Home LiteratureArticle Details
PMID: 17895890 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural

Molecular consequences of SOD2 expression in epigenetically silenced pancreatic carcinoma cell lines.

British journal of cancer ·Vol. 97 ·No. 8 ·2007-10-22 ·Pages 1116-23

Hurt EM, Thomas SB, Peng B, Farrar WL

Abstract

Manganese superoxide dismutase (SOD2) is an enzyme that catalyses the dismutation of superoxide in the mitochondria, leading to reduced levels of reactive oxygen species. Reduced expression levels of SOD2 have been shown to result in increased DNA damage and sod2 heterozygous mice have increased incidences of cancer. It has also been shown that SOD2 expression is lost in pancreatic cell lines, with reintroduction of SOD2 resulting in decreased rate of proliferation. The mechanism of decreased SOD2 expression in pancreatic carcinoma has not been previously determined. We demonstrate, through sodium bisulphite sequencing, that the sod2 locus is methylated in some pancreatic cell lines leading to a corresponding decrease in SOD2 expression. Methylation can be reversed by treatment with zebularine, a methyltransferase inhibitor, resulting in restored SOD2 expression. Furthermore, we demonstrate that sensitivity of pancreatic carcinoma cell lines to 2-methoxyestradiol correlates with SOD2 expression and SOD2 modulation can alter the sensitivity of these cells. Using both genomics and proteomics, we also identify molecular consequences of SOD2 expression in MIA-PaCa2 cells, including dephosphorylation of VEGFR2 and the identification of both SOD2-regulated genes and transcription factors with altered binding activity in response to SOD2 expression.

