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PMID: 12640121 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses.

Molecular and cellular biology ·Vol. 23 ·No. 7 ·2003-04-00 ·Pages 2362-78

Guo G, Yan-Sanders Y, Lyn-Cook BD, Wang T, Tamae D, Ogi J, Khaletskiy A, Li Z, Weydert C, Longmate JA, Huang TT, Spitz DR, Oberley LW, Li JJ

Abstract

Antioxidant enzymes are critical in oxidative stress responses. Radioresistant variants isolated from MCF-7 human carcinoma cells following fractionated ionizing radiation (MCF+FIR cells) or overexpression of manganese superoxide dismutase (MCF+SOD cells) demonstrated dose-modifying factors at 10% isosurvival of 1.8 and 2.3, respectively. MCF+FIR and MCF-7 cells (exposed to single-dose radiation) demonstrated 5- to 10-fold increases in MnSOD activity, mRNA, and immunoreactive protein. Radioresistance in MCF+FIR and MCF+SOD cells was reduced following expression of antisense MnSOD. DNA microarray analysis and immunoblotting identified p21, Myc, 14-3-3 zeta, cyclin A, cyclin B1, and GADD153 as genes constitutively overexpressed (2- to 10-fold) in both MCF+FIR and MCF+SOD cells. Radiation-induced expression of these six genes was suppressed in fibroblasts from Sod2 knockout mice (-/-) as well as in MCF+FIR and MCF+SOD cells expressing antisense MnSOD. Inhibiting NF-kappa B transcriptional activity in MCF+FIR cells, by using mutant I kappa B alpha, inhibited radioresistance as well as reducing steady-state levels of MnSOD, 14-3-3 zeta, GADD153, cyclin A, and cyclin B1 mRNA. In contrast, mutant I kappa B alpha was unable to inhibit radioresistance or reduce 14-3-3 zeta, GADD153, cyclin A, and cyclin B1 mRNAs in MCF+SOD cells, where MnSOD overexpression was independent of NF-kappa B. These results support the hypothesis that NF-kappa B is capable of regulating the expression of MnSOD, which in turn is capable of increasing the expression of genes that participate in radiation-induced adaptive responses.

MeSH Terms
14-3-3 Proteins Adaptation, Physiological/physiology,radiation effects Adenocarcinoma/metabolism,radiotherapy Animals Breast Neoplasms/metabolism,radiotherapy CCAAT-Enhancer-Binding Proteins/genetics,metabolism Cell Line Cell Survival/radiation effects Cyclin A/genetics,metabolism Cyclin B/genetics,metabolism Cyclin B1 Dose Fractionation, Radiation Dose-Response Relationship, Radiation Female Fibroblasts/cytology,drug effects,radiation effects Gamma Rays Gene Expression Profiling Gene Expression Regulation, Neoplastic/physiology,radiation effects Humans I-kappa B Proteins/biosynthesis,genetics,pharmacology Mice Mice, Knockout NF-KappaB Inhibitor alpha NF-kappa B/antagonists & inhibitors Oligonucleotide Array Sequence Analysis RNA, Messenger/metabolism Radiation Tolerance/genetics,physiology,radiation effects Superoxide Dismutase/deficiency,genetics,metabolism Transcription Factor CHOP Transcription Factors/genetics,metabolism Tyrosine 3-Monooxygenase/genetics,metabolism
Chemicals
14-3-3 Proteins CCAAT-Enhancer-Binding Proteins CCNB1 protein, human Ccnb1 protein, mouse Cyclin A Cyclin B Cyclin B1 DDIT3 protein, human Ddit3 protein, mouse I-kappa B Proteins NF-kappa B NFKBIA protein, human Nfkbia protein, mouse RNA, Messenger Transcription Factors NF-KappaB Inhibitor alpha Transcription Factor CHOP Tyrosine 3-Monooxygenase Superoxide Dismutase superoxide dismutase 2
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Guo Guozheng
Radiation Biology, Division of Radiation Oncology, City of Hope National Medical Center, Duarte, California 91010, USA.
