Thioredoxin: A redox-regulating cellular cofactor for glucocorticoid hormone action: Crosstalk between endocrine control of stress response and cellular antioxidant defense system

Journal of Clinical Investigation

Volumn 98, Issue 11, 1996, Pages 2469-2477

  Makino, Yuichi ^a   Okamoto, Kensaku ^a   Yoshikawa, Noritada ^a   Aoshima, Masaru ^a   Hirota, Kiichi ^b   Yodoi, Junji ^b   Umesono, Kazuhiko ^c   Makino, Isao ^a   Tanaka, Hirotoshi ^a  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

gene expression; glucocorticoids; oxidative stress; redox; thioredoxin

Indexed keywords

GLUCOCORTICOID; THIOREDOXIN;

ADAPTATION; ANIMAL CELL; ARTICLE; CELL METABOLISM; CHO CELL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC TRANSCRIPTION; HOMEOSTASIS; HORMONAL REGULATION; HORMONE ACTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RESPIRATORY CHAIN;

EID: 0029804576     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119065     Document Type: Article

References (48)

1. Selye, H. 1946. The general adaptation syndrome and the diseases of adaptation. J. Clin. Endocrinol. Metab. 6:117-230.
2. Munck, A., P.M. Guyre, and N.J. Holbrook. 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5:25-44.
3. Yu, B.P. 1994. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 74:139-162.
4. Bauskin, A.R., I. Aikalay, and Y. Ben-Neriah. 1991. Redox regulation of a protein tyrosine kinase in the endoplasmic reticulum. Cell 66:685-696.
5. Demple, B., and C.F. Amabile-Cuevas. 1991. Redox redux: the control of oxidative stress responses. Cell. 67:837-839.
6. Firth, J.D., B.L. Ebert, C.W. Pugh, and P.J. Ratcliffe. 1994. Oxygen-regulated control elements in the phosphoglycerate kinase and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl. Acad. Sci. USA. 91:6496-6500.
7. Devary, Y., R.A, Gottlieb, T. Smeal, and M. Karin. 1992. The mammalian ultraviolet is triggered by activation of Src tyrosine kinases. Cell. 71:1081-1091.
8. Schreck, R., P. Rieber, and P.A. Baeuerle. 1991. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO (Eur. Mol. Biol. Organ.) J. 10:2247-2258.
9. Abate, C., L. Patel, F.J. Rauscher III, and T. Curran. 1990. Redox regulation of Fos and Jun DNA-binding activity in vitro. Science (Wash. DC). 249: 1157-1161.
10. Klebanoff, S.J., M.A. Vadas, J.M. Harlan, L.H. Sparks, J.R. Gamble, J.M. Agosti, and A.M. Waltersdorf. 1986. Stimulation of neutrophils by tumor necrosis factor. J. Immunol. 136:4220-4225.
11. Yoshie, O., T. Majima, and H. Saito. 1989. Membrane oxidative metabolism of human eosinophilic cell line EoL-1 in response to phorbol diester and formyl peptide: synergistic augmentation by interferon-gamma and tumor necrosis factor. J. Leukocyte Biol. 45:10-20.
12. DeChatelet, L.R., P.S. Shirley, and R.B. Johnston. 1976. Effect of phorbol myristate acetate on the oxidative metabolism of human polymorphonuclear leukocytes. Blood. 47:545-554.
13. Beato, M., P. Herrlich, and G. Schütz. 1995. Steroid receptors: many actors in search of a plot. Cell. 83:851-857.
14. Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science (Wash. DC). 240:889-895.
15. Glass, K.C. 1994. Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Mol. Endocrinol. 15:391-407.
