Endogenous production of tumour necrosis factor is required for manganese superoxide dismutase expression by irradiation in the human monocytic cell line THP-1.
Journal: 1998/January - Biochemical Journal
ISSN: 0264-6021
PUBMED: 9371723
Abstract:
Manganese superoxide dismutase (MnSOD) is a mitochondrial enzyme that scavenges superoxide (O2-) ions. We studied the regulation of MnSOD gene expression by irradiation and the mechanisms in human monocytic cell line THP-1. We found that irradiation induced expression of the MnSOD gene through the autocrine mechanism, involving the production of tumour necrosis factor (TNF). Irradiation increased TNF production in THP-1 cells, and TNF increased the levels of MnSOD transcripts. Supernatant from irradiated THP-1 cells induced the expression of MnSOD mRNA, and anti-TNF antibody blocked the induction of MnSOD mRNA. Irradiation also increased the levels of MnSOD mRNA in other myelocytic cell lines, HL60 and KG-1, and the ovarian cancer cell line SK-OV-3. Moreover, increased levels of MnSOD mRNA were observed in mature myeloid cells, including macrophages and granulocytes, as well as in immature cells. However, irradiation did not increase the level of MnSOD mRNA in THP-1 cells with prolonged exposure to PMA. We also found that irradiation increased the rate of MnSOD transcription, and irradiation stabilized MnSOD mRNA in THP-1 cells. Our results indicate that the endogenous production of TNF is required, at least in part, for the induction of MnSOD mRNA expression by irradiation in THP-1 cells, and the increased levels of MnSOD transcripts on irradiation occur through a pathway involving protein kinase C activation. Our results also indicate that the increase in MnSOD mRNA caused by irradiation is regulated by both transcriptional and post-transcriptional mechanisms.
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Biochem J 328(Pt 2): 615-623

Endogenous production of tumour necrosis factor is required for manganese superoxide dismutase expression by irradiation in the human monocytic cell line THP-1.

Abstract

Manganese superoxide dismutase (MnSOD) is a mitochondrial enzyme that scavenges superoxide (O2-) ions. We studied the regulation of MnSOD gene expression by irradiation and the mechanisms in human monocytic cell line THP-1. We found that irradiation induced expression of the MnSOD gene through the autocrine mechanism, involving the production of tumour necrosis factor (TNF). Irradiation increased TNF production in THP-1 cells, and TNF increased the levels of MnSOD transcripts. Supernatant from irradiated THP-1 cells induced the expression of MnSOD mRNA, and anti-TNF antibody blocked the induction of MnSOD mRNA. Irradiation also increased the levels of MnSOD mRNA in other myelocytic cell lines, HL60 and KG-1, and the ovarian cancer cell line SK-OV-3. Moreover, increased levels of MnSOD mRNA were observed in mature myeloid cells, including macrophages and granulocytes, as well as in immature cells. However, irradiation did not increase the level of MnSOD mRNA in THP-1 cells with prolonged exposure to PMA. We also found that irradiation increased the rate of MnSOD transcription, and irradiation stabilized MnSOD mRNA in THP-1 cells. Our results indicate that the endogenous production of TNF is required, at least in part, for the induction of MnSOD mRNA expression by irradiation in THP-1 cells, and the increased levels of MnSOD transcripts on irradiation occur through a pathway involving protein kinase C activation. Our results also indicate that the increase in MnSOD mRNA caused by irradiation is regulated by both transcriptional and post-transcriptional mechanisms.