Yan-Sanders Yan
Lyn-Cook Beverly D
Wang Tieli
Tamae Daniel
Ogi Julie
Khaletskiy Alexander
Li Zhongkui
Weydert Christine
Longmate Jeffrey A
Huang Ting-Ting
Spitz Douglas R
Oberley Larry W
Li Jian Jian
References (67)
67 references, click to expand
  1. Fluorescent cDNA microarray hybridization reveals complexity and heterogeneity of cellular genotoxic stress responses.
    Oncogene. 1999 Jun 17;18(24):3666-72 PMID: 10380890
  2. The complexity of radiation stress responses: analysis by informatics and functional genomics approaches.
    Gene Expr. 1999;7(4-6):387-400 PMID: 10440239
  3. Induction of stress genes by low doses of gamma rays.
    Radiat Res. 1999 Sep;152(3):225-31 PMID: 10453082
  4. Hypoxia--a key regulatory factor in tumour growth.
    Nat Rev Cancer. 2002 Jan;2(1):38-47 PMID: 11902584
  5. NF-kappaB-dependent MnSOD expression protects adenocarcinoma cells from TNF-alpha-induced apoptosis.
    Oncogene. 2002 May 30;21(24):3917-24 PMID: 12032830
  6. Activation of matrix metalloproteinase-2 by overexpression of manganese superoxide dismutase in human breast cancer MCF-7 cells involves reactive oxygen species.
    J Biol Chem. 2002 Jun 7;277(23):20919-26 PMID: 11929863
  7. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-kappaB activity that facilitates MnSOD-mediated ROS elimination.
    Mol Cell. 2002 May;9(5):1017-29 PMID: 12049738
  8. The c-Rel transcription factor can both induce and inhibit apoptosis in the same cells via the upregulation of MnSOD.
    Oncogene. 2002 Jun 27;21(28):4392-402 PMID: 12080470
  9. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.
    Anal Biochem. 1971 Nov;44(1):276-87 PMID: 4943714
  10. Superoxide dismutase activities of differentiating clones from an immortal cell line.
    J Cell Physiol. 1989 Jan;138(1):50-60 PMID: 2910887
  11. Irradiation increases superoxide dismutase in rat intestinal smooth muscle.
    Free Radic Biol Med. 1989;6(3):261-70 PMID: 2744576
  12. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor.
    Cell. 1989 Sep 8;58(5):923-31 PMID: 2476237
  13. Oxygen toxicity in control and H2O2-resistant Chinese hamster fibroblast cell lines.
    Arch Biochem Biophys. 1990 Jun;279(2):249-60 PMID: 2350176
  14. Tumor cell drug and radiation resistance: does an interrelationship exist?
    Cancer Treat Res. 1989;48:189-203 PMID: 2577138
  15. The induction of gene expression in mammalian cells by radiation.
    Semin Cancer Biol. 1993 Apr;4(2):119-28 PMID: 8513147
  16. Expression of manganese superoxide dismutase promotes cellular differentiation.
    Free Radic Biol Med. 1994 Feb;16(2):275-82 PMID: 7516302
  17. The molecular basis for cell cycle delays following ionizing radiation: a review.
    Radiother Oncol. 1994 Apr;31(1):1-13 PMID: 8041894
  18. Role of intracellular SOD in protecting human leukemic and cancer cells against superoxide and radiation.
    Free Radic Biol Med. 1994 Nov;17(5):389-95 PMID: 7835745
  19. Molecular structure and organization of the human manganese superoxide dismutase gene.
    DNA Cell Biol. 1994 Nov;13(11):1127-36 PMID: 7702755
  20. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase.
    Oncogene. 1995 May 18;10(10):1989-2000 PMID: 7761099
  21. Protective roles of cytokines against radiation: induction of mitochondrial MnSOD.
    Biochim Biophys Acta. 1995 May 24;1271(1):205-9 PMID: 7599209
  22. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction.
    Science. 1995 Oct 13;270(5234):296-9 PMID: 7569979
  23. Manganese-containing superoxide dismutase overexpression causes phenotypic reversion in SV40-transformed human lung fibroblasts.