16. Hörlein, A.J., A.M. Näär, T. Heinzel, J. Torchis, B. Gloss, R. Kurokawa, A. Ryan, Y. Kamei, M. Söderström, C.K. Glass, and M.G. Rosenfeld. 1995. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature (Lond.). 377:397-404.
17. Katzenellenbogen, J.A., B.W. O'Malley, and B.S. Katzellenbogen. 1996. Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol. Endocrinol. 10:119-131.
18. Onate, S.A., S.Y. Tsai, M.-J., Tsai, and B.W. O'Malley. 1995. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science (Wash. DC). 270:1354-1357.
19. Kamei, Y., L. Xu, T. Heinzel, J. Torchia, R. Kurokawa, B. Gloss, S.-C. Lin, R.A. Heyman, D.W. Rose, C.K. Glass, and M.G. Rosenfeld. 1996. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell. 85:403-414.
20. Chakraborti, P.K., M.J. Garabedian, K.R. Yamamoto, and S.S. Simons, Jr. 1992. Role of cysteines 640, 656, and 661 in steroid binding to rat glucocorticoid. J. Biol. Chem. 267:11366-11373.
21. Simons, S.S., Jr., and W.B. Pratt. 1995. Glucocorticoid receptor thiols and steroid-binding activity. Methods Enzymol. 251:406-422.
22. Luisi, B.F., W.X. Xu, Z. Otwinowski, L.P. Freedman, K.R. Yamamoto, and P.B. Sigler. 1991. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature (Lond.). 352:497-505.
23. Bodwell, J.E., N.J. Holbrook, and A. Munck. 1984. Sulfhydryl-modifying reagents reversibly inhibit binding of glucocorticoid-receptor complexes to DNA-cellulose. Biochemistry. 23:1392-1398.
24. Makino, Y., H. Tanaka, K. Dahlman-Wright, and I. Makino. 1996. Modulation of glucocorticoid-inducible gene expression by metal ions. Mol. Pharmacol. 49:612-620.
25. Holmgren, A. 1995. Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure (Lond.). 3:239-243.
26. Holmgren, A. 1985. Thioredoxin. Annu. Rev. Biochem. 54:237-271.
27. Tagaya, Y., Y. Maeda, A. Mitsui, N. Kondo, H. Matsui, J. Hamuro, N. Brown, K.-I. Arai, T. Yokota, H. Wakasugi, and J. Yodoi. 1989. ATL-derived factor (ADF), an IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement of dithiol-reduction in the IL-2 receptor induction. EMBO (Eur. Mol. Biol. Organ.) J. 8:757-764.
28. Tagaya, Y., M. Okada, K. Sugie, T. Kasahara, N. Kondo, J. Hamuro, K. Matsushima, C.A. Dinarello, and J. Yodoi. 1988. IL-2 receptor(p55)/Tac-inducing factor. Purification and characterization of adult T cell leukemia-derived factor. J. Immunol. 140:2614-2620.
29. Wakasugi, N., Y. Tagaya, H. Wakasugi, A. Mitsui, M. Maeda, J. Yodoi, and T. Tursz. 1990. Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotrophic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc. Natl. Acad. Sci. USA. 87:8282-8286.
30. Schenk, H., M. Klein, W. Erdhrugger, W. Droge, and K. Schulze-Osthoff. 1994. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-κB and AP-1. Proc. Natl. Acad. Sci. USA. 91:1672-1676.
31. Meyer, M., R. Schreck, and P.A. Baeuerle. 1993. H2O2 and antioxidants have opposite effects on activation of NF-κB and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO (Eur. Mol. Biol. Organ.) J. 12: 2005-2015.
32. Grippo, J.F., A. Holmgren, and W.B. Pratt. 1985. Proof that the endogenous, heat-stable glucocorticoid receptor-activating factor is thioredoxin. J. Biol. Chem. 260:93-97.
