High levels of thioredoxin reductase 1 modulate drug-specific cytotoxic efficacy

Free Radical Biology and Medicine

Volumn 47, Issue 11, 2009, Pages 1661-1671

  Eriksson, Sofi E ^a   Prast Nielsen, Stefanie ^a   Flaberg, Emilie ^a   Szekely, Laszlo ^a   Arnér, Elias S J ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cancer; Chemotherapy; Cytotoxicity; Free radicals; Selenoprotein; Thioredoxin reductase

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; AURANOFIN; CISPLATIN; GLUTATHIONE; JUGLONE; MENADIONE; OXALIPLATIN; SMALL INTERFERING RNA; THIOREDOXIN; THIOREDOXIN REDUCTASE 1;

ARTICLE; CANCER RESISTANCE; CARCINOMA CELL; CELL CYCLE PHASE; CELL DEATH; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG SENSITIVITY; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOCARCINOMA; APOPTOSIS; AURANOFIN; CELL CYCLE; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CISPLATIN; DINITROCHLOROBENZENE; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; NAPHTHOQUINONES; RNA, SMALL INTERFERING; THIOREDOXIN REDUCTASE 1; VITAMIN K 3;

EID: 70350617658     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.09.016     Document Type: Article

References (71)

1. Nordberg J., and Arnér E.S.J. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31 (2001) 1287-1312
2. Arner E.S., and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267 (2000) 6102-6109
3. 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) H1227-1236
4. Nordlund P., and Reichard P. Ribonucleotide reductases. Annu. Rev. Biochem. 75 (2006) 681-706
5. Luthman M., and Holmgren A. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry 21 (1982) 6628-6633
6. Rundlöf A.K., and Arnér E.S.J. Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxid. Redox Signal. 6 (2004) 41-52
7. Rigobello M.P., Callegaro M.T., Barzon E., Benetti M., and Bindoli A. Purification of mitochondrial thioredoxin reductase and its involvement in the redox regulation of membrane permeability. Free Radic. Biol. Med. 24 (1998) 370-376
8. Sun Q.A., Su D., Novoselov S.V., Carlson B.A., Hatfield D.L., and Gladyshev V.N. Reaction mechanism and regulation of mammalian thioredoxin/glutathione reductase. Biochemistry 44 (2005) 14528-14537
9. Jakupoglu C., Przemeck G.K., Schneider M., Moreno S.G., Mayr N., Hatzopoulos A.K., de Angelis M.H., Wurst W., Bornkamm G.W., Brielmeier M., and Conrad M. Cytoplasmic thioredoxin reductase is essential for embryogenesis but dispensable for cardiac development. Mol. Cell. Biol. 25 (2005) 1980-1988
10. Conrad M., Jakupoglu C., Moreno S.G., Lippl S., Banjac A., Schneider M., Beck H., Hatzopoulos A.K., Just U., Sinowatz F., Schmahl W., Chien K.R., Wurst W., Bornkamm G.W., and Brielmeier M. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24 (2004) 9414-9423
11. Nonn L., Williams R.R., Erickson R.P., and Powis G. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol. Cell. Biol. 23 (2003) 916-922
12. Matsui M., Oshima M., Oshima H., Takaku K., Maruyama T., Yodoi J., and Taketo M.M. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev. Biol. 178 (1996) 179-185
13. 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
14. Gromer S., Eubel J.K., Lee B.L., and Jacob J. Human selenoproteins at a glance. Cell. Mol. Life Sci. 62 (2005) 2414-2437
15. Berggren M.M., Mangin J.F., Gasdaka J.R., and Powis G. Effect of selenium on rat thioredoxin reductase activity: increase by supranutritional selenium and decrease by selenium deficiency. Biochem. Pharmacol. 57 (1999) 187-193
