Regulation of SOD2 in cancer by histone modifications and CpG Methylation: Closing the loop between redox biology and epigenetics

Antioxidants and Redox Signaling

Volumn 18, Issue 15, 2013, Pages 1946-1955

  Cyr, Anthony R ^a   Hitchler, Michael J ^b   Domann, Frederick E ^a  

^a UNIVERSITY OF IOWA   (United States)

^b KAISER PERMANENTE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; HISTONE; MANGANESE SUPEROXIDE DISMUTASE; OXYGEN; REACTIVE OXYGEN METABOLITE; SUCCINATE DEHYDROGENASE;

CANCER GROWTH; CARCINOGENESIS; CPG ISLAND; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; GENE CONTROL; GENE STRUCTURE; GENOMIC INSTABILITY; HISTONE ACETYLATION; HISTONE METHYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 84876105336     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4850     Document Type: Review

References (50)

1. Bubber P, Haroutunian V, Fisch G, Blass JP, and Gibson GE. Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann Neurol 57: 695-703, 2005. (Pubitemid 40628858)
2. Case AJ, McGill JL, Tygrett LT, Shirasawa T, Spitz DR, Waldschmidt TJ, Legge KL, and Domann FE. Elevated mitochondrial superoxide disrupts normal T cell development, impairing adaptive immune responses to an influenza challenge. Free Radic Biol Med 50: 448-458, 2011.
3. Cervera AM, Bayley JP, Devilee P, and McCreath KJ. Inhibition of succinate dehydrogenase dysregulates histone modification in mammalian cells. Mol Cancer 8: 89, 2009.
4. Cody DT, 2nd, Huang Y, Darby CJ, Johnson GK, and Domann FE. Differential DNA methylation of the p16 INK4A/CDKN2A promoter in human oral cancer cells and normal human oral keratinocytes. Oral Oncol 35: 516-522, 1999. (Pubitemid 29386789)
5. Cyr AR and Domann FE. The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 15: 551-589, 2011.
6. Dhar SK, Tangpong J, Chaiswing L, Oberley TD, and St Clair DK. Manganese superoxide dismutase is a p53-regulated gene that switches cancers between early and advanced stages. Cancer Res 71: 6684-6695, 2011.
7. Domann FE, Rice JC, Hendrix MJ, and Futscher BW. Epigenetic silencing of maspin gene expression in human breast cancers. Int J Cancer 85: 805-810, 2000. (Pubitemid 30131470)
8. Feinberg AP, Ohlsson R, and Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet 7: 21-33, 2006. (Pubitemid 41828945)
9. Fukai T and Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15: 1583-1606, 2011.
10. Futscher BW, O'Meara MM, Kim CJ, Rennels MA, Lu D, Gruman LM, Seftor RE, Hendrix MJ, and Domann FE. Aberrant methylation of the maspin promoter is an early event in human breast cancer. Neoplasia 6: 380-389, 2004. (Pubitemid 38924853)
11. Gantt SL, Gattis SG, and Fierke CA. Catalytic activity and inhibition of human histone deacetylase 8 is dependent on the identity of the active site metal ion. Biochemistry 45: 6170-6178, 2006. (Pubitemid 43727109)
12. Govindarajan B, Klafter R, Miller MS, Mansur C, Mizesko M, Bai X, LaMontagne K, Jr, and Arbiser JL. Reactive oxygeninduced carcinogenesis causes hypermethylation of p16 (Ink4a) and activation of MAP kinase. Mol Med 8: 1-8, 2002. (Pubitemid 34451115)
13. Guo Z, Boekhoudt GH, and Boss JM. Role of the intronic enhancer in tumor necrosis factor-mediated induction of manganous superoxide dismutase. J Biol Chem 278: 23570-23578, 2003. (Pubitemid 36830177)
14. Guzy RD, Sharma B, Bell E, Chandel NS, and Schumacker PT. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxiainducible factor activation and tumorigenesis. Mol Cell Biol 28: 718-731, 2008.
