Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1996 Jul 15;24(14):2746–2752. doi: 10.1093/nar/24.14.2746

A novel promoter sequence is involved in the oxidative stress-induced expression of the adult T-cell leukemia-derived factor (ADF)/human thioredoxin (Trx) gene.

Y Taniguchi 1, Y Taniguchi-Ueda 1, K Mori 1, J Yodoi 1
PMCID: PMC145999  PMID: 8759006

Abstract

Adult T cell leukemia-derived factor (ADF) is a human thioredoxin (Trx) and is a disulfide reducing protein with various biological functions. We found that expression of the ADF/Trx gene was increased by oxidative agents such as hydrogen peroxide, diamide and menadione in Jurkat cells. Analysis using a CAT expression vector plasmid under the control of the ADF/Trx gene promoter revealed that CAT gene expression in Jurkat cells was increased after exposure to oxidative agents. A series of deletion analyses showed that a region from -976 to -890 of the 5' flanking sequence was required for enhancement of ADF/Trx promoter activity against the oxidative agents. Gel mobility shift assay revealed the specific DNA binding activities to the sequences from -953 to -930 in the nuclear extracts from the Jurkat cells. The sequences in this region showed no homology with any known consensus sequences for DNA binding factors. It is suggested that ADF/Trx gene expression is enhanced through a novel cis-acting regulatory element responsive for the oxidative stress and a new factor(s) is involved in this oxidative stress responsive element.

