Metabolism of selenium compounds catalyzed by the mammalian selenoprotein thioredoxin reductase

Biochimica et Biophysica Acta - General Subjects

Volumn 1790, Issue 11, 2009, Pages 1513-1519

  Lu, Jun ^a   Berndt, Carsten ^a   Holmgren, Arne ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Ebselen; Redox cycling; Selenite; Selenocysteine; Selenoprotein; Thioredoxin reductase

Indexed keywords

DOXORUBICIN; EBSELEN; HYDROGEN PEROXIDE; LIPID HYDROPEROXIDE; OXYGEN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SELENATE; SELENIDE; SELENITE; SELENIUM; SELENIUM DERIVATIVE; SELENIUM OXIDE; SELENOCYSTEINE; SELENOCYSTINE; SELENOMETHIONINE; SODIUM SELENITE; THIOREDOXIN; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ASTHMA; ATHEROSCLEROSIS; CANCER PREVENTION; CANCER RESISTANCE; CARDIOVASCULAR DISEASE; CATALYSIS; CELL DEATH; CLINICAL TRIAL; CYTOTOXICITY; DIET SUPPLEMENTATION; DRUG EFFICACY; DRUG SENSITIVITY; DRUG TARGETING; EHRLICH ASCITES TUMOR; ENZYME METABOLISM; ENZYME SUBSTRATE; ESCHERICHIA COLI; HEART PROTECTION; HUMAN; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; CARDIOVASCULAR SYSTEM; CATALYSIS; HUMANS; MAMMALS; MODELS, BIOLOGICAL; NEOPLASMS; SELENIUM; SELENIUM COMPOUNDS; SELENOPROTEINS; THIOREDOXIN-DISULFIDE REDUCTASE;

MAMMALIA;

EID: 72649091301     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2009.04.013     Document Type: Review

References (93)