15. Hitchler MJ and Domann FE. An epigenetic perspective on the free radical theory of development. Free Radic Biol Med 43: 1023-1036, 2007. (Pubitemid 47302657)
16. Hitchler MJ and Domann FE. Metabolic defects provide a spark for the epigenetic switch in cancer. Free Radic Biol Med 47: 115-127, 2009.
17. Hitchler MJ, Oberley LW, and Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 45: 1573-1580, 2008.
18. Hitchler MJ, Wikainapakul K, Yu L, Powers K, Attatippaholkun W, and Domann FE. Epigenetic regulation of manganese superoxide dismutase expression in human breast cancer cells. Epigenetics 1: 163-171, 2006.
19. Hodge DR, Xiao W, Peng B, Cherry JC, Munroe DJ, and Farrar WL. 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 65: 6255-6263, 2005. (Pubitemid 40994411)
20. Huang Y, He T, and Domann FE. Decreased expression of manganese superoxide dismutase in transformed cells is associated with increased cytosine methylation of the SOD2 gene. DNA Cell Biol 18: 643-652, 1999. (Pubitemid 29387801)
21. Huang Y, Peng J, Oberley LW, and Domann FE. Transcriptional inhibition of manganese superoxide dismutase (SOD2) gene expression by DNA methylation of the 5' CpG island. Free Radic Biol Med 23: 314-320, 1997. (Pubitemid 27276612)
22. Hurt EM, Thomas SB, Peng B, and Farrar WL. Molecular consequences of SOD2 expression in epigenetically silenced pancreatic carcinoma cell lines. Br J Cancer 97: 1116-1123, 2007. (Pubitemid 47587014)
23. Ikegami T, Suzuki Y, Shimizu T, Isono K, Koseki H, and Shirasawa T. Model mice for tissue-specific deletion of the manganese superoxide dismutase (SOD2) gene. Biochem Biophys Res Commun 296: 729-736, 2002.
24. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, and Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303, 2011.
25. Jones PL, Ping D, and Boss JM. 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 17: 6970-6981, 1997. (Pubitemid 27505927)
26. King A, Selak MA, and Gottlieb E. Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25: 4675-4682, 2006. (Pubitemid 44187617)
27. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, and Burgering BM. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419: 316-321, 2002.
28. Lemarie A and Grimm S. Mitochondrial respiratory chain complexes: apoptosis sensors mutated in cancer? Oncogene 30: 3985-4003, 2011.
29. Lustgarten M, Jang Y, Liu Y, Muller F, Qi W, Steinhelper M, Brooks S, Larkin LM, Shimizu T, Shirasawa T, McManus L, Bhattacharya A, Richardson A, and Van Remmen H. Conditional knockout of SOD2 targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity. Am J Physiol Cell Physiol 297: C1520-32, 2009.
30. Maehara K, Uekawa N, and Isobe K. Effects of histone acetylation on transcriptional regulation of manganese superoxide dismutase gene. Biochem Biophys Res Commun 295: 187-192, 2002. (Pubitemid 34743796)
31. Misawa H, Nakata K, Matsuura J, Moriwaki Y, Kawashima K, Shimizu T, Shirasawa T, and Takahashi R. Conditional knockout of Mn superoxide dismutase in postnatal motor neurons reveals resistance to mitochondrial generated superoxide radicals. Neurobiol Dis 23: 169-177, 2006. (Pubitemid 43903638)
32. Missirlis F, Hu J, Kirby K, Hilliker AJ, Rouault TA, and Phillips JP. Compartment-specific protection of iron-sulfur proteins by superoxide dismutase. J Biol Chem 278: 47365-47369, 2003. (Pubitemid 37523175)
