Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP): Protective effect of human thioredoxin against CDDP-induced cytotoxicity

Journal of Clinical Investigation

Volumn 97, Issue 10, 1996, Pages 2268-2276

  Sasada, Tetsuro ^a   Iwata, Satoshi ^a   Sato, Norihito ^a   Kitaoka, Yuki ^a   Hirota, Kiichi ^a   Nakamura, Kazuhiro ^a   Nishiyama, Akira ^a   Taniguchi, Yoshihisa ^a   Takabayashi, Arimichi ^b   Yodoi, Junji ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Kitano Hospital   (Japan)

Author keywords

cis diamminedichloroplatinum (II); Human thioredoxin; Reactive oxygen intermediate; Redox; Resistance

Indexed keywords

BUTYLATED HYDROXYANISOLE; CHLORAMPHENICOL ACETYLTRANSFERASE; CISPLATIN; COMPLEMENTARY DNA; REACTIVE OXYGEN METABOLITE; THIOREDOXIN;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL STRAIN L 929; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DRUG RESISTANCE; GENE ACTIVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; REPORTER GENE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CISPLATIN; DNA REPLICATION; DRUG RESISTANCE; HUMANS; MICE; MICE, INBRED BALB C; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; THIOREDOXIN;

EID: 0029976986     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118668     Document Type: Article

References (62)