16. Nalvarte I., Damdimopoulos A.E., Nystom C., Nordman T., Miranda-Vizuete A., Olsson J.M., Eriksson L., Bjornstedt M., Arner E.S.J., and Spyrou G. Overexpression of enzymatically active human cytosolic and mitochondrial thioredoxin reductase in HEK-293 cells-effect on cell growth and differentiation. J. Biol. Chem. 279 (2004) 54510-54517
17. 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
18. Crosley L.K., Meplan C., Nicol F., Rundlof A.K., Arner E.S.J., Hesketh J.E., and Arthur J.R. Differential regulation of expression of cytosolic and mitochondrial thioredoxin reductase in rat liver and kidney. Arch. Biochem. Biophys. 459 (2007) 178-188
19. 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
20. Urig S., and Becker K. On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin. Cancer Biol. 16 (2006) 452-465
21. Gromer S., Urig S., and Becker K. The thioredoxin system-from science to clinic. Med. Res. Rev. 24 (2004) 40-89
22. Arner E.S.J., and Holmgren A. The thioredoxin system in cancer. Semin. Cancer Biol. 16 (2006) 420-426
23. Yoo M.H., Xu X.M., Carlson B.A., Gladyshev V.N., and Hatfield D.L. Thioredoxin reductase 1 deficiency reverses tumor phenotype and tumorigenicity of lung carcinoma cells. J. Biol. Chem 281 (2006) 13005-13008
24. Yoo M.H., Xu X.M., Carlson B.A., Patterson A.D., Gladyshev V.N., and Hatfield D.L. Targeting thioredoxin reductase 1 reduction in cancer cells inhibits self-sufficient growth and DNA replication. PLoS ONE e1112 (2007) 2
25. Yoo M.H., Xu X.M., Turanov A.A., Carlson B.A., Gladyshev V.N., and Hatfield D.L. A new strategy for assessing selenoprotein function: siRNA knockdown/knock-in targeting the 3′-UTR. RNA 13 (2007) 921-929
26. Nishimoto M., Sakaue M., and Hara S. Short-interfering RNA-mediated silencing of thioredoxin reductase 1 alters the sensitivity of HeLa cells toward cadmium. Biol. Pharm. Bull. 29 (2006) 543-546
27. Zhong L., Arnér E.S.J., 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. USA 97 (2000) 5854-5859
28. 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
29. Cenas N., Nivinskas H., Anusevicius Z., Sarlauskas J., Lederer F., and Arnér E.S.J. Interactions of quinones with thioredoxin reductase: a challenge to the antioxidant role of the mammalian selenoprotein. J. Biol. Chem. 279 (2004) 2583-2592
30. May J.M., Mendiratta S., Hill K.E., and Burk R.F. Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. J. Biol. Chem. 272 (1997) 22607-22610
31. Arnér E.S.J., Nordberg J., and Holmgren A. Efficient reduction of lipoamide and lipoic acid by mammalian thioredoxin reductase. Biochem. Biophys. Res. Commun. 225 (1996) 268-274
32. Holmgren A. Thioredoxin. Annu. Rev. Biochem. 54 (1985) 237-271
33. Björnstedt M., Kumar S., Björkhem L., Spyrou G., and Holmgren A. Selenium and the thioredoxin and glutaredoxin systems. Biomed. Environ. Sci. 10 (1997) 271-279
34. Lothrop A.P., Ruggles E.L., and Hondal R.J. No selenium required: reactions catalyzed by mammalian thioredoxin reductase that are independent of a selenocysteine residue. Biochemistry 48 (2009) 6213-6223
35. Omata Y., Folan M., Shaw M., Messer R.L., Lockwood P.E., Hobbs D., Bouillaguet S., Sano H., Lewis J.B., and Wataha J.C. Sublethal concentrations of diverse gold compounds inhibit mammalian cytosolic thioredoxin reductase (TrxR1). Toxicol. In Vitro 20 (2006) 882-890
36. Gromer S., Wissing J., Behne D., Ashman K., Schirmer R.H., Flohe L., and Becker K.A. hypothesis on the catalytic mechanism of the selenoenzyme thioredoxin reductase. Biochem. J 332 Pt 2 (1998) 591-592
