernandes A.P., Holmgren A. 2004. Short interfering RNA-mediated silencing of glutaredoxin 2 increases the sensitivity of HeLa cells toward doxorubicin and phenylarsine oxide. Proc. Natl. Acad. Sci. U. S. A. 101, 13227–13232.

    Article  PubMed  CAS  Google Scholar 

  81. Enoksson M., Fernandes A.P., Prast S., Lillig C.H., Holmgren A., Orrenius S. 2005. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem. Biophys. Res. Commun. 327, 774–779.

    Article  PubMed  CAS  Google Scholar 

  82. Rodriguez-Manzaneque M.T., Tamarit J., Belli G., Ros J., Herrero E. 2002. Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol. Biol. Cell. 13, 1109–1121.

    Article  PubMed  CAS  Google Scholar 

  83. Wood Z.A., Schrüder E., Harris J.R., Poole L.B. 2003. Structure, mechanism, and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32–40.

    Article  PubMed  CAS  Google Scholar 

  84. Soito L., Williamson C, Knutson S.T., Fetrow J.S., Poole L.B. and Nelson K.J. 2011. PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family. Nucleic Acids Res. 39, D332–D337.

    Article  PubMed  CAS  Google Scholar 

  85. Nelson K.J., Knutson S.T., Soito L., Klomsiri C., Poole L.B., Fetrow J.S. 2010. Analysis of the peroxiredoxin family: Using active-site structure and sequence information for global classification and residue analysis. Proteins. 79, 947–964.

    Article  PubMed  CAS  Google Scholar 

  86. Jeong W., Cha M.K., Kim I.H. 2000. Thioredoxindependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/ alkyl hydroperoxide peroxidase C (AhpC) family. J. Biol. Chem. 275, 2924–2930.

    Article  PubMed  CAS  Google Scholar 

  87. Hofmann B., Hecht H.H., Flohe L. 2002. Peroxiredoxins. Biol. Chem. 383, 347–364.

    PubMed  CAS  Google Scholar 

  88. Copley S.D., Novak W.R., Babbitt P.C. 2004. Divergence of function in the thioredoxin fold suprafamily: evidence for evolution of peroxiredoxins from a thioredoxin-like ancestor. Biochemistry. 43, 13981–13995.

    Article  PubMed  CAS  Google Scholar 

  89. Claiborne A., Yeh J.I., Mallett T.C., Luba J., Crane E.J., Charrier V., Parsonage D. 1999. Protein-sulfenic acids: Diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry. 38, 15407–15416.

    Article  PubMed  CAS  Google Scholar 

  90. Wood Z.A., Poole L.B., Karplus P.A. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science. 300, 650–653.

    Article  PubMed  CAS  Google Scholar 

  91. Seo M.S., Kang S.W., Kim K., Baines I.C., Lee T.H., Rhee S.G. 2000. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 275, 20346–20354.

    Article  PubMed  CAS  Google Scholar 

  92. Poole L.B., Reynolds C.M., Wood Z.A., Karplus P.A., Ellis H.R., Li Calzi M. 2000. AhpF and other NADH: Peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur. J. Biochem. 267, 6126–6133.

    Article  PubMed  CAS  Google Scholar 

  93. Choi H.J., Kang S.W., Yang C.H., Rhee S.G., Ryu S.E. 1998. Crystal structure of a novel human peroxidase enzyme at 2.0 Nature Struct. Biol. 5, 400–406.

    Article  PubMed  CAS  Google Scholar 

  94. Ishii T., Yamada M., Sato H., Matsue M., Taketani S., Nakayama K., Sugita Y., Bannai S. 1993. Cloning and characterization of a 23-kDa stress-induced mouse peritoneal macrophage protein. J. Biol. Chem. 268, 18633–18636.

    PubMed  CAS  Google Scholar 

  95. Wonsey D.R., Zeller K.I., Dang C.V. 2002. The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc. Natl. Acad. Sci. U. S. A. 99, 6649–6654.