Full Text

The Full Text of this article is available as a PDF (132.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alessi D. R., Smythe C., Keyse S. M. The human CL100 gene encodes a Tyr/Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene. 1993 Jul;8(7):2015–2020. [PubMed] [Google Scholar]
  2. Becker J., Mezger V., Courgeon A. M., Best-Belpomme M. Hydrogen peroxide activates immediate binding of a Drosophila factor to DNA heat-shock regulatory element in vivo and in vitro. Eur J Biochem. 1990 May 20;189(3):553–558. doi: 10.1111/j.1432-1033.1990.tb15522.x. [DOI] [PubMed] [Google Scholar]
  3. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  4. Datta R., Taneja N., Sukhatme V. P., Qureshi S. A., Weichselbaum R., Kufe D. W. Reactive oxygen intermediates target CC(A/T)6GG sequences to mediate activation of the early growth response 1 transcription factor gene by ionizing radiation. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2419–2422. doi: 10.1073/pnas.90.6.2419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Demple B. Regulation of bacterial oxidative stress genes. Annu Rev Genet. 1991;25:315–337. doi: 10.1146/annurev.ge.25.120191.001531. [DOI] [PubMed] [Google Scholar]
  6. Fernando M. R., Nanri H., Yoshitake S., Nagata-Kuno K., Minakami S. Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells. Eur J Biochem. 1992 Nov 1;209(3):917–922. doi: 10.1111/j.1432-1033.1992.tb17363.x. [DOI] [PubMed] [Google Scholar]
  7. Ghosh D. TFD: the transcription factors database. Nucleic Acids Res. 1992 May 11;20 (Suppl):2091–2093. doi: 10.1093/nar/20.suppl.2091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grippo J. F., Holmgren A., Pratt W. B. Proof that the endogenous, heat-stable glucocorticoid receptor-activating factor is thioredoxin. J Biol Chem. 1985 Jan 10;260(1):93–97. [PubMed] [Google Scholar]
  9. Hayashi T., Ueno Y., Okamoto T. Oxidoreductive regulation of nuclear factor kappa B. Involvement of a cellular reducing catalyst thioredoxin. J Biol Chem. 1993 May 25;268(15):11380–11388. [PubMed] [Google Scholar]
  10. Holmgren A. Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. J Biol Chem. 1979 Sep 25;254(18):9113–9119. [PubMed] [Google Scholar]
  11. Ito W., Ishiguro H., Kurosawa Y. A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction. Gene. 1991 Jun 15;102(1):67–70. doi: 10.1016/0378-1119(91)90539-n. [DOI] [PubMed] [Google Scholar]
  12. Iwata S., Hori T., Sato N., Ueda-Taniguchi Y., Yamabe T., Nakamura H., Masutani H., Yodoi J. Thiol-mediated redox regulation of lymphocyte proliferation. Possible involvement of adult T cell leukemia-derived factor and glutathione in transferrin receptor expression. J Immunol. 1994 Jun 15;152(12):5633–5642. [PubMed] [Google Scholar]
  13. Kaghad M., Dessarps F., Jacquemin-Sablon H., Caput D., Fradelizi D., Wollman E. E. Genomic cloning of human thioredoxin-encoding gene: mapping of the transcription start point and analysis of the promoter. Gene. 1994 Mar 25;140(2):273–278. doi: 10.1016/0378-1119(94)90557-6. [DOI] [PubMed] [Google Scholar]
  14. Kuge S., Jones N. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 1994 Feb 1;13(3):655–664. doi: 10.1002/j.1460-2075.1994.tb06304.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Larrick J. W., Wright S. C. Cytotoxic mechanism of tumor necrosis factor-alpha. FASEB J. 1990 Nov;4(14):3215–3223. doi: 10.1096/fasebj.4.14.2172061. [DOI] [PubMed] [Google Scholar]
  16. Matsuda M., Masutani H., Nakamura H., Miyajima S., Yamauchi A., Yonehara S., Uchida A., Irimajiri K., Horiuchi A., Yodoi J. Protective activity of adult T cell leukemia-derived factor (ADF) against tumor necrosis factor-dependent cytotoxicity on U937 cells. J Immunol. 1991 Dec 1;147(11):3837–3841. [PubMed] [Google Scholar]
  17. Matthews J. R., Wakasugi N., Virelizier J. L., Yodoi J., Hay R. T. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 1992 Aug 11;20(15):3821–3830. doi: 10.1093/nar/20.15.3821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Matthews N., Neale M. L., Jackson S. K., Stark J. M. Tumour cell killing by tumour necrosis factor: inhibition by anaerobic conditions, free-radical scavengers and inhibitors of arachidonate metabolism. Immunology. 1987 Sep;62(1):153–155. [PMC free article] [PubMed] [Google Scholar]
  19. Meyer M., Schreck R., Baeuerle P. A. H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J. 1993 May;12(5):2005–2015. doi: 10.1002/j.1460-2075.1993.tb05850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mitsui A., Hirakawa T., Yodoi J. Reactive oxygen-reducing and protein-refolding activities of adult T cell leukemia-derived factor/human thioredoxin. Biochem Biophys Res Commun. 1992 Aug 14;186(3):1220–1226. doi: 10.1016/s0006-291x(05)81536-0. [DOI] [PubMed] [Google Scholar]
  21. Miyazaki J., Takaki S., Araki K., Tashiro F., Tominaga A., Takatsu K., Yamamura K. Expression vector system based on the chicken beta-actin promoter directs efficient production of interleukin-5. Gene. 1989 Jul 15;79(2):269–277. doi: 10.1016/0378-1119(89)90209-6. [DOI] [PubMed] [Google Scholar]
  22. Nakamura H., Matsuda M., Furuke K., Kitaoka Y., Iwata S., Toda K., Inamoto T., Yamaoka Y., Ozawa K., Yodoi J. Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide. Immunol Lett. 1994 Sep;42(1-2):75–80. doi: 10.1016/0165-2478(94)90038-8. [DOI] [PubMed] [Google Scholar]
