Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension: A basis for excessive cell proliferation and a new therapeutic target

Circulation

Volumn 121, Issue 24, 2010, Pages 2661-2671

  Archer, Stephen L ^a   Marsboom, Glenn ^a   Kim, Gene H ^a   Zhang, Hannah J ^a   Toth, Peter T ^a   Svensson, Eric C ^a   Dyck, Jason R B ^b   Gomberg Maitland, Mardi ^a   Thébaud, Bernard ^c   Husain, Aliya N ^a   Cipriani, Nicole ^a   Rehman, Jalees ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b Departments of Pharmacology and Pediatrics   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

epigenesis; gene silencing; genetic; hypertension; hypoxia inducible factor 1; mitochondrial diseases; oxidation reduction; pulmonary; subunit; superoxide dismutase 2

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CASPASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3B; DNA METHYLTRANSFERASE INHIBITOR; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MANGANESE TETRAKIS(4 BENZOIC ACID) PORPHYRIN; PORPHYRIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; SMOOTH MUSCLE FIBER;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; BIOMIMETICS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; HUMANS; HYDROGEN PEROXIDE; HYPERTENSION, PULMONARY; MITOCHONDRIA, MUSCLE; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; RATS; RATS, MUTANT STRAINS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

EID: 77954083190     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.916098     Document Type: Article

References (37)

1. 2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am J Physiol Heart Circ Physiol. 2008;294:H570-H578.
2. Bonnet S, Michelakis ED, Porter CJ, Andrade-Navarro MA, Thebaud B, Bonnet SN, Haromy A, Harry G, Moudgil R, McMurtry MS, Weir E, Archer SL. An abnormal mitochondrial-HIF-1-Kv channel pathway disrupts oxygen-sensing and triggers pulmonary arterial hypertension (PAH) in fawn-hooded rats: similarities to human PAH. Circulation. 2006;113:2630-2641.
3. Voelkel NF, Cool C, Lee SD, Wright L, Geraci MW, Tuder RM. Primary pulmonary hypertension between inflammation and cancer. Chest. 1998; 114:225S-230S.
4. Bowers R, Cool C, Murphy RC, Tuder RM, Hopken MW, Flores SC, Voelkel NF. Oxidative stress in severe pulmonary hypertension. Am J Respir Crit Care Med. 2004;169:764-769.
5. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006;3: 177-185.
6. Tuder RM, Chacon M, Alger L, Wang J, Taraseviciene-Stewart L, Kasahara Y, Cool CD, Bishop AE, Geraci M, Semenza GL, Yacoub M, Polak JM, Voelkel NF. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol. 2001;195:367-374
7. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Bonnet S, Harry G, Hashimoto K, Porter CJ, Andrade MA, Thebaud B, Michelakis ED. A mitochondria-K + channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell. 2007;11:37-51.
8. Li N, Oberley TD, Oberley LW, Zhong W. Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate. 1998;35:221-233.
9. Bravard A, Sabatier L, Hoffschir F, Ricoul M, Luccioni C, Dutrillaux B. SOD2: a new type of tumor-suppressor gene? Int J Cancer. 1992;51: 476-480.
10. Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypox-ia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem. 1996;271: 32253-32259.
11. Wang GL, Jiang BH, Semenza GL. Effect of altered redox states on expression and DNA-binding activity of hypoxia-inducible factor 1. Biochem Biophys Res Commun. 1995;212:550-556.
12. Weir EK, Lopez-Barneo J, Buckler KJ, Archer SL. Acute oxygen-sensing mechanisms. N Engl J Med. 2005;353:2042-2055.
13. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem. 2004;279:22284-22293.
14. Martin RC, Liu Q, Wo JM, Ray MB, Li Y. Chemoprevention of carcinogenic progression to esophageal adenocarcinoma by the manganese superoxide dismutase supplementation. Clin Cancer Res. 2007;13: 5176-5182. (Pubitemid 47502087)
15. Platoshyn O, Yu Y, Golovina VA, McDaniel SS, Krick S, Li L, Wang JY, Rubin LJ, Yuan JX. Chronic hypoxia decreases K(V) channel expression and function in pulmonary artery myocytes. Am J Physiol Lung Cell Mol Physiol. 2001;280:L801-L812.
16. Hitchler MJ, Oberley LW, Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med. 2008;45:1573-1580.
17. Hurt EM, Thomas SB, Peng B, Farrar WL. Molecular consequences of SOD2 expression in epigenetically silenced pancreatic carcinoma cell lines. Br J Cancer. 2007;97:1116-1123.
18. Ngo VM, Laverriere JN, Gourdji D. CpG methylation represses the activity of the rat prolactin promoter in rat GH3 pituitary cell lines. Mol Cell Endocrinol. 1995;108:95-105.
19. Razin A, Kantor B. DNA methylation in epigenetic control of gene expression. Prog Mol Subcell Biol. 2005;38:151-167.
20. Huang Y, He T, Domann FE. Decreased expression of manganese superoxide dismutase in transformed cells is associated with increased cytosine methylation of the SOD2 gene. DNA Cell Biol. 1999;18: 643-652.
21. Taylor SM, Jones PA. Mechanism of action of eukaryotic DNA methyl-transferase: use of 5-azacytosine-containing DNA. J Mol Biol. 1982;162: 679-692.
22. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005;74:481-514.
23. Beaulieu N, Morin S, Chute IC, Robert MF, Nguyen H, MacLeod AR. An essential role for DNA methyltransferase DNMT3B in cancer cell survival. J Biol Chem. 2002;277:28176-28181.
24. Robertson KD, Uzvolgyi E, Liang G, Talmadge C, Sumegi J, Gonzales FA, Jones PA. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res. 1999;27:2291-2298.
25. Bachman KE, Rountree MR, Baylin SB. Dnmt3a and Dnmt3b are tran-scriptional repressors that exhibit unique localization properties to het-erochromatin. J Biol Chem. 2001;276:32282-32287.
26. Hurt EM, Thomas SB, Peng B, Farrar WL. Integrated molecular profiling of SOD2 expression in multiple myeloma. Blood. 2007;109: 3953-3962.
27. Hodge DR, Xiao W, Peng B, Cherry JC, Munroe DJ, 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. 2005;65:6255-6263.
28. Kim A, Zhong W, Oberley TD. Reversible modulation of cell cycle kinetics in NIH/3T3 mouse fibroblasts by inducible overexpression of mitochondrial manganese superoxide dismutase. Antioxid Redox Signal. 2004;6:489-500.
29. Rodriguez AM, Carrico PM, Mazurkiewicz JE, Melendez JA. Mito-chondrial or cytosolic catalase reverses the MnSOD-dependent inhibition of proliferation by enhancing respiratory chain activity, net ATP production, and decreasing the steady state levels of H(2)O(2). Free Radic Biol Med. 2000;29:801-813.
30. Schroder E, Eaton P. Hydrogen peroxide as an endogenous mediator and exogenous tool in cardiovascular research: issues and considerations. Curr Opin Pharmacol. 2008;8:153-159.
31. Elmedal B, de Dam MY, Mulvany MJ, Simonsen U. The superoxide dismutase mimetic, tempol, blunts right ventricular hypertrophy in chronic hypoxic rats. Br J Pharmacol. 2004;141:105-113.
32. Steinhorn RH, Albert G, Swartz DD, Russell JA, Levine CR, Davis JM. Recombinant human superoxide dismutase enhances the effect of inhaled nitric oxide in persistent pulmonary hypertension. Am J Respir Crit Care Med. 2001;164:834-839.
33. Harju T, Kaarteenaho-Wiik R, Sirvio R, Paakko P, Crapo JD, Oury TD, Soini Y, Kinnula VL. Manganese superoxide dismutase is increased in the airways of smokers' lungs. Eur Respir J. 2004;24:765-771.
34. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, Alderson NL, Baynes JW, Epstein CJ, Huang TT, Nelson J, Strong R, Richardson A. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics. 2003;16:29-37.
35. BelAiba RS, Djordjevic T, Bonello S, Flugel D, Hess J, Kietzmann T, Gorlach A. Redox-sensitive regulation of the HIF pathway under non-hypoxic conditions in pulmonary artery smooth muscle cells. Biol Chem. 2004;385:249-257. (Pubitemid 38679070)
36. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, Chandel NS. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol. 2007;177:1029-1036.
37. Kaewpila S, Venkataraman S, Buettner GR, Oberley LW. Manganese superoxide dismutase modulates hypoxia-inducible factor-1 alpha induction via superoxide. Cancer Res. 2008;68:2781-2788.