1. Holmgren, A. 1985. Thioredoxin. Annu. Rev. Biochem. 54:237-271.
2. Holmgren, A. 1989. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264:13963-13966.
3. 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 ATL-derived factor (ADF). J. Immunol. 140:2613-2620.
4. Tagaya, Y., Y. Maeda, A. Mitsui, N. Kondo, H. Matsui, J. Hamuro, N. Brown, K.-i. Arai, T. Yokota, H. Wakasugi, et al. 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.
5. Yodoi, J., and T. Uchiyama. 1992. Diseases associated with HTLV-I: virus, IL-2 receptor dysregulation and redox regulation. Immunol. Today. 13: 405-411.
6. Gasdaska, P.Y., J.E. Oblong, I.A. Cotgreave, and G. Powis. 1994. The predicted amino acid sequence of human thioredoxin is identical to that of the autocrine growth factor human adult T-cell leukemia derived factor (ADF): thioredoxin mRNA is elevated in some human tumors. Biochim. Biophys. Acta. 1218:292-296.
7. Okamoto, T., H. Ogiwara, T. Hayashi, A. Mitsui, T. Kawabe, and J. Yodoi. 1992. 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. 4:811-819.
8. 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.
9. Mitsui, A., T. Hirakawa, and J. Yodoi. 1992. Reactive oxygen-reducing and protein-refolding activities of adult T cell leukemia-derived factor/human thioredoxin. Biochem. Biophys. Res. Commun. 186:1220-1226.
10. Matsuda, M., H. Masutani, H. Nakamura, S. Miyajima, A. Yamauchi, S. Yonehara, A. Uchida, K. Irimajiri, A. Horiuchi, and J. Yodoi. 1992. Protective activity of ATL-derived factor (ADF) against tumor necrosis factor-dependent cytotoxicity on U937 cells. J. Immunol. 147:3837-3841.
11. Nakamura, H., M. Matsuda, K. Furuke, Y. Kitaoka, S. Iwata, K. Toda, T. Inamoto, Y. Yamaoka, K. Ozawa, and J. Yodoi. 1994. Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide. Immunol Lett. 42:75-80.
12. 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.
13. Chu, G. 1994. Cellular response to cisplatin. J. Biol. Chem. 269:787-790.
14. Timmer-Bosscha, H., N.H. Mulder, and E.G.E. de Vries. 1992. Modulation of cis-diamminedichloroplatinum (II) resistance: a review. Br. J. Cancer. 66:227-238.
15. McGinness, J.E., P.H. Proctor, H.B. Demopoulos, J.A. Hokanson, and D.S. Kirkpatrick. 1978. Amelioration of cis-platinum nephrotoxicity by Orgotein (superoxide dismutase). Physiol. Chem. Phys. 10:267-277.
16. Sugihara, K., and M. Gemba. 1986. Modification of cisplatin toxicity by antioxidants. Jpn. J. Pharmacol. 40:353-355.
17. Hannemann, J., and K. Baumann. 1988. Cisplatin-induced lipid peroxidation and decrease of gluconeogenesis in rat kidney cortex: different effects of antioxidants and radical scavengers. Toxicology. 51:119-132.
18. -) by murine macrophages in vitro after cisplatin treatment. Int. J. Immunopharmacol. 8:709-714.
19. Masuda, H., T. Tanaka, and U. Takahama. 1994. Cisplatin generates superoxide anion by interaction with DNA in a cell-free system. Biochem. Biophys. Res. Commun. 203:1175-1180.
20. Makino, S., H. Masutani, N. Maekawa, I. Konishi, S. Fujii, R. Yamamoto, and J. Yodoi. 1992. Adult T-cell leukemia-derived factor/thioredoxin expression on the HTLV-I transformed T-cell lines: heterogeneous expression in ATL-2 cells. Immunology. 76:578-583.
21. Fujii, S., Y. Nanbu, H. Nonogaki, I. Konishi, T. Mori, H. Masutani, and J. Yodoi. 1991. Coexpression of adult T-cell leukemia-derived factor, a human thioredoxin homologue, and human papilloma virus DNA in neoplastic cervical squamous epithelium. Cancer (Phila.). 68:1583-1591.
22. Nakamura, H., H. Masutani, Y. Tagaya, A. Yamauchi, T. Inamoto, Y. Nanbu, S. Fujii, K. Ozawa, and J. Yodoi. 1992. Expression and growth-promoting effect of adult T-cell Leukemia-derived factor: a human thioredoxin homologue in hepatocellular carcinoma. Cancer (Phila.). 69:2091-2097.
23. Huston, K., D. Silberstein, and D.R. Spriggs. 1994. Eosinophil cytotoxicity enhancing factor (ECEF) overexpression in human cancer cells with acquired cisplatin resistance. Proc. Am. Assoc. Cancer Res. Annual Meeting. 35: 2611. (Abstr.)
24. 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.
25. Kitaoka, Y., K. Sorachi, H. Nakamura, H. Masutani, A. Mitsui, F. Kobayashi, T. Mori, and J. Yodoi. 1995. Detection of adult T-cell leukemia-derived factor/human thioredoxin in human serum. Immunol. Lett. 41:155-161.
26. Luthman, M., and A. Holmgren. 1982. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry. 21:6628-6633.
27. Holmgren, A., and M. Björnstedt. 1995. Thioredoxin and thioredoxin reductase. Methods Enzymol. 252:199-208.
28. Oblong, J.E., P. Y. Gasdaska, K. Sherrill, and G. Powis. 1993. Purification of human thioredoxin reductase: properties and characterization by absorption and circular dichroism spectroscopy. Biochemistry. 32:7271-7277.
29. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 16.30-16.65.
30. Bass, D.A., J.W. Parce, L.R. Dechatelet, P. Szejda, M.C. Seeds, and M. Thomas. 1983. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J. Immunol. 130:1910-1917.
31. Southern, P.J., and P. Berg. 1982. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J. Mol. Appl. Genet. 1:327-341.
32. Israel, N., M.-A. Gougerot-Pocidalo, F. Aillet, and J.-L. Virelizier. 1992. Redox status of cells influences constitutive or induced NF-κB translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J. Immunol. 149:3386-3393.