37. Talbot S., Nelson R., and Self W.T. Arsenic trioxide and auranofin inhibit selenoprotein synthesis: implications for chemotherapy for acute promyelocytic leukaemia. Br. J. Pharmacol. 154 (2008) 940-948
38. Arnér E.S.J., Bjornstedt M., and Holmgren A. 1-Chloro-2,4-dinitrobenzene is an irreversible inhibitor of human thioredoxin reductase: loss of thioredoxin disulfide reductase activity is accompanied by a large increase in NADPH oxidase activity. J. Biol. Chem. 270 (1995) 3479-3482
39. Cenas N., Prast S., Nivinskas H., Sarlauskas J., and Arner E.S. Interactions of nitroaromatic compounds with the mammalian selenoprotein thioredoxin reductase and the relation to induction of apoptosis in human cancer cells. J. Biol. Chem. 281 (2006) 5593-5603
40. Brown K.K., Eriksson S.E., Arner E.S.J., and Hampton M.B. Mitochondrial peroxiredoxin 3 is rapidly oxidized in cells treated with isothiocyanates. Free Radic. Biol. Med. 45 (2008) 494-502
41. Carvalho C.M., Chew E.H., Hashemy S.I., Lu J., and Holmgren A. Inhibition of the human thioredoxin system: a molecular mechanism of mercury toxicity. J. Biol. Chem. 283 (2008) 11913-11923
42. Wallenborg K., Vlachos P., Eriksson S., Huijbregts L., Arner E.S., Joseph B., and Hermanson O. Red wine triggers cell death and thioredoxin reductase inhibition: effects beyond resveratrol and SIRT1. Exp. Cell Res. 315 (2009) 1360-1371
43. Lu J., Papp L.V., Fang J., Rodriguez-Nieto S., Zhivotovsky B., and Holmgren A. Inhibition of mammalian thioredoxin reductase by some flavonoids: implications for myricetin and quercetin anticancer activity. Cancer Res. 66 (2006) 4410-4418
44. Lu J., Chew E.H., and Holmgren A. Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. Proc. Natl. Acad. Sci. USA 104 (2007) 12288-12293
45. Hellberg V., Wallin I., Eriksson S., Hernlund E., Jerremalm E., Berndtsson M., Eksborg S., Arner E.S., Shoshan M., Ehrsson H., and Laurell G. Cisplatin and oxaliplatin toxicity: importance of cochlear kinetics as a determinant for ototoxicity. J. Natl. Cancer Inst. 101 (2009) 37-47
46. Witte A.B., Anestal K., Jerremalm E., Ehrsson H., and Arner E.S.J. Inhibition of thioredoxin reductase but not of glutathione reductase by the major classes of alkylating and platinum-containing anticancer compounds. Free Radic. Biol. Med. 39 (2005) 696-703
47. Arnér E.S.J., Nakamura H., Sasada T., Yodoi J., Holmgren A., and Spyrou G. Analysis of the inhibition of mammalian thioredoxin, thioredoxin reductase, and glutaredoxin by cis-diamminedichloroplatinum (II) and its major metabolite, the glutathione-platinum complex. Free Radic. Biol. Med. 31 (2001) 1170-1178
48. Anestal K., and Arner E.S. Rapid induction of cell death by selenium-compromised thioredoxin reductase 1 but not by the fully active enzyme containing selenocysteine. J. Biol. Chem. 278 (2003) 15966-15972
49. Anestal K., Prast-Nielsen S., Cenas N., and Arner E.S. Cell death by SecTRAPs: thioredoxin reductase as a prooxidant killer of cells. PLoS ONE e1846 (2008) 3
50. Rengby O., Johansson L., Carlson L.A., Serini E., Vlamis-Gardikas A., Karsnas P., and Arnér E.S.J. Assessment of production conditions for efficient use of Escherichia coli in high-yield heterologous recombinant selenoprotein synthesis. Appl. Environ. Microbiol. 70 (2004) 5159-5167
51. Ren X., Björnstedt M., Shen B., Ericson M.L., and Holmgren A. Mutagenesis of structural half-cystine residues in human thioredoxin and effects on the regulation of activity by selenodiglutathione. Biochemistry 32 (1993) 9701-9708