1. Holmgren A. Thioredoxin. Annu. Rev. Biochem. 54 (1985) 237-271
2. Holmgren A. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264 (1989) 13963-13966
3. Engstrom N.E., Holmgren A., Larsson A., and Soderhall S. Isolation and characterization of calf liver thioredoxin. J. Biol. Chem. 249 (1974) 205-210
4. Holmgren A. Bovine thioredoxin system. Purification of thioredoxin reductase from calf liver and thymus and studies of its function in disulfide reduction. J. Biol. Chem. 252 (1977) 4600-4606
5. Luthman M., and Holmgren A. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry 21 (1982) 6628-6633
6. Zhong L., Arnér E.S., Ljung J., Aslund F., and Holmgren A. Rat and calf thioredoxin reductase are homologous to glutathione reductase with a carboxyl-terminal elongation containing a conserved catalytically active penultimate selenocysteine residue. J. Biol. Chem. 273 (1998) 8581-8591
7. Kryukov G.V., Castellano S., Novoselov S.V., et al. Characterization of mammalian selenoproteomes. Science 300 (2003) 1439-1443
8. Lu J., and Holmgren A. Selenoproteins. J. Biol. Chem. 284 (2009) 723-727
9. Papp L.V., Lu J., Striebel F., Kennedy D., Holmgren A., and Khanna K.K. The redox state of SECIS binding protein 2 controls its localization and selenocysteine incorporation function. Mol. Cell. Biol. 26 (2006) 4895-4910
10. Holmgren A. Enzymatic reduction-oxidation of protein disulfides by thioredoxin. Methods Enzymol. 107 (1984) 295-300
11. Rozell B., Hansson H.A., Luthman M., and Holmgren A. Immunohistochemical localization of thioredoxin and thioredoxin reductase in adult rats. Eur. J. Cell. Biol. 38 (1985) 79-86
12. Stemme S., Hansson H.A., Holmgren A., and Rozell B. Axoplasmic transport of thioredoxin and thioredoxin reductase in rat sciatic nerve. Brain Res. 359 (1985) 140-146
13. Williams C.H., Arscott L.D., Muller S., et al. Thioredoxin reductase two modes of catalysis have evolved. Eur. J. Biochem. 267 (2000) 6110-6117
14. Gustafsson T.N., Sandalova T., Lu J., Holmgren A., and Schneider G. High-resolution structures of oxidized and reduced thioredoxin reductase from Helicobacter pylori. Acta Crystallogr. D Biol. Crystallogr. 63 (2007) 833-843
15. Sandalova T., Zhong L., Lindqvist Y., Holmgren A., and Schneider G. Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 9533-9538
16. Lennon B.W., Williams Jr. C.H., and Ludwig M.L. Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase. Science 289 (2000) 1190-1194
17. Schwarz K., and Foltz C.M. Selenium as an integral part of factor-3 against dietary necrotic liver degeneration. J. Am. Chem. Soc. 79 (1957) 3292-3293
18. Papp L.V., Lu J., Holmgren A., and Khanna K.K. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid. Redox. Signal. 9 (2007) 775-806
19. Greeder G.A., and Milner J.A. Factors influencing the inhibitory effect of selenium on mice inoculated with Ehrlich ascites tumor cells. Science 209 (1980) 825-827
20. Holmgren A., and Kumar S. Reactions of thioredoxin system with selenium. In: Wendel A., et al. (Ed). Proceedings of the 4th International Symposium on Selenium in Biology and Medicine (1989), Spinger-Verlag, Berlin 47-51
21. Kumar S., Bjornstedt M., and Holmgren A. Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen. Eur. J. Biochem. 207 (1992) 435-439
22. Milner J.A. Effect of selenium on virally induced and transplantable tumor models. Fed. Proc. 44 (1985) 2568-2572
23. Bjornstedt M., Kumar S., and Holmgren A. Selenite and selenodiglutathione: reactions with thioredoxin systems. Methods Enzymol. 252 (1995) 209-219
24. Bjornstedt M., Kumar S., and Holmgren A. Selenodiglutathione is a highly efficient oxidant of reduced thioredoxin and a substrate for mammalian thioredoxin reductase. J. Biol. Chem. 267 (1992) 8030-8034
25. Ganther H.E. Reduction of the selenotrisulfide derivative of glutathione to a persulfide analog by glutathione reductase. Biochemistry 10 (1971) 4089-4098
26. Holmgren A. Tryptophan fluorescence study of conformational transitions of the oxidized and reduced form of thioredoxin. J. Biol. Chem. 247 (1972) 1992-1998