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  • Unanue ER, Allen PM. The basis for the immunoregulatory role of macrophages and other accessory cells. Science. 1987 May 1;236(4801):551–557. [PubMed] [Google Scholar]
  • Nathan CF. Secretory products of macrophages. J Clin Invest. 1987 Feb;79(2):319–326.[PMC free article] [PubMed] [Google Scholar]
  • Fridovich I. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem. 1989 May 15;264(14):7761–7764. [PubMed] [Google Scholar]
  • Taniguchi N. Clinical significances of superoxide dismutases: changes in aging, diabetes, ischemia, and cancer. Adv Clin Chem. 1992;29:1–59. [PubMed] [Google Scholar]
  • Fujii J, Taniguchi N. Phorbol ester induces manganese-superoxide dismutase in tumor necrosis factor-resistant cells. J Biol Chem. 1991 Dec 5;266(34):23142–23146. [PubMed] [Google Scholar]
  • Harris CA, Derbin KS, Hunte-McDonough B, Krauss MR, Chen KT, Smith DM, Epstein LB. Manganese superoxide dismutase is induced by IFN-gamma in multiple cell types. Synergistic induction by IFN-gamma and tumor necrosis factor or IL-1. J Immunol. 1991 Jul 1;147(1):149–154. [PubMed] [Google Scholar]
  • Masuda A, Longo DL, Kobayashi Y, Appella E, Oppenheim JJ, Matsushima K. Induction of mitochondrial manganese superoxide dismutase by interleukin 1. FASEB J. 1988 Dec;2(15):3087–3091. [PubMed] [Google Scholar]
  • Visner GA, Dougall WC, Wilson JM, Burr IA, Nick HS. Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor. Role in the acute inflammatory response. J Biol Chem. 1990 Feb 15;265(5):2856–2864. [PubMed] [Google Scholar]
  • Wong GH, Goeddel DV. Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science. 1988 Nov 11;242(4880):941–944. [PubMed] [Google Scholar]
  • Warner BB, Stuart L, Gebb S, Wispé JR. Redox regulation of manganese superoxide dismutase. Am J Physiol. 1996 Jul;271(1 Pt 1):L150–L158. [PubMed] [Google Scholar]
  • Wong GH. Protective roles of cytokines against radiation: induction of mitochondrial MnSOD. Biochim Biophys Acta. 1995 May 24;1271(1):205–209. [PubMed] [Google Scholar]
  • Lin PS, Ho KC, Sung SJ, Tsai S. Cytotoxicity and manganese superoxide dismutase induction by tumor necrosis factor-alpha and ionizing radiation in MCF-7 human breast carcinoma cells. Lymphokine Cytokine Res. 1993 Oct;12(5):303–308. [PubMed] [Google Scholar]
  • Fridovich I. The biology of oxygen radicals. Science. 1978 Sep 8;201(4359):875–880. [PubMed] [Google Scholar]
  • Clark IA, Cowden WB, Hunt NH. Free radical-induced pathology. Med Res Rev. 1985 Jul-Sep;5(3):297–332. [PubMed] [Google Scholar]
  • Hirose K, Longo DL, Oppenheim JJ, Matsushima K. Overexpression of mitochondrial manganese superoxide dismutase promotes the survival of tumor cells exposed to interleukin-1, tumor necrosis factor, selected anticancer drugs, and ionizing radiation. FASEB J. 1993 Feb 1;7(2):361–368. [PubMed] [Google Scholar]
  • Scott MD, Meshnick SR, Eaton JW. Superoxide dismutase amplifies organismal sensitivity to ionizing radiation. J Biol Chem. 1989 Feb 15;264(5):2498–2501. [PubMed] [Google Scholar]
  • Cross CE, Halliwell B, Borish ET, Pryor WA, Ames BN, Saul RL, McCord JM, Harman D. Oxygen radicals and human disease. Ann Intern Med. 1987 Oct;107(4):526–545. [PubMed] [Google Scholar]
  • Akashi M, Hachiya M, Koeffler HP, Suzuki G. Irradiation increases levels of GM-CSF through RNA stabilization which requires an AU-rich region in cancer cells. Biochem Biophys Res Commun. 1992 Dec 15;189(2):986–993. [PubMed] [Google Scholar]
  • Hachiya M, Suzuki G, Koeffler HP, Akashi M. Irradiation increases expression of GM-CSF in human fibroblasts by transcriptional and post-transcriptional regulation. Exp Cell Res. 1994 Sep;214(1):343–350. [PubMed] [Google Scholar]
  • Hallahan DE, Virudachalam S, Sherman ML, Huberman E, Kufe DW, Weichselbaum RR. Tumor necrosis factor gene expression is mediated by protein kinase C following activation by ionizing radiation. Cancer Res. 1991 Sep 1;51(17):4565–4569. [PubMed] [Google Scholar]
  • Hallahan DE, Sukhatme VP, Sherman ML, Virudachalam S, Kufe D, Weichselbaum RR. Protein kinase C mediates x-ray inducibility of nuclear signal transducers EGR1 and JUN. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2156–2160.[PMC free article] [PubMed] [Google Scholar]
  • Sherman ML, Datta R, Hallahan DE, Weichselbaum RR, Kufe DW. Regulation of tumor necrosis factor gene expression by ionizing radiation in human myeloid leukemia cells and peripheral blood monocytes. J Clin Invest. 1991 May;87(5):1794–1797.[PMC free article] [PubMed] [Google Scholar]
  • Witte L, Fuks Z, Haimovitz-Friedman A, Vlodavsky I, Goodman DS, Eldor A. Effects of irradiation on the release of growth factors from cultured bovine, porcine, and human endothelial cells. Cancer Res. 1989 Sep 15;49(18):5066–5072. [PubMed] [Google Scholar]
  • Woloschak GE, Chang-Liu CM, Jones PS, Jones CA. Modulation of gene expression in Syrian hamster embryo cells following ionizing radiation. Cancer Res. 1990 Jan 15;50(2):339–344. [PubMed] [Google Scholar]
  • Neta R, Oppenheim JJ. Cytokines in therapy of radiation injury. Blood. 1988 Sep;72(3):1093–1095. [PubMed] [Google Scholar]
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. [PubMed] [Google Scholar]
  • Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971 Nov;44(1):276–287. [PubMed] [Google Scholar]
  • Oberley LW, Spitz DR. Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol. 1984;105:457–464. [PubMed] [Google Scholar]