    Article  PubMed  CAS  Google Scholar 

  96. Prosperi M.T., Ferbus D., Rouillard D., Goubin G. 1998. The pag gene product, a physiological inhibitor of c-abl tyrosine kinase, is overexpressed in cells entering S phase and by contact with agents inducing oxidative stress. FEBS Lett. 423, 39–44.

    Article  PubMed  CAS  Google Scholar 

  97. Wang X., Phelan S.A., Forsman-Semb K., Taylor E.F., Petros C., Brown A., Lerner C.P., Paigen, B. 2003. Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 278, 25179–25190.

    Article  PubMed  CAS  Google Scholar 

  98. Kim H.S., Manevich Y., Feinsteine S.I., Pak J.H., Ho Y.S., Fisher A.B. 2003. Induction of 1-cys peroxiredoxin expression by oxidative stress in lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 285, 363–369.

    Google Scholar 

  99. Jin D.Y., Chae H.Z., Rhee S.G., Jeang K.T. 1997. Regulatory role for a novel human thioredoxin peroxidase in NF-kappaB activation. J. Biol. Chem. 272, 30952–30961.

    Article  PubMed  CAS  Google Scholar 

  100. Chang J.W., Jeon H.B., Lee J.H., Yoo J.S., Chun J.S., Kim J.H., Yoo Y.J. 2001. Augmented expression of peroxiredoxin I in lung cancer. Biochem. Biophys. Res. Commun. 289, 507–512.

    Article  PubMed  CAS  Google Scholar 

  101. Kim H.S., Kang S.W., Rhee S.G., Clerch L.B. 2001. Rat lung peroxiredoxins I and II are differentially regulated during development and by hyperoxia. Am. J. Physiol. Lung Cell Physiol. 280, 1212–1217.

    Google Scholar 

  102. Yanagawa T., Ishikawa T., Ishii T., Tabuchi K., Iwasa S., Bannai S., Omura K., Suzuki H., Yoshida H. 1999. Peroxiredoxin I expression in human thyroid tumors. Cancer Lett. 145, 127–132.

    Article  PubMed  CAS  Google Scholar 

  103. Yanagawa T., Iwasa S., Ishii T., Tabuchi K., Yu S.A.H., Onizawa K., Omura K., Harada H., Suzuki H., Yoshida H. 2000. Peroxiredoxin I expression in oral cancer: A potential new tumor marker. Cancer Lett. 156, 27–35.

    Article  PubMed  CAS  Google Scholar 

  104. Noh D.Y., Ahn S.J., Lee R.A., Kim S.W., Park I.A., Chae H.Z. 2001. Overexpression of peroxiredoxin in human breast cancer. Anticancer Res. 21, 2085–2090.

    PubMed  CAS  Google Scholar 

  105. Karihtala P., Mäntyniemi A., Kang S.W., Kinnula V.L., Soini Y. 2003. Peroxiredoxins in breast carcinoma. Clin. Cancer Res. 9, 3418–3424.

    PubMed  CAS  Google Scholar 

  106. Immenschuh S., Baumgart-Vogt E., Tan M., Iwahara S., Ramadori G., Fahimi H.D. 2003. Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J. Histochem. Cytochem. 51, 1621–1631.

    Article  PubMed  CAS  Google Scholar 

  107. Neumann C.A., Krause D.S., Carman C.V., Das S., Dubey D.P., Abraham J.L., Bronson R.T., Fujiwara Y., Orkin S.H., van Etten R.A. 2003. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature. 424, 561–565.

    Article  PubMed  CAS  Google Scholar 

  108. Knoops B., Clippe A., Bogard C., Arsalane K., Wattiez R., Hermans C., Duconseille E., Falmagne P., Bernard A. 1999. Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J. Biol. Chem. 274, 30451–30458.

    Article  PubMed  CAS  Google Scholar 

  109. Peshenko I.V., Novoselov V.I., Evdokimov V.A., Nikolaev Yu.V., Shuvaeva T.M., Lipkin V.M., Fesenko E.E. 1996. Novel 28-kDa secretory protein from rat olfactory epithelium. FEBS Lett. 381, 12–14.