33. Schulze-Osthoff, K., R. Beyaert, V. Vandevoorde, G. Haegeman, and W. Fiers. 1993. Depletion of the mitochondrial electron transport abrogates the cytotoxicand gene-inductive effects of TNF. EMBO (Eur. Mol. Biol. Organ.) J. 12:3095-3104.
34. Hollander, M.C., and A.J. Fornance. Jr. 1989. Induction of fos RNA by DNA-damaging agents. Cancer Res. 49:1687-1692.
35. Rubin, E., S. Kharbanda, H. Gunji, R. Weichselbaum, and D. Kufe. 1992. cis-diamminedichloroplatinum (II) induces c-jun expression in human myeloid leukemia cells: potential involvement of a protein kinase C-dependent signaling pathway. Cancer Res. 52:878-882.
36. Zoumpourlis, V., D.J. Kerr, and D.A. Spandidos. 1992. Carboplatin as opposed to cisplatin does not stimulate the expression of the human immunodeficiency virus long terminal repeat sequences. Biochem. Pharmacol. 43:650-654.
37. Devary, Y., R.A. Gottlieb, L.F. Lau, and M. Karin. 1991. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol. Cell. Biol. 11:2804-2811.
38. 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.
39. Buttke, T.M., and P.A. Sandstrom. 1994. Oxidative stress as a mediator of apoptosis. Immunol. Today. 15:7-10.
40. Hockenbery, D.M., Z.N. Oltvai, X.-M. Yin, C.L. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:241-251.
41. Kane, D.J., T.A. Sarafian, R. Anton, H. Hahn, E.B. Gralla, J.S. Valentine, T. Örd, and D.E. Bredesen. 1993. Bcl-2 inhibition of neuronal death: decreased generation of reactive oxygen species. Science (Wash. DC). 262:1274-1277.
42. Miyashita, T., and J.C. Reed. 1993. Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line. Blood. 81:151-157.
43. Dole, M., G. Nunez, A.K. Merchant, J. Maybaun, C.K. Rode, C.A. Bloch, and V.P. Castle. 1994. Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res. 54:3253-3259.
44. Chae, H.Z., S.J. Chung, and S.G. Rhee. 1994. Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 269:27670-27678.
45. Dedon, P.C., and R.F. Borch. 1987. Characterization of the reactions of platinum antitumor agents with biologic and nonbiologic sulfur-containing nucleophiles. Biochem. Pharmacol. 36:1955-1964.
46. Zelazowski, A.J., J.S. Garvey, and J.D. Hoeschele. 1984. In vivo and in vitro binding of platinum to metallothionein. Arch. Biochem. Biophys. 229:246-252.
47. Meijer, C., N.H. Mulder, G.A.P. Hospers, D.R.A. Uges, and E.G.E. de Varies. 1990. The role of glutathione in resistance to cisplatin in a human small cell lung cancer cell line. Br. J. Cancer. 62:72-77.
48. Godwin, A.K., A. Meister, P.J. O'Dwyer, C.S. Huang, T.C. Hamilton, and M.E. Anderson. 1992. High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc. Natl. Acad. Sci. USA. 89:3070-3074.
49. Andrews, P.A., M.P. Murphy, and S.B. Howell. 1987. Metallothionein-mediated cisplatin resistance in human ovarian carcinoma cells. Cancer Chemother Pharmacol. 19:149-154.
50. Kelly, S.L., A. Basu, B.A. Teicher, M.P. Hacker, D.H. Hamer, and J.S. Lazo. 1988. Overexpression of metallothionein confers resistance to anticancer drugs. Science (Wasn. DC). 241:1813-1815.
51. Iwata, S., T. Hori, N. Sato, Y. Ueda-Taniguchi, T. Yamabe, H. Nakamura, H. Masutani, and J. Yodoi. 1994. Thiol-medialed redox regulation of lymphocyte proliferation: possible involvement of adult T cell leukemia-derived factor and glutathione in transferrin receptor expression. J. Immunol. 152:5633-5642.
52. Hori, K., M. Katayama, N. Sato, K. Ishii, S. Waga, and J. Yodoi. 1994. Neuroprotection hy glial cells through adult T cell leukemia-derived factor/human thioredoxin (ADF/TRX). Brain Res. 652:304-310.
53. Sato, N., S. Iwata, K. Nakamura, T. Hori, K. Mori, and J. Yodoi. 1995. Thiol-mediated redox regulation of apoptosis: possible roles of cellular thiols other than glutathione in T cell apoplosis. J. Immunol. 154:3194-3203.
54. Smith, S.L., and K.T. Douglas. 1989. Stereoselective, strong inhibition of ribonucleolide reduclase from E. coli by cisplatin. Biochem. Biophys. Res. Commun. 162:715-723.
55. Chiu, C.S.M., A.K. Chan, and J.A. Wright. 1992. Inhibition of mammalian ribonucleotide reductase by cis-diamminedichloroplatinum(II). Biochem. Cell Biol. 70:1332-1338.
56. Mcclarty, G.A., A.K.M. Chan, and J.A. Wright. 1986. Hydroxyurea-induced conversion of mammalian ribonucleotide reductase to a form hypersensitive to bleomycin. Cancer Res. 46:4516-4521.
57. Hurta, R.A.R., and J.A. Wright. 1992. Alterations in the activity and regulation of mammalian ribonucleotide reductase by chlorambucil, a DNA damaging agent. J. Biol. Chem. 267:7066-7071.
58. Wells, W.W., P.A. Rocque, D.-P. Xu, Y. Yang, and T.L. Deits. 1991. Interaction of platinum complexes with thioltransferase (glutaredoxin), in vitro. Biochem. Biophys. Res. Commun. 180:735-741.
59. Björnstedt, M., M. Hamberg, S. Kumar, J. Xue, and A. Holmgren. 1995. Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J. Biol. Chem. 270:11761-11764.
60. Björnstedt, M., J. Xue, W. Huang, B. Akesson, and A. Holmgren. 1994. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269:29382-29384.
61. Arnér, E.S.J., M. Björnstedt, and A. Holmgren. 1995. 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. 270:3479-3482.
62. Toyokuni, S., K. Okamoto, J. Yodoi, and H. Hiai. 1995. Persistent oxidative stress in cancer. FEBS Lett. 358:1-3.