  • Pennica D, Nedwin GE, Hayflick JS, Seeburg PH, Derynck R, Palladino MA, Kohr WJ, Aggarwal BB, Goeddel DV. Human tumour necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature. 1984 Dec 20;312(5996):724–729. [PubMed] [Google Scholar]
  • Auron PE, Webb AC, Rosenwasser LJ, Mucci SF, Rich A, Wolff SM, Dinarello CA. Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7907–7911.[PMC free article] [PubMed] [Google Scholar]
  • Ponte P, Gunning P, Blau H, Kedes L. Human actin genes are single copy for alpha-skeletal and alpha-cardiac actin but multicopy for beta- and gamma-cytoskeletal genes: 3' untranslated regions are isotype specific but are conserved in evolution. Mol Cell Biol. 1983 Oct;3(10):1783–1791.[PMC free article] [PubMed] [Google Scholar]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed] [Google Scholar]
  • Rovera G, Santoli D, Damsky C. Human promyelocytic leukemia cells in culture differentiate into macrophage-like cells when treated with a phorbol diester. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2779–2783.[PMC free article] [PubMed] [Google Scholar]
  • Koeffler HP. Induction of differentiation of human acute myelogenous leukemia cells: therapeutic implications. Blood. 1983 Oct;62(4):709–721. [PubMed] [Google Scholar]
  • Marklund SL, Westman NG, Roos G, Carlsson J. Radiation resistance and the CuZn superoxide dismutase, Mn superoxide dismutase, catalase, and glutathione peroxidase activities of seven human cell lines. Radiat Res. 1984 Oct;100(1):115–123. [PubMed] [Google Scholar]
  • Davies KJ, Doroshow JH. Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem. 1986 Mar 5;261(7):3060–3067. [PubMed] [Google Scholar]
  • Davies KJ, Doroshow JH, Hochstein P. Mitochondrial NADH dehydrogenase-catalyzed oxygen radical production by adriamycin, and the relative inactivity of 5-iminodaunorubicin. FEBS Lett. 1983 Mar 7;153(1):227–230. [PubMed] [Google Scholar]
  • Doroshow JH. Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4514–4518.[PMC free article] [PubMed] [Google Scholar]
  • Richter C, Park JW, Ames BN. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6465–6467.[PMC free article] [PubMed] [Google Scholar]
  • Brown WM, George M, Jr, Wilson AC. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971.[PMC free article] [PubMed] [Google Scholar]
  • Le J, Vilcek J. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab Invest. 1987 Mar;56(3):234–248. [PubMed] [Google Scholar]
  • Hallahan DE, Spriggs DR, Beckett MA, Kufe DW, Weichselbaum RR. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10104–10107.[PMC free article] [PubMed] [Google Scholar]
  • Faure E, Cavard C, Zider A, Guillet JP, Resbeut M, Champion S. X irradiation-induced transcription from the HIV type 1 long terminal repeat. AIDS Res Hum Retroviruses. 1995 Jan;11(1):41–43. [PubMed] [Google Scholar]
  • Lin CS, Goldthwait DA, Samols D. Induction of transcription from the long terminal repeat of Moloney murine sarcoma provirus by UV-irradiation, x-irradiation, and phorbol ester. Proc Natl Acad Sci U S A. 1990 Jan;87(1):36–40.[PMC free article] [PubMed] [Google Scholar]
  • Sherman ML, Datta R, Hallahan DE, Weichselbaum RR, Kufe DW. Ionizing radiation regulates expression of the c-jun protooncogene. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5663–5666.[PMC free article] [PubMed] [Google Scholar]
  • Hallahan DE, Dunphy E, Virudachalam S, Sukhatme VP, Kufe DW, Weichselbaum RR. C-jun and Egr-1 participate in DNA synthesis and cell survival in response to ionizing radiation exposure. J Biol Chem. 1995 Dec 22;270(51):30303–30309. [PubMed] [Google Scholar]
  • Beck Y, Oren R, Amit B, Levanon A, Gorecki M, Hartman JR. Human Mn superoxide dismutase cDNA sequence. Nucleic Acids Res. 1987 Nov 11;15(21):9076–9076.[PMC free article] [PubMed] [Google Scholar]
  • Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science. 1992 Oct 23;258(5082):607–614. [PubMed] [Google Scholar]
  • Ballester R, Rosen OM. Fate of immunoprecipitable protein kinase C in GH3 cells treated with phorbol 12-myristate 13-acetate. J Biol Chem. 1985 Dec 5;260(28):15194–15199. [PubMed] [Google Scholar]
  • Blackshear PJ, Witters LA, Girard PR, Kuo JF, Quamo SN. Growth factor-stimulated protein phosphorylation in 3T3-L1 cells. Evidence for protein kinase C-dependent and -independent pathways. J Biol Chem. 1985 Oct 25;260(24):13304–13315. [PubMed] [Google Scholar]
  • Lamph WW, Wamsley P, Sassone-Corsi P, Verma IM. Induction of proto-oncogene JUN/AP-1 by serum and TPA. Nature. 1988 Aug 18;334(6183):629–631. [PubMed] [Google Scholar]
  • Uckun FM, Tuel-Ahlgren L, Song CW, Waddick K, Myers DE, Kirihara J, Ledbetter JA, Schieven GL. Ionizing radiation stimulates unidentified tyrosine-specific protein kinases in human B-lymphocyte precursors, triggering apoptosis and clonogenic cell death. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9005–9009.[PMC free article] [PubMed] [Google Scholar]
  • Asayama K, Janco RL, Burr IM. Selective induction of manganous superoxide dismutase in human monocytes. Am J Physiol. 1985 Nov;249(5 Pt 1):C393–C397. [PubMed] [Google Scholar]
  • Kizaki M, Sakashita A, Karmakar A, Lin CW, Koeffler HP. Regulation of manganese superoxide dismutase and other antioxidant genes in normal and leukemic hematopoietic cells and their relationship to cytotoxicity by tumor necrosis factor. Blood. 1993 Aug 15;82(4):1142–1150. [PubMed] [Google Scholar]
Division of Radiation Health, National Institute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba-city, Chiba, 263 Japan.
Division of Radiation Health, National Institute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba-city, Chiba, 263 Japan.