    Cancer Res. 1996 Jun 15;56(12):2864-71 PMID: 8665527
  24. Antioxidant and glutathione-associated enzymes in Wilms' tumour after chemotherapy.
    J Cancer Res Clin Oncol. 1996;122(8):483-8 PMID: 8698748
  25. Biologic basis for radiation oncology.
    Oncology (Williston Park). 1996 Mar;10(3):399-411; discussion: 411-5 PMID: 8820451
  26. NF-kappa B: ten years after.
    Cell. 1996 Oct 4;87(1):13-20 PMID: 8858144
  27. Inhibition of cell growth and sensitization to oxidative damage by overexpression of manganese superoxide dismutase in rat glioma cells.
    Cell Growth Differ. 1996 Sep;7(9):1175-86 PMID: 8877099
  28. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L)
    Cell. 1996 Nov 15;87(4):619-28 PMID: 8929531
  29. The manganese superoxide dismutase gene of Drosophila: structure, expression, and evidence for regulation by MAP kinase.
    DNA Cell Biol. 1997 Apr;16(4):391-9 PMID: 9150426
  30. Superoxide-mediated cytotoxicity in superoxide dismutase-deficient fetal fibroblasts.
    Arch Biochem Biophys. 1997 Aug 15;344(2):424-32 PMID: 9264557
  31. Tumor necrosis factor alpha and interleukin-1beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB.
    Mol Cell Biol. 1997 Dec;17(12):6970-81 PMID: 9372929
  32. Overexpression of manganese superoxide dismutase selectively modulates the activity of Jun-associated transcription factors in fibrosarcoma cells.
    Cancer Res. 1997 Dec 1;57(23):5265-71 PMID: 9393747
  33. The structural basis for 14-3-3:phosphopeptide binding specificity.
    Cell. 1997 Dec 26;91(7):961-71 PMID: 9428519
  34. Effects of pre-exposure of mouse testis with low-dose (16)O8+ ions or 60Co gamma-rays on sperm shape abnormalities, lipid peroxidation and superoxide dismutase (SOD) activity induced by subsequent high-dose irradiation.
    Int J Radiat Biol. 1998 Feb;73(2):163-7 PMID: 9489563
  35. Role of antioxidant enzymes on ionizing radiation resistance.
    Free Radic Biol Med. 1998 Mar 1;24(4):586-93 PMID: 9559871
  36. Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1.
    J Biol Chem. 1998 May 22;273(21):13245-54 PMID: 9582369
  37. Efficacy of recombinant methioninase in combination with cisplatin on human colon tumors in nude mice.
    Clin Cancer Res. 1999 Aug;5(8):2157-63 PMID: 10473100
  38. An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta.
    DNA Cell Biol. 1999 Sep;18(9):709-22 PMID: 10492402
  39. Increase in manganese superoxide dismutase activity in the mouse heart after X-irradiation.
    Arch Biochem Biophys. 1987 Apr;254(1):69-80 PMID: 3579307
  40. Principles of chemoradiation: theoretical and practical considerations.
    Oncology (Williston Park). 1999 Oct;13(10 Suppl 5):11-22 PMID: 10550823
  41. Role of redox potential and reactive oxygen species in stress signaling.
    Oncogene. 1999 Nov 1;18(45):6104-11 PMID: 10557101
  42. Inhibition of NF-kappaB, clonogenicity, and radiosensitivity of human cancer cells.
    J Natl Cancer Inst. 1999 Nov 17;91(22):1956-60 PMID: 10564680
  43. Control of apoptosis by Rel/NF-kappaB transcription factors.
    Oncogene. 1999 Nov 22;18(49):6910-24 PMID: 10602466
  44. Nuclear factor-kappaB activation by the photochemotherapeutic agent verteporfin.
    Blood. 2000 Jan 1;95(1):256-62 PMID: 10607710
  45. Molecular mechanisms of radiation-induced accelerated repopulation.
    Radiat Oncol Investig. 1999;7(6):321-30 PMID: 10644055
  46. 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades.
