Overexpression of TFAM or twinkle increases mtDNA copy number and facilitates cardioprotection associated with limited mitochondrial oxidative stress

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Ikeda, Masataka ^a   Ide, Tomomi ^a   Fujino, Takeo ^a   Arai, Shinobu ^a   Saku, Keita ^a   Kakino, Takamori ^a   Tyynismaa, Henna ^b   Yamasaki, Toshihide ^c   Yamada, Ken Ichi ^c   Kang, Dongchon ^a   Suomalainen, Anu ^b   Sunagawa, Kenji ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF HELSINKI   (Finland)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; HELICASE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; REACTIVE OXYGEN