52. Zhong L., Arnér E.S.J., Ljung J., Åslund 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
53. Rengby O., Cheng Q., Vahter M., Jornvall H., and Arner E.S. Highly active dimeric and low-activity tetrameric forms of selenium-containing rat thioredoxin reductase 1. Free Radic. Biol. Med. 46 (2009) 893-904
54. Arnér E.S.J., Zhong L., and Holmgren A. Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol. 300 (1999) 226-239
55. Carlberg I., and Mannervik B. Glutathione reductase. Methods Enzymol. 113 (1985) 484-490
56. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27 (1969) 502-522
57. Vandeputte C., Guizon I., Genestie-Denis I., Vannier B., and Lorenzon G. A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol. Toxicol. 10 (1994) 415-421
58. Flaberg E., Sabelstrom P., Strandh C., and Szekely L. Extended field laser confocal microscopy (EFLCM): combining automated gigapixel image capture with in silico virtual microscopy. BMC Med. Imaging 8 (2008) 13
59. Rundlöf A.K., Janard M., Miranda-Vizuete A., and Arnér E.S.J. Evidence for intriguingly complex transcription of human thioredoxin reductase 1. Free Radic. Biol. Med. 36 (2004) 641-656
60. Berggren M., Gallegos A., Gasdaska J.R., Gasdaska P.Y., Warneke J., and Powis G. Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia. Anticancer Res. 16 (1996) 3459-3466
61. Yoo M.H., Xu X.M., Carlson B.A., Gladyshev V.N., and Hatfield D.L. Thioredoxin reductase 1 deficiency reverses tumor phenotype and tumorigenicity of lung carcinoma cells. J. Biol. Chem. 281 (2006) 13005-13008
62. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., and Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17 (1998) 2596-2606
63. Cassidy P.B., Edes K., Nelson C.C., Parsawar K., Fitzpatrick F.A., and Moos P.J. Thioredoxin reductase is required for the inactivation of tumor suppressor p53 and for apoptosis induced by endogenous electrophiles. Carcinogenesis 27 (2006) 2538-2549
64. Avval F.Z., and Holmgren A. Molecular mechanisms of thioredoxin and glutaredoxin as hydrogen donors for mammalian S phase ribonucleotide reductase. J. Biol. Chem. 284 (2009) 8233-8240
65. Fujiwara N., Fujii T., Fujii J., and Taniguchi N. Functional expression of rat thioredoxin reductase: selenocysteine insertion sequence element is essential for the active enzyme. Biochem. J. 340 Pt. 2 (1999) 439-444
66. Dammeyer P., Damdimopoulos A.E., Nordman T., Jimenez A., Miranda-Vizuete A., and Arner E.S. Induction of cell membrane protrusions by the N-terminal glutaredoxin domain of a rare splice variant of human thioredoxin reductase 1. J. Biol. Chem. 283 (2008) 2814-2821
67. Su D., and Gladyshev V.N. Alternative splicing involving the thioredoxin reductase module in mammals: a glutaredoxin-containing thioredoxin reductase 1. Biochemistry 43 (2004) 12177-12188
68. 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. USA 98 (2001) 9533-9538
69. Jung H.I., Lim H.W., Kim B.C., Park E.H., and Lim C.J. Differential thioredoxin reductase activity from human normal hepatic and hepatoma cell lines. Yonsei Med. J. 45 (2004) 263-272
70. Singh A., Boldin-Adamsky S., Thimmulappa R.K., Rath S.K., Ashush H., Coulter J., Blackford A., Goodman S.N., Bunz F., Watson W.H., Gabrielson E., Feinstein E., and Biswal S. RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res. 68 (2008) 7975-7984
71. Armstrong R.N. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10 (1997) 2-18