Abstract

Manganese superoxide dismutase (MnSOD) is a mitochondrial enzyme that scavenges superoxide (O2-) ions. We studied the regulation of MnSOD gene expression by irradiation and the mechanisms in human monocytic cell line THP-1. We found that irradiation induced expression of the MnSOD gene through the autocrine mechanism, involving the production of tumour necrosis factor (TNF). Irradiation increased TNF production in THP-1 cells, and TNF increased the levels of MnSOD transcripts. Supernatant from irradiated THP-1 cells induced the expression of MnSOD mRNA, and anti-TNF antibody blocked the induction of MnSOD mRNA. Irradiation also increased the levels of MnSOD mRNA in other myelocytic cell lines, HL60 and KG-1, and the ovarian cancer cell line SK-OV-3. Moreover, increased levels of MnSOD mRNA were observed in mature myeloid cells, including macrophages and granulocytes, as well as in immature cells. However, irradiation did not increase the level of MnSOD mRNA in THP-1 cells with prolonged exposure to PMA. We also found that irradiation increased the rate of MnSOD transcription, and irradiation stabilized MnSOD mRNA in THP-1 cells. Our results indicate that the endogenous production of TNF is required, at least in part, for the induction of MnSOD mRNA expression by irradiation in THP-1 cells, and the increased levels of MnSOD transcripts on irradiation occur through a pathway involving protein kinase C activation. Our results also indicate that the increase in MnSOD mRNA caused by irradiation is regulated by both transcriptional and post-transcriptional mechanisms.

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