MeSH Terms
2-Methoxyestradiol Animals Carcinoma/enzymology,genetics Cell Line, Tumor DNA Methylation Epigenesis, Genetic Estradiol/analogs & derivatives,pharmacology Gene Expression Gene Expression Profiling Gene Expression Regulation, Enzymologic Mice Oligonucleotide Array Sequence Analysis Oxidative Stress/physiology Pancreatic Neoplasms/enzymology,genetics Promoter Regions, Genetic/genetics Reverse Transcriptase Polymerase Chain Reaction Superoxide Dismutase/genetics,metabolism Tubulin Modulators/pharmacology Vascular Endothelial Growth Factor Receptor-2/metabolism
Chemicals
Tubulin Modulators Estradiol 2-Methoxyestradiol Superoxide Dismutase superoxide dismutase 2 Vascular Endothelial Growth Factor Receptor-2
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hurt E M
Laboratory of Cancer Prevention, Center for Cancer Research, National Cancer Institute at Frederick, National Institutes of Health, Frederick, MD 21702, USA. [email protected]
Thomas S B
Peng B
Farrar W L
References (33)
33 references, click to expand
  1. Epigenetic silencing of manganese superoxide dismutase (SOD-2) in KAS 6/1 human multiple myeloma cells increases cell proliferation.
    Cancer Biol Ther. 2005 May;4(5):585-92 PMID: 15908783
  2. Enforced expression of superoxide dismutase 2/manganese superoxide dismutase disrupts autocrine interleukin-6 stimulation in human multiple myeloma cells and enhances dexamethasone-induced apoptosis.
    Cancer Res. 2005 Jul 15;65(14):6255-63 PMID: 16024627
  3. Cross-talk between calcium and reactive oxygen species signaling.
    Acta Pharmacol Sin. 2006 Jul;27(7):821-6 PMID: 16787564
  4. Mechanisms of endothelial response to oxidative aggression: protective role of autologous VEGF and induction of VEGFR2 by H2O2.
    Am J Physiol Heart Circ Physiol. 2006 Sep;291(3):H1395-401 PMID: 16899768
  5. The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma.
    Cancer Res. 2003 Mar 15;63(6):1297-303 PMID: 12649190
  6. Radical causes of cancer.
    Nat Rev Cancer. 2003 Apr;3(4):276-85 PMID: 12671666
  7. Suppression of the malignant phenotype in human pancreatic cancer cells by the overexpression of manganese superoxide dismutase.
    Mol Cancer Ther. 2003 Apr;2(4):361-9 PMID: 12700280
  8. Superoxide-dependent and -independent mitochondrial signaling during apoptosis in multiple myeloma cells.
    Oncogene. 2003 Sep 18;22(40):6296-300 PMID: 13679868
  9. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging.
    Physiol Genomics. 2003 Dec 16;16(1):29-37 PMID: 14679299
  10. Redox regulation of pancreatic cancer cell growth: role of glutathione peroxidase in the suppression of the malignant phenotype.
    Hum Gene Ther. 2004 Mar;15(3):239-50 PMID: 15018733
  11. Alteration of cellular phenotype and responses to oxidative stress by manganese superoxide dismutase and a superoxide dismutase mimic in RWPE-2 human prostate adenocarcinoma cells.
    Antioxid Redox Signal. 2004 Jun;6(3):513-22 PMID: 15130278
  12. Biochemistry of oxygen toxicity.
    Annu Rev Biochem. 1989;58:79-110 PMID: 2673022
  13. Antitumor properties of 2(1H)-pyrimidinone riboside (zebularine) and its fluorinated analogues.
    J Med Chem. 1991 Nov;34(11):3280-4 PMID: 1956046
  14. Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase.
    Oncogene. 1997 Jan 30;14(4):481-90 PMID: 9053845
  15. Transfection and expression of MnSOD cDNA decreases tumor malignancy of human oral squamous carcinoma SCC-25 cells.
    Hum Gene Ther. 1997 Mar 20;8(5):585-95 PMID: 9095410
  16. 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
  17. Mitochondrial oxidative stress. Physiologic consequences and potential for a role in aging.
    Ann N Y Acad Sci. 2000 Jun;908:219-25 PMID: 10911961
  18. The molecular pathogenesis of prostate cancer: Implications for prostate cancer prevention.
    Urology. 2001 Apr;57(4 Suppl 1):39-45 PMID: 11295593
  19. Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front.
    Oncogene. 2001 Apr 12;20(16):1981-9 PMID: 11360182
  20. Overexpression of manganese superoxide dismutase suppresses tumor formation by modulation of activator protein-1 signaling in a multistage skin carcinogenesis model.
    Cancer Res. 2001 Aug 15;61(16):6082-8 PMID: 11507057
  21. MnSOD expression is less frequent in tumour cells of invasive breast carcinomas than in in situ carcinomas or non-neoplastic breast epithelial cells.
    J Pathol. 2001 Sep;195(2):156-62 PMID: 11592093
  22. GSTP1 CpG island hypermethylation is responsible for the absence of GSTP1 expression in human prostate cancer cells.
    Am J Pathol. 2001 Nov;159(5):1815-26 PMID: 11696442
  23. Superoxide dismutase is induced during rat pancreatic acinar cell injury.
    Pancreas. 2002 Mar;24(2):146-52 PMID: 11854619
  24. 2-Methoxyestradiol induces mitochondria dependent apoptotic signaling in pancreatic cancer cells.
    Oncogene. 2002 Jun 13;21(26):4149-57 PMID: 12037671
  25. Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases.
    J Mol Biol. 2002 Aug 23;321(4):591-9 PMID: 12206775
  26. Stable suppression of tumorigenicity by virus-mediated RNA interference.
    Cancer Cell. 2002 Sep;2(3):243-7 PMID: 12242156
  27. Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype.
    Prostate. 1998 May 15;35(3):221-33 PMID: 9582091
  28. Maspin gene expression in tumor suppression induced by overexpressing manganese-containing superoxide dismutase cDNA in human breast cancer cells.
    Carcinogenesis. 1998 May;19(5):833-9 PMID: 9635871
  29. Mutations in the promoter reveal a cause for the reduced expression of the human manganese superoxide dismutase gene in cancer cells.
    Oncogene. 1999 Jan 7;18(1):93-102 PMID: 9926924
  30. Potent antitumor activity of 2-methoxyestradiol in human pancreatic cancer cell lines.
    Clin Cancer Res. 1999 Mar;5(3):493-9 PMID: 10100698
  31. Inhibition of cell growth by overexpression of manganese superoxide dismutase (MnSOD) in human pancreatic carcinoma.
    Free Radic Res. 2004 Nov;38(11):1223-33 PMID: 15621700
  32. Manganese superoxide dismutase overexpression inhibits the growth of androgen-independent prostate cancer cells.
    Oncogene. 2005 Jan 6;24(1):77-89 PMID: 15543233
  33. Molecular alterations in primary prostate cancer after androgen ablation therapy.
    Clin Cancer Res. 2005 Oct 1;11(19 Pt 1):6823-34 PMID: 16203770
Article Info
Journal
British journal of cancer
Abbr.
Br J Cancer
ISSN
0007-0920
Published
2007-10-22
Epub
2007-00-25
Pages
1116-23
Language
English
Region
England
NLM ID
0370635
PMCID
PMC2360443
Subset
IM
Grants
NCI NIH HHS · N01CO12400 · United States
NCI NIH HHS · N01-CO-12400 · United States
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]