27. Bjornstedt M., Kumar S., Bjorkhem L., Spyrou G., and Holmgren A. Selenium and the thioredoxin and glutaredoxin systems. Biomed. Environ. Sci. 10 (1997) 271-279
28. Spyrou G., Bjornstedt M., Skog S., and Holmgren A. Selenite and selenate inhibit human lymphocyte growth via different mechanisms. Cancer. Res. 56 (1996) 4407-4412
29. Bjornstedt M., Odlander B., Kuprin S., Claesson H.E., and Holmgren A. Selenite incubated with NADPH and mammalian thioredoxin reductase yields selenide, which inhibits lipoxygenase and changes the electron spin resonance spectrum of the active site iron. Biochemistry 35 (1996) 8511-8516
30. Bjornstedt M., Hamberg M., Kumar S., Xue J., and Holmgren A. Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J. Biol. Chem. 270 (1995) 11761-11764
31. Takahata M., Tamura T., Abe K., et al. Selenite assimilation into formate dehydrogenase H depends on thioredoxin reductase in Escherichia coli. J. Biochem. 143 (2008) 467-473
32. Drake E.N. Cancer chemoprevention: selenium as a prooxidant, not an antioxidant. Med. Hypotheses 67 (2006) 318-322
33. Tarze A., Dauplais M., Grigoras I., et al. Extracellular production of hydrogen selenide accounts for thiol-assisted toxicity of selenite against Saccharomyces cerevisiae. J. Biol. Chem. 282 (2007) 8759-8767
34. Batist G., Katki A.G., Klecker Jr. R.W., and Myers C.E. Selenium-induced cytotoxicity of human leukemia cells: interaction with reduced glutathione. Cancer Res. 46 (1986) 5482-5485
35. Tamura T., and Stadtman T.C. A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 1006-1011
36. Gladyshev N., Jeang K.T., and Stadtman T.C. Selenocysteine, identified as the penultimate C-terminal residue in human T-cell thioredoxin reductase, corresponds to TGA in the human placental gene. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 6146-6151
37. Zhong L., and Holmgren A. Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J. Biol. Chem. 275 (2000) 18121-18128
38. Zhong L., Arnér E.S., and Holmgren A. Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5854-5859
39. Lee S.R., Bar-Noy S., Kwon J., Levine R.L., Stadtman T.C., and Rhee S.G. Mammalian thioredoxin reductase: oxidation of the C-terminal cysteine/selenocysteine active site forms a thioselenide, and replacement of selenium with sulfur markedly reduces catalytic activity. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 2521-2526
40. Cheng Q., Sandalova T., Lindqvist Y., and Arner E.S. Crystal structure and catalysis of the selenoprotein thioredoxin reductase 1. J. Biol. Chem. 284 (2009) 3998-4008
41. Lee S.R., Kim J.R., Kwon K.S., et al. Molecular cloning and characterization of a mitochondrial selenocysteine-containing thioredoxin reductase from rat liver. J. Biol. Chem. 274 (1999) 4722-4734
42. Sun Q.A., Kirnarsky L., Sherman S., and Gladyshev V.N. Selenoprotein oxidoreductase with specificity for thioredoxin and glutathione systems. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3673-3678
43. Arnér E.S., Sarioglu H., Lottspeich F., Holmgren A., and Bock A. High-level expression in Escherichia coli of selenocysteine-containing rat thioredoxin reductase utilizing gene fusions with engineered bacterial-type SECIS elements and co-expression with the selA, selB and selC genes. J. Mol. Biol. 292 (1999) 1003-1016
44. Hatfield D.L., Yoo M.H., Carlson B.A., and Gladyshev V.N. Selenoproteins that function in cancer prevention and promotion. Biochim. Biophys. Acta (2009) doi:10.1016/j.bbagen.2009.03.001
45. Hill K.E., McCollum G.W., Boeglin M.E., and Burk R.F. Thioredoxin reductase activity is decreased by selenium deficiency. Biochem. Biophys. Res. Commun. 234 (1997) 293-295
46. Lu J., Zhong L.W., Lönn M.E., Burk R.F., Hill K.E., and Holmgre A. Penultimate selenocysteine residue replaced by cysteine in thioredoxin reductase from selenium deficient rat liver. FASEB J 23 (2009) 2394-2402
47. Lippman S.M., Klein E.A., Goodman P.J., et al. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 301 (2009) 39-51
48. El-Bayoumy K. The negative results of the SELECT study do not necessarily discredit the selenium-cancer prevention hypothesis. Nutr. Cancer 61 (2009) 285-286