33. Sasada, T., S. Iwata, N. Sato, Y. Kitaoka, K. Hirota, K. Nakamura, A. Nishiyama, Y. Taniguchi, A. Takabayashi, and J. Yodoi. 1996. Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP). Protective effect of human thioredoxin against CDDP-induced cytotoxicity. J. Clin. Invest. 97: 2268-2276.
34. Alksnis, M., T. Barkhem, P.-E. Strömstedt, H. Ahola, E. Kutoh, J.-Å. Gustafsson, L. Poellinger, and S. Nilson. 1991. High level expression of functional full length and truncated glucocorticoid receptor in Chinese hamster ovary cells. J. Biol. Chem. 266:10078-10085.
35. Tagaya, Y., H. Wakasugi, H. Masutani, H. Nakamura, S. Iwata, A. Mitsui, S. Fujii, N. Wakasugi, T. Tursz, and J. Yodoi. 1990. Role of ATL-derived factor (ADF) in the normal and abnormal cellular activation: involvement of dithiol related reduction. Mol. Immunol. 27:1279-1289.
36. Rangarajan, P.N., K. Umesono, and R.M. Evans. 1992. Modulation of glucocorticoid receptor function by protein kinase A. Mol. Endocrinol. 6:1451-1457.
37. Matthews, J.R., N. Wakasugi, J.-L. Virelizer, J. Yodoi, and R.T. Hay. 1992. Thioredoxin regulates the DNA binding activity of NF-κB by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 20:3821-3830.
38. Yokomizo, A., M. Ono, H. Nanri, Y. Makino, T. Ohga, M. Wada, T. Okamoto, J. Yodoi, M. Kuwano, and K. Kohno. 1995. Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res. 55:4293-4296.
39. Makino, Y., H. Tanaka, and I. Makino. 1994. Paradoxical derepression of the collagenase gene expression by the anti-rheumatic gold compound aurothiomalate. Mol. Pharmacol. 46:1084-1089.
40. Tanaka, H., Y. Makino, K.-D. Wright, J.-Å. Gustafsson, K. Okamoto, and I. Makino. 1995. Zinc ions antagonize the inhibitory effect of aurothiomalate on glucocorticoid receptor function at physiological concentrations. Mol. Pharmacol. 48:938-945.
41. Sachi, Y., K. Hirota, H. Masutani, K. Toda, T. Okamoto, M. Takigawa, and J. Yodoi. 1995. Induction of ADF/TRX by oxidative stress in keratinocytes and lymphoid cells. Immunol. Lett. 44:189-193.
42. Cappel, R.E., and H.F. Gilbert. 1988. Thiol/disulfide exchange between 3-hydroxy-3-methyglutaryl-CoA reductase and glutathione. J. Biol. Chem. 263: 12201-12212.
43. Snyder, G.H., M.J. Cennerazzo, A.J. Karalis, and D. Field. 1981. Electrostatic influence of local cysteine environments on disulfide exchange kinetics. Biochemistry. 20:6509-6518.
44. Xanthoudakis, S., G. Miao, F. Wang, Y.-C.E. Pan, and T. Curran. 1992. Redox-activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO (Eur. Mol. Biol. Organ.) J. 11:3323-3335.
45. Mangelsdorf, D.J., C. Thummel, M. Beato, P. Herrlich, G. Schütz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R.M. Evans. 1995. The nuclear receptor superfamily: the second decade. Cell. 83:835-839.
46. Qin, J., G.M. Clore, W.M.P. Kennedy, J.R. Huth, and A.M. Gronenborn. 1995. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NFκB. Structure (Lond.). 3:289-297.
47. Blake, M.J., R. Udelsman, G.J. Feulner, D.D. Norton, and N.J. Holbrook. 1991. Stress-induced heat shock protein 70 expression in adrenal cortex: an adrenocorticotropic hormone-sensitive, age-dependent response. Proc. Natl. Acad. Sci. USA. 88:9873-9877.
48. Picard, D., B. Khursheed, M.J. Garabedian, M.G. Fortin, S. Lindquist, and K.R. Yamamoto. 1990. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature (Lond.). 348:166-168.