    EMBO J. 2000 Feb 1;19(3):349-58 PMID: 10654934
  47. Cellular commitment to radiation-induced apoptosis.
    Radiat Res. 2000 Mar;153(3):347-50 PMID: 10669558
  48. Intratracheal injection of manganese superoxide dismutase (MnSOD) plasmid/liposomes protects normal lung but not orthotopic tumors from irradiation.
    Gene Ther. 2000 Jun;7(12):1011-8 PMID: 10871749
  49. The role of cellular glutathione peroxidase redox regulation in the suppression of tumor cell growth by manganese superoxide dismutase.
    Cancer Res. 2000 Jul 15;60(14):3927-39 PMID: 10919671
  50. Nuclear factor kappaB-dependent mechanisms coordinate the synergistic effect of PMA and cytokines on the induction of superoxide dismutase 2.
    Biochem J. 2001 Jan 1;353(Pt 1):147-156 PMID: 11115408
  51. Modulation of radiation-induced cytokine elevation associated with esophagitis and esophageal stricture by manganese superoxide dismutase-plasmid/liposome (SOD2-PL) gene therapy.
    Radiat Res. 2001 Jan;155(1 Pt 1):2-14 PMID: 11121210
  52. Genes regulated in human breast cancer cells overexpressing manganese-containing superoxide dismutase.
    Free Radic Biol Med. 2001 Feb 1;30(3):260-7 PMID: 11165872
  53. Effector genes altered in MCF-7 human breast cancer cells after exposure to fractionated ionizing radiation.
    Radiat Res. 2001 Apr;155(4):543-53 PMID: 11260656
  54. Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB.
    Nat Cell Biol. 2001 Apr;3(4):409-16 PMID: 11283615
  55. Anticancer therapy by overexpression of superoxide dismutase.
    Antioxid Redox Signal. 2001 Jun;3(3):461-72 PMID: 11491657
  56. Indomethacin-induced radiosensitization and inhibition of ionizing radiation-induced NF-kappaB activation in HeLa cells occur via a mechanism involving p38 MAP kinase.
    Cancer Res. 2001 Oct 15;61(20):7689-96 PMID: 11606413
  57. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling.
    Nature. 2001 Nov 15;414(6861):308-13 PMID: 11713530
  58. Inhibition of JNK activation through NF-kappaB target genes.
    Nature. 2001 Nov 15;414(6861):313-7 PMID: 11713531
  59. Activation of nuclear factor kappaB in radioresistance of TP53-inactive human keratinocytes.
    Cancer Res. 2002 Feb 15;62(4):1213-21 PMID: 11861406
  60. The DNA-dependent protein kinase participates in the activation of NF kappa B following DNA damage.
    Biochem Biophys Res Commun. 1998 Jun 9;247(1):79-83 PMID: 9636658
  61. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice.
    J Biol Chem. 1998 Oct 23;273(43):28510-5 PMID: 9774481
  62. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress.
    Oncogene. 1998 Dec 24;17(25):3287-99 PMID: 9916991
  63. A multidrug-resistant breast cancer cell line induced by weekly exposure to doxorubicin.
    Int J Oncol. 1999 Feb;14(2):273-9 PMID: 9917502
  64. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor.
    Cell. 1999 Mar 19;96(6):857-68 PMID: 10102273
  65. Redox regulation of cellular signalling.
    Cell Signal. 1999 Jan;11(1):1-14 PMID: 10206339
  66. Antioxidant defenses in the TNF-treated MCF-7 cells: selective increase in MnSOD.
    Free Radic Biol Med. 1999 Apr;26(7-8):919-24 PMID: 10232835
  67. Induction of superoxide dismutase and cytotoxicity by manganese in human breast cancer cells.
    Arch Biochem Biophys. 1999 May 15;365(2):317-27 PMID: 10328827
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2003-04-00
Pages
2362-78
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC150726
Subset
IM
Grants
NHLBI NIH HHS · R01 HL51469 · United States
NCI NIH HHS · P01 CA066081 · United States
NCI NIH HHS · T32 CA078586 · United States
NHLBI NIH HHS · R01 HL051469 · United States
NCI NIH HHS · T32CA78586 · United States
NCI NIH HHS · P01 CA66081 · United States
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