49. Gromer S., and Gross J.H. Methylseleninate is a substrate rather than an inhibitor of mammalian thioredoxin reductase. Implications for the antitumor effects of selenium. J. Biol. Chem. 277 (2002) 9701-9706
50. Selenius M., Fernandes A.P., Brodin O., Bjornstedt M., and Rundlof A.K. Treatment of lung cancer cells with cytotoxic levels of sodium selenite: effects on the thioredoxin system. Biochem. Pharmacol. 75 (2008) 2092-2099
51. Spyrou G., and Holmgren A. Deoxyribonucleoside triphosphate pools and growth of glutathione-depleted 3T6 mouse fibroblasts. Biochem. Biophys. Res. Commun. 220 (1996) 42-46
52. Smart D.K., Ortiz K.L., Mattson D., et al. Thioredoxin reductase as a potential molecular target for anticancer agents that induce oxidative stress. Cancer Res. 64 (2004) 6716-6724
53. Grogan T.M., Fenoglio-Prieser C., Zeheb R., et al. Thioredoxin, a putative oncogene product, is overexpressed in gastric carcinoma and associated with increased proliferation and increased cell survival. Hum. Pathol. 31 (2000) 475-481
54. Urig S., and Becker K. On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin. Cancer Biol. 16 (2006) 452-465
55. Lu J., Chew E.H., and Holmgren A. Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 12288-12293
56. Holmgren A. Selenite in cancer therapy: a commentary on "Selenite induces apoptosis in sarcomatoid malignant mesothelioma cells through oxidative stress". Free. Radic. Biol. Med. 41 (2006) 862-865
57. Bjorkhem-Bergman L., Jonsson K., Eriksson L.C., et al. Drug-resistant human lung cancer cells are more sensitive to selenium cytotoxicity. Effects on thioredoxin reductase and glutathione reductase. Biochem. Pharmacol. 63 (2002) 1875-1884
58. Jonsson-Videsater K., Bjorkhem-Bergman L., Hossain A., et al. Selenite-induced apoptosis in doxorubicin-resistant cells and effects on the thioredoxin system. Biochem. Pharmacol. 67 (2004) 513-522
59. Neve J. Selenium as a risk factor for cardiovascular diseases. J. Cardiovasc. Risk 3 (1996) 42-47
60. Ge K., and Yang G. The epidemiology of selenium deficiency in the etiological study of endemic diseases in China. Am. J. Clin. Nutr. 57 (1993) 259S-263S
61. Salvini S., Hennekens C.H., Morris J.S., Willett W.C., and Stampfer M.J. Plasma levels of the antioxidant selenium and risk of myocardial infarction among U.S. physicians. Am. J. Cardiol. 76 (1995) 1218-1221
62. Virtamo J., Valkeila E., Alfthan G., Punsar S., Huttunen J.K., and Karvonen M.J. Serum selenium and the risk of coronary heart disease and stroke. Am. J. Epidemiol. 122 (1985) 276-282
63. Kardinaal A.F., Kok F.J., Kohlmeier L., et al. Association between toenail selenium and risk of acute myocardial infarction in European men. The EURAMIC Study. European Antioxidant Myocardial Infarction and Breast Cancer. Am. J. Epidemiol. 145 (1997) 373-379
64. Rayman M.P. The importance of selenium to human health. Lancet 356 (2000) 233-241
65. de Lorgeril M., Salen P., Accominotti M., et al. Dietary and blood antioxidants in patients with chronic heart failure. Insights into the potential importance of selenium in heart failure,. Eur. J. Heart Fail. 3 (2001) 661-669
66. Salonen J.T., Salonen R., Seppanen K., et al. Relationship of serum selenium and antioxidants to plasma lipoproteins, platelet aggregability and prevalent ischaemic heart disease in Eastern Finnish men. Atherosclerosis 70 (1988) 155-160
67. Toufektsian M.C., Boucher F., Pucheu S., et al. Effects of selenium deficiency on the response of cardiac tissue to ischemia and reperfusion. Toxicology 148 (2000) 125-132
68. Poltronieri R., Cevese A., and Sbarbati A. Protective effect of selenium in cardiac ischemia and reperfusion. Cardioscience 3 (1992) 155-160
69. Tanguy S., Morel S., Berthonneche C., et al. Preischemic selenium status as a major determinant of myocardial infarct size in vivo in rats. Antioxid. Redox. Signal. 6 (2004) 792-796
70. Rakotovao A., Tanguy S., Toufektsian M.C., et al. Selenium status as determinant of connexin-43 dephosphorylation in ex vivo ischemic/reperfused rat myocardium. J. Trace Elem. Med. Biol. 19 (2005) 43-47