  23. Nose K., Shibanuma M., Kikuchi K., Kageyama H., Sakiyama S., Kuroki T. Transcriptional activation of early-response genes by hydrogen peroxide in a mouse osteoblastic cell line. Eur J Biochem. 1991 Oct 1;201(1):99–106. doi: 10.1111/j.1432-1033.1991.tb16261.x. [DOI] [PubMed] [Google Scholar]
  24. Okada M., Maeda M., Tagaya Y., Taniguchi Y., Teshigawara K., Yoshiki T., Diamantstein T., Smith K. A., Uchiyama T., Honjo T. TCGF(IL 2)-receptor inducing factor(s). II. Possible role of ATL-derived factor (ADF) on constitutive IL 2 receptor expression of HTLV-I(+) T cell lines. J Immunol. 1985 Dec;135(6):3995–4003. [PubMed] [Google Scholar]
  25. Okamoto T., Ogiwara H., Hayashi T., Mitsui A., Kawabe T., Yodoi J. Human thioredoxin/adult T cell leukemia-derived factor activates the enhancer binding protein of human immunodeficiency virus type 1 by thiol redox control mechanism. Int Immunol. 1992 Jul;4(7):811–819. doi: 10.1093/intimm/4.7.811. [DOI] [PubMed] [Google Scholar]
  26. Prestera T., Holtzclaw W. D., Zhang Y., Talalay P. Chemical and molecular regulation of enzymes that detoxify carcinogens. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2965–2969. doi: 10.1073/pnas.90.7.2965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schenk H., Klein M., Erdbrügger W., Dröge W., Schulze-Osthoff K. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1672–1676. doi: 10.1073/pnas.91.5.1672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schreck R., Albermann K., Baeuerle P. A. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic Res Commun. 1992;17(4):221–237. doi: 10.3109/10715769209079515. [DOI] [PubMed] [Google Scholar]
  29. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991 Aug;10(8):2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shah G., Ghosh R., Amstad P. A., Cerutti P. A. Mechanism of induction of c-fos by ultraviolet B (290-320 nm) in mouse JB6 epidermal cells. Cancer Res. 1993 Jan 1;53(1):38–45. [PubMed] [Google Scholar]
  31. Spector A., Yan G. Z., Huang R. R., McDermott M. J., Gascoyne P. R., Pigiet V. The effect of H2O2 upon thioredoxin-enriched lens epithelial cells. J Biol Chem. 1988 Apr 5;263(10):4984–4990. [PubMed] [Google Scholar]
  32. Storz G., Tartaglia L. A., Ames B. N. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science. 1990 Apr 13;248(4952):189–194. doi: 10.1126/science.2183352. [DOI] [PubMed] [Google Scholar]
  33. Tagaya Y., Maeda Y., Mitsui A., Kondo N., Matsui H., Hamuro J., Brown N., Arai K., Yokota T., Wakasugi H. 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 J. 1989 Mar;8(3):757–764. doi: 10.1002/j.1460-2075.1989.tb03436.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tagaya Y., Wakasugi H., Masutani H., Nakamura H., Iwata S., Mitsui A., Fujii S., Wakasugi N., Tursz T., Yodoi J. Role of ATL-derived factor (ADF) in the normal and abnormal cellular activation: involvement of dithiol related reduction. Mol Immunol. 1990 Dec;27(12):1279–1289. doi: 10.1016/0161-5890(90)90032-u. [DOI] [PubMed] [Google Scholar]
  35. Teshigawara K., Maeda M., Nishino K., Nikaido T., Uchiyama T., Tsudo M., Wano Y., Yodoi J. Adult T leukemia cells produce a lymphokine that augments interleukin 2 receptor expression. J Mol Cell Immunol. 1985;2(1):17–26. [PubMed] [Google Scholar]
  36. Toledano M. B., Leonard W. J. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4328–4332. doi: 10.1073/pnas.88.10.4328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tonissen K. F., Wells J. R. Isolation and characterization of human thioredoxin-encoding genes. Gene. 1991 Jun 30;102(2):221–228. doi: 10.1016/0378-1119(91)90081-l. [DOI] [PubMed] [Google Scholar]
  38. Wakasugi H., Rimsky L., Mahe Y., Kamel A. M., Fradelizi D., Tursz T., Bertoglio J. Epstein-Barr virus-containing B-cell line produces an interleukin 1 that it uses as a growth factor. Proc Natl Acad Sci U S A. 1987 Feb;84(3):804–808. doi: 10.1073/pnas.84.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wakasugi N., Tagaya Y., Wakasugi H., Mitsui A., Maeda M., Yodoi J., Tursz T. Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic 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 U S A. 1990 Nov;87(21):8282–8286. doi: 10.1073/pnas.87.21.8282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wollman E. E., d'Auriol L., Rimsky L., Shaw A., Jacquot J. P., Wingfield P., Graber P., Dessarps F., Robin P., Galibert F. Cloning and expression of a cDNA for human thioredoxin. J Biol Chem. 1988 Oct 25;263(30):15506–15512. [PubMed] [Google Scholar]
  41. Xanthoudakis S., Miao G., Wang F., Pan Y. C., Curran T. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 1992 Sep;11(9):3323–3335. doi: 10.1002/j.1460-2075.1992.tb05411.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yamauchi A., Masutani H., Tagaya Y., Wakasugi N., Mitsui A., Nakamura H., Inamoto T., Ozawa K., Yodoi J. Lymphocyte transformation and thiol compounds; the role of ADF/thioredoxin as an endogenous reducing agent. Mol Immunol. 1992 Feb;29(2):263–270. doi: 10.1016/0161-5890(92)90108-a. [DOI] [PubMed] [Google Scholar]
  43. Yodoi J., Tursz T. ADF, a growth-promoting factor derived from adult T cell leukemia and homologous to thioredoxin: involvement in lymphocyte immortalization by HTLV-I and EBV. Adv Cancer Res. 1991;57:381–411. doi: 10.1016/s0065-230x(08)61004-0. [DOI] [PubMed] [Google Scholar]
  44. Yodoi J., Uchiyama T. Diseases associated with HTLV-I: virus, IL-2 receptor dysregulation and redox regulation. Immunol Today. 1992 Oct;13(10):405–411. doi: 10.1016/0167-5699(92)90091-K. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES