Interaction of Sirt3 with OGG1 contributes to repair of mitochondrial DNA and protects from apoptotic cell death under oxidative stress

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Cheng, Y ^a   Ren, X ^a   Gowda, A S P ^a   Shan, Y ^a   Zhang, L ^a   Yuan, Y S ^a   Patel, R ^a   Wu, H ^a   Huber Keener, K ^a   Yang, J W ^a   Liu, D ^a   Spratt, T E ^a   Yang, J M ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; DNA repair; Mitochondria; OGG1; Sirt3

Indexed keywords

8 OXOGUANINE DNA GLYCOSYLASE 1; DNA GLYCOSYLTRANSFERASE; MITOCHONDRIAL DNA; SIRTUIN 3; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DEACETYLATION; DNA DAMAGE; DNA REPAIR; ENZYME DEGRADATION; ENZYME METABOLISM; GENE EXPRESSION; GENE SILENCING; GENOTOXICITY; HUMAN; HUMAN CELL; IONIZING RADIATION; MITOCHONDRIAL GENOME; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

EID: 84881076472     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.254     Document Type: Article

References (47)

1. Finkel T, Deng CX, Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009; 460: 587-591.
2. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R et al. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 2007; 27: 8807-8814.
3. Lu Z, Bourdi M, Li JH, Aponte AM, Chen Y, Lombard DB et al. SIRT3-dependent deacetylation exacerbates acetaminophen hepatotoxicity. EMBO Rep 2011; 12: 840-846.
4. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C et al. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 2010; 143: 802-812.
5. Schlicker C, Gertz M, Papatheodorou P, Kachholz B, Becker CF, Steegborn C. Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J Mol Biol 2008; 382: 790-801.
6. Cimen H, Han MJ, Yang Y, Tong Q, Koc H, Koc EC. Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 2010; 49: 304-311.
7. Hallows WC, Lee S, Denu JM. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 2006; 103: 10230-10235.
8. Haigis MC, Deng CX, Finley LW, Kim HS, Gius D. SIRT3 is a mitochondrial tumor suppressor: a scientific tale that connects aberrant cellular ROS, the Warburg effect, and carcinogenesis. Cancer Res 2012; 72: 2468-2472.
9. Onyango P, Celic I, McCaffery JM, Boeke JD, Feinberg AP. SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria. Proc Natl Acad Sci USA 2002; 99: 13653-13658.
10. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 2010; 12: 662-667.
11. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 2010; 40: 893-904.
12. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S et al. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 2011; 12: 534-541.
13. Yu W, Dittenhafer-Reed KE, Denu JM. SIRT3 protein deacetylates isocitrate dehydrogenase 2 (IDH2) and regulates mitochondrial redox status. J Biol Chem 2012; 287: 14078-14086.
14. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A et al. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci USA 2008; 105: 14447-14452.
15. Shulga N, Wilson-Smith R, Pastorino JG. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J Cell Sci 2010; 123(Pt 6): 894-902.
16. Schon EA. Mitochondrial genetics and disease. Trends Biochem Sci 2000; 25: 555-560.
17. Richter C, Park JW, Ames BN. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci USA 1988; 85: 6465-6467.
18. Grollman AP, Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet 1993; 9: 246-249.
19. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J Biol Chem 1992; 267: 166-172.
20. Roldan-Arjona T, Wei YF, Carter KC, Klungland A, Anselmino C, Wang RP et al. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc Natl Acad Sci USA 1997; 94: 8016-8020.
21. Bhakat KK, Mokkapati SK, Boldogh I, Hazra TK, Mitra S. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol Cell Biol 2006; 26: 1654-1665.
22. Bohr VA, Stevnsner T, de Souza-Pinto NC. Mitochondrial DNA repair of oxidative damage in mammalian cells. Gene 2002; 286: 127-134.
23. Parlanti E, Fortini P, Macpherson P, Laval J, Dogliotti E. Base excision repair of adenine/8-oxoguanine mispairs by an aphidicolin-sensitive DNA polymerase in human cell extracts. Oncogene 2002; 21: 5204-5212.
24. Takao M, Aburatani H, Kobayashi K, Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res 1998; 26: 2917-2922.
25. de Souza-Pinto NC, Eide L, Hogue BA, Thybo T, Stevnsner T, Seeberg E et al. Repair of 8-oxodeoxyguanosine lesions in mitochondrial DNA depends on the oxoguanine DNA glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-defective mice. Cancer Res 2001; 61: 5378-5381.
26. Minowa O, Arai T, Hirano M, Monden Y, Nakai S, Fukuda M et al. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc Natl Acad Sci USA 2000; 97: 4156-4161.
27. Hill JW, Hu JJ, Evans MK. OGG1 is degraded by calpain following oxidative stress and cisplatin exposure. DNA Repair (Amst) 2008; 7: 648-654.
28. Lee HC, Wei YH. Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging. Exp Biol Med (Maywood) 2007; 232: 592-606.
29. Oka S, Ohno M, Tsuchimoto D, Sakumi K, Furuichi M, Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J 2008; 27: 421-432.
30. Jensen A, Calvayrac G, Karahalil B, Bohr VA, Stevnsner T. Mammalian 8-oxoguanine DNA glycosylase 1 incises 8-oxoadenine opposite cytosine in nuclei and mitochondria, while a different glycosylase incises 8-oxoadenine opposite guanine in nuclei. J Biol Chem 2003; 278: 19541-19548.
31. Dobson AW, Xu Y, Kelley MR, LeDoux SP, Wilson GL. Enhanced mitochondrial DNA repair and cellular survival after oxidative stress by targeting the human 8-oxoguanine glycosylase repair enzyme to mitochondria. J Biol Chem 2000; 275: 37518-37523.
32. Sundaresan NR, Samant SA, Pillai VB, Rajamohan SB, Gupta MP. SIRT3 is a stressresponsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol Cell Biol 2008; 28: 6384-6401.
33. Chen CJ, Fu YC, Yu W, Wang W. SIRT3 protects cardiomyocytes from oxidative stressmediated cell death by activating NF-kappaB. Biochem Biophys Res Commun 2013; 430: 798-803.
34. Pellegrini L, Pucci B, Villanova L, Marino ML, Marfe G, Sansone L et al. SIRT3 protects from hypoxia and staurosporine-mediated cell death by maintaining mitochondrial membrane potential and intracellular pH. Cell Death Differ 2012; 19: 1815-1825.
35. Shulga N, Pastorino JG. Ethanol sensitizes mitochondria to the permeability transition by inhibiting deacetylation of cyclophilin-D mediated by sirtuin-3. J Cell Sci 2010; 123(Pt 23): 4117-4127.
36. Rachek LI, Thornley NP, Grishko VI, LeDoux SP, Wilson GL. Protection of INS-1 cells from free fatty acid-induced apoptosis by targeting hOGG1 to mitochondria. Diabetes 2006; 55: 1022-1028.
37. Chatterjee A, Chang X, Nagpal JK, Chang S, Upadhyay S, Califano J et al. Targeting human 8-oxoguanine DNA glycosylase to mitochondria protects cells from 2-methoxyestradiol-induced-mitochondria-dependent apoptosis. Oncogene 2008; 27: 3710-3720.
38. Ricci C, Pastukh V, Leonard J, Turrens J, Wilson G, Schaffer D et al. Mitochondrial DNA damage triggers mitochondrial-superoxide generation and apoptosis. Am J Physiol Cell Physiol 2008; 294: C413-C422.
39. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J et al. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 2011; 19: 416-428.
40. Bell EL, Emerling BM, Ricoult SJ, Guarente L. SirT3 suppresses hypoxia inducible factor 1alpha and tumor growth by inhibiting mitochondrial ROS production. Oncogene 2011; 30: 2986-2996.
41. Alhazzazi TY, Kamarajan P, Verdin E, Kapila YL. SIRT3 and cancer: tumor promoter or suppressor? Biochim Biophys Acta 2011; 1816: 80-88.
42. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 2010; 17: 41-52.
43. Alhazzazi TY, Kamarajan P, Joo N, Huang JY, Verdin E, D'Silva NJ et al. Sirtuin-3 (SIRT3), a novel potential therapeutic target for oral cancer. Cancer 2011; 117: 1670-1678.
44. Ashraf N, Zino S, Macintyre A, Kingsmore D, Payne AP, George WD et al. Altered sirtuin expression is associated with node-positive breast cancer. Br J Cancer 2006; 95: 1056-1061.
45. Ohno M, Oka S, Nakabeppu Y. Quantitative analysis of oxidized guanine, 8-oxoguanine, in mitochondrial DNA by immunofluorescence method. Methods Mol Biol 2009; 554: 199-212.
46. Chen T, He J, Shen L, Fang H, Nie H, Jin T et al. The mitochondrial DNA 4,977-bp deletion and its implication in copy number alteration in colorectal cancer. BMC Med Genet 2011; 12: 8.
47. Prithivirajsingh S, Story MD, Bergh SA, Geara FB, Ang KK, Ismail SM et al. Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett 2004; 571: 227-232.