    Article  PubMed  CAS  Google Scholar 

  110. Peshenko I.V., Novoselov V.I., Evdokimov V.A., Nikolaev Y.V., Kamzalov S.S., Shuvaeva T.M., Lipkin V.M., Fesenko E.E. 1998. Identification of a 28 kDa secretory protein from rat olfactory epithelium as a thiol-specific antioxidant. Free Radic. Biol. Med. 25, 654–659.

    Article  PubMed  CAS  Google Scholar 

  111. Novoselov V.I., Peshenko I.V., Evdokimov V.A., Kamzalov S.S., Novoselov S.V., Nikolaev Iu.V., Bystrova M.F., Fesenko E.E. 1998. Properties of the catalytic center of a secretory 28 kDa protein (1-cys peroxiredoxin) from rat olfactory epithelium. Biophysics (Moscow). 43 (4), 575–580.

    Google Scholar 

  112. Peshenko I.V., Shichi H. 2001. Oxidation of active center cysteine of bovine 1-Cys peroxiredoxin to the cysteine sulfenic acid form by peroxide and peroxynitrite. Free Radic. Biol. Med. 31, 292–303.

    Article  PubMed  CAS  Google Scholar 

  113. Chen J.W., Dodia C., Feinstein S.I., Jain M.K., Fisher A.B. 2000. 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J. Biol. Chem. 275, 28421–28427.

    Article  PubMed  CAS  Google Scholar 

  114. Novoselov V.I., Baryshnikova L.M., Yanin V.A., Amelina S.E., Fesenko E.E. 2003. The influence of peroxyredoxin VI on incised-wound healing in rats. Doklady Biochem. Biophys. 393, 326–327.

    Article  CAS  Google Scholar 

  115. Muller F.L., Lustgarten M.S., Jang Y., Richardson A., Van Remmen H. 2007. Trends in oxidative aging theories. Free Radic. Biol. Med. 43, 477–503.

    Article  PubMed  CAS  Google Scholar 

  116. Holmgren A. 1989. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264, 13963–13966.

    PubMed  CAS  Google Scholar 

  117. Brandes H.K., Larimer F.W., Geck M.K., Stringer C.D., Schurmann P., Hartman F.C. 1993. Direct identification of the primary nucleophile of thioredoxin f. J. Biol. Chem. 268, 18411–18414.

    PubMed  CAS  Google Scholar 

  118. Laurent T.C., Moore E.C., Reichard P. 1964. Enzymatic synthesis of deoxyribonucleotides: 4. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J. Biol. Chem. 239, 3436–3444

    CAS  Google Scholar 

  119. Krone F.A., Westphal G., Meyer H.E., Schwenn J.D. 1990. PAPS-reductase of Escherichia coli: Correlating the N-terminal amino acid sequence with the DNA of gene cys H. FEBS Lett. 260, 6–9

    Article  PubMed  CAS  Google Scholar 

  120. Shi J., Vlamis-Gardikas A., Aslund F., Holmgren A., Rosen B.P. 1999. Reactivity of glutaredoxins 1, 2, and 3 from Escherichia coli shows that glutaredoxin 2 is the primary hydrogen donor to ArsC-catalyzed arsenate reduction. J. Biol. Chem. 274, 36039–36042

    Article  PubMed  CAS  Google Scholar 

  121. Meyer Y., Vignols F. and Reichheld J. P. 2002. Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol. 347, 394–402

    Article  PubMed  CAS  Google Scholar 

  122. Lemaire S. D., Collin V., Keryer E., Quesada A., Miginiac-Maslow M. 2003. Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett. 543, 87–92

    Article  PubMed  CAS  Google Scholar 

  123. Sahrawy M., Hecht V., Lopez-Jaramillo J., Chueca A., Chartier Y., Meyer Y. 1996. Intron position as an evolutionary marker of thioredoxins and thioredoxin domains. J. Mol. Evol. 42, 422–431.