71. Tanguy S., Toufektsian M.C., Besse S., Ducros V., De Leiris J., and Boucher F. Dietary selenium intake affects cardiac susceptibility to ischaemia/reperfusion in male senescent rats. Age Ageing 32 (2003) 273-278
72. de Lorgeril M., and Salen P. Selenium and antioxidant defenses as major mediators in the development of chronic heart failure. Heart Fail. Rev. 11 (2006) 13-17
73. Blankenberg S., Rupprecht H.J., Bickel C., et al. Glutathione peroxidase 1 activity and cardiovascular events in patients with coronary artery disease. N. Engl. J. Med. 349 (2003) 1605-1613
74. Schnabel R., Lackner K.J., Rupprecht H.J., et al. Glutathione peroxidase-1 and homocysteine for cardiovascular risk prediction: results from the AtheroGene study. J. Am. Coll. Cardiol. 45 (2005) 1631-1637
75. Espinola-Klein C., Rupprecht H.J., Bickel C., et al. Glutathione peroxidase-1 activity, atherosclerotic burden, and cardiovascular prognosis. Am. J. Cardiol. 99 (2007) 808-812
76. Loeper J., Goy J., Rozensztajn L., Bedu O., and Moisson P. Lipid peroxidation and protective enzymes during myocardial infarction. Clin. Chim. Acta 196 (1991) 119-125
77. Maulik N., Yoshida T., and Das D.K. Oxidative stress developed during the reperfusion of ischemic myocardium induces apoptosis. Free Radic. Biol. Med. 24 (1998) 869-875
78. Yoshida T., Watanabe M., Engelman D.T., et al. Transgenic mice overexpressing glutathione peroxidase are resistant to myocardial ischemia reperfusion injury. J. Mol. Cell. Cardiol. 28 (1996) 1759-1767
79. Yoshida T., Maulik N., Engelman R.M., et al. Glutathione peroxidase knockout mice are susceptible to myocardial ischemia reperfusion injury. Circulation 96 (1997) II-216-220
80. Maulik N., Yoshida T., and Das D.K. Regulation of cardiomyocyte apoptosis in ischemic reperfused mouse heart by glutathione peroxidase. Mol. Cell. Biochem. 196 (1999) 13-21
81. World C.J., Yamawaki H., and Berk B.C. Thioredoxin in the cardiovascular system. J. Mol. Med. 84 (2006) 997-1003
82. Berndt C., Lillig C.H., and Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 292 (2007) H1227-H1236
83. Furman C., Rundlof A.K., Larigauderie G., et al. Thioredoxin reductase 1 is upregulated in atherosclerotic plaques: specific induction of the promoter in human macrophages by oxidized low-density lipoproteins. Free Radic. Biol. Med. 37 (2004) 71-85
84. Neves C., Alves M., Medina J.L., and Delgado J.L. Thyroid diseases, dyslipidemia and cardiovascular pathology. Rev. Port Cardiol. 27 (2008) 1211-1236
85. Fazio S., Palmieri E.A., Lombardi G., and Biondi B. Effects of thyroid hormone on the cardiovascular system. Recent Prog. Horm. Res. 59 (2004) 31-50
86. Kohrle J., Jakob F., Contempre B., and Dumont J.E. Selenium, the thyroid, and the endocrine system. Endocr. Rev. 26 (2005) 944-984
87. Jakupoglu C., Przemeck G.K., Schneider M., et al. Cytoplasmic thioredoxin reductase is essential for embryogenesis but dispensable for cardiac development. Mol. Cell. Biol. 25 (2005) 1980-1988
88. Conrad M., Jakupoglu C., Moreno S.G., et al. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24 (2004) 9414-9423
89. Miranda-Vizuete A., and Spyrou G. Genomic organization and identification of a novel alternative splicing variant of mouse mitochondrial thioredoxin reductase (TrxR2) gene. Mol. Cells 13 (2002) 488-492
90. Sies H., and Masumoto H. Ebselen as a glutathione peroxidase mimic and as a scavenger of peroxynitrite. Adv. Pharmacol. 38 (1997) 229-246
91. Zhao R., Masayasu H., and Holmgren A. Ebselen: a substrate for human thioredoxin reductase strongly stimulating its hydroperoxide reductase activity and a superfast thioredoxin oxidant. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 8579-8584
92. Zhao R., and Holmgren A. A novel antioxidant mechanism of ebselen involving ebselen diselenide, a substrate of mammalian thioredoxin and thioredoxin reductase. J. Biol. Chem. 277 (2002) 39456-39462
93. Fang J., Zhong L., Zhao R., and Holmgren A. Ebselen: a thioredoxin reductase-dependent catalyst for alpha-tocopherol quinone reduction. Toxicol. Appl. Pharmacol. 207 (2005) 103-109