33. Mosammaparast N and Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79: 155-179, 2010.
34. Murrell A. Setting up and maintaining differential insulators and boundaries for genomic imprinting. Biochem Cell Biol 89: 469-478, 2011.
35. Oberley LW, Oberley TD, and Buettner GR. Cell differentiation, aging and cancer: the possible roles of superoxide and superoxide dismutases. Med Hypotheses 6: 249-268, 1980. (Pubitemid 10057422)
36. Parajuli N, Marine A, Simmons S, Saba H, Mitchell T, Shimizu T, Shirasawa T, and Macmillan-Crow LA. Generation and characterization of a novel kidney-specific manganese superoxide dismutase knockout mouse. Free Radic Biol Med 51: 406-416, 2011.
37. Ralph SJ, Rodriguez-Enriquez S, Neuzil J, Saavedra E, and Moreno-Sanchez R. The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation-why mitochondria are targets for cancer therapy. Mol Aspects Med 31: 145-170, 2010.
38. Ranjan P and Boss JM. C/EBPbeta regulates TNF induced SOD2 expression and protection against apoptosis. Apoptosis 11: 1837-1849 2006. (Pubitemid 44371056)
39. Rosenbloom KR, Dreszer TR, Pheasant M, Barber GP, Meyer LR, Pohl A, Raney BJ, Wang T, Hinrichs AS, Zweig AS, Fujita PA, Learned K, Rhead B, Smith KE, Kuhn RM, Karolchik D, Haussler D, and Kent WJ. ENCODE wholegenome data in the UCSC Genome Browser. Nucleic Acids Res 38(Database issue):D620-5, 2010.
40. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, Simon MC, Thompson CB, and Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7: 77-85, 2005. (Pubitemid 40126384)
41. Smith EH, Janknecht R, and Maher LJ, 3rd. Succinate inhibition of alpha-ketoglutarate-dependent enzymes in a yeast model of paraganglioma. Hum Mol Genet 16: 3136-3148, 2007. (Pubitemid 350131331)
42. St Clair DK and Holland JC. Complementary DNA encoding human colon cancer manganese superoxide dismutase and the expression of its gene in human cells. Cancer Res 51: 939-943, 1991.
43. St Clair DK, Porntadavity S, Xu Y, and Kiningham K. Transcription regulation of human manganese superoxide dismutase gene. Methods Enzymol 349: 306-312, 2002. (Pubitemid 34229517)
44. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y,Agarwal S, Iyer LM, LiuDR, Aravind L, and Rao A. Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by theMLL Fusion Partner TET1. Science 324: 930-935, 2009.
45. Uchiyama S, Shimizu T, and Shirasawa T. CuZn-SOD deficiency causes ApoB degradation and induces hepatic lipid accumulation by impaired lipoprotein secretion in mice. J Biol Chem 281: 31713-31719, 2006. (Pubitemid 46041436)
46. Warburg O, Posener K, and Negelein E. On the metabolism of carcinoma cells. Biochemische Zeitschrift 152: 309-344, 1924.
47. Wong GH and Goeddel DV. Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 242: 941-944, 1988. (Pubitemid 19015257)
48. Yang C, Bolotin E, Jiang T, Sladek FM, and Martinez E. Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters. Gene 389: 52-65, 2007. (Pubitemid 46107776)
49. Zhang T, Berrocal JG, Frizzell KM, Gamble MJ, DuMond ME, Krishnakumar R, Yang T, Sauve AA, and Kraus WL. Enzymes in the NAD+ salvage pathway regulate SIRT1 activity at target gene promoters. J Biol Chem 284: 20408-20417, 2009.
50. Zhao Y, Oberley TD, Chaiswing L, Lin SM, Epstein CJ, Huang TT, and St Clair D. Manganese superoxide dismutase deficiency enhances cell turnover via tumor promoter-induced alterations in AP-1 and p53-mediated pathways in a skin cancer model. Oncogene 21: 3836-3846, 2002. (Pubitemid 34620851)