    Article  PubMed  CAS  Google Scholar 

  124. Laloi C., Rayapuram N., Chartier Y., Grienenberger J.M., Bonnard G., Meyer Y. 2001. Identification and characterization of a mitochondrial thioredoxin system in plants. Proc. Natl. Acad. Sci. U. S. A. 98, 14144–14149.

    Article  PubMed  CAS  Google Scholar 

  125. Gasdaska P.Y., Gasdaska J.R., Cochran S., Powis G. 1995. Cloning and sequencing of a human thioredoxin reductase. FEBS Lett. 373, 5–9.

    Article  PubMed  CAS  Google Scholar 

  126. Gasdaska P.Y., Berggren M.M., Berry M.J., Powis G. 1999. Cloning, sequencing and functional expression of a novel human thioredoxin reductase. FEBS Lett. 442, 105–111.

    Article  PubMed  CAS  Google Scholar 

  127. Jimenez A., Johansson C., Ljung J. et al. 2002. Human spermatid-specific thioredoxin-1 (Sptrx-1) is a two-domain protein with oxidizing activity. FEBS Lett. 530, 79–84.

    Article  PubMed  CAS  Google Scholar 

  128. Sadek C.M., Damdimopoulos A.E., Pelto-Huikko M., Gustafsson J.A., Spyrou G., Miranda-Vizuete A. 2001. Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells. 6, 1077–1090.

    Article  PubMed  CAS  Google Scholar 

  129. Jeong W., Yoon H.W., Lee S., Rhee S.G. 2004. Identification and characterization of TRP14, a thioredoxinrelated protein of 14 kDa: New insights into the specificity of thioredoxin function. J. Biol. Chem. 279, 3142–3150.

    Article  PubMed  CAS  Google Scholar 

  130. Witte S., Villalba M., Bi K., Liu Y., Isakov N., Altman A. 2000. Inhibition of the c-Jun N-terminal kinase/AP-1 and NF-kappaB pathways by PICOT, a novel protein kinase C-interacting protein with a thioredoxin homology domain. J. Biol. Chem. 275, 1902–1909.

    Article  PubMed  CAS  Google Scholar 

  131. Matsui M., Oshima M., Oshima H., Takaku K., Maruyama T. 1996. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev. Biol. 178, 179–185.

    Article  PubMed  CAS  Google Scholar 

  132. Bondareva A.A., Capecchi M.R., Iverson S.V., Li Y., Lopez N.I. 2007. Effects of thioredoxin reductase-1 deletion on embryogenesis and transcriptome. Free Radic. Biol. Med. 43, 911–923.

    Article  PubMed  CAS  Google Scholar 

  133. Nonn L., Williams R.R., Erickson R.P., Powis G. 2003. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol. Cell. Biol. 23, 916–922.

    Article  PubMed  CAS  Google Scholar 

  134. Conrad M., Jakupoglu C., Moreno S.G., et al. 2004. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24, 9414–9423.

    Article  PubMed  CAS  Google Scholar 

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  1. Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia

    E. G. Varlamova, M. V. Goltyaev, S. V. Novoselov, V. I. Novoselov & E. E. Fesenko

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  1. E. G. Varlamova
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  2. M. V. Goltyaev
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  3. S. V. Novoselov
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  4. V. I. Novoselov
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  5. E. E. Fesenko
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Correspondence to E. G. Varlamova.

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Original Russian Text © E.G. Varlamova, M.V. Goltyaev, S.V. Novoselov, V.I. Novoselov, E.E. Fesenko, 2013, published in Molekulyarnaya Biologiya, 2013, Vol. 47, No. 4, pp. 568–582.

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Varlamova, E.G., Goltyaev, M.V., Novoselov, S.V. et al. Characterization of several members of the thiol oxidoreductase family. Mol Biol 47, 496–508 (2013). https://doi.org/10.1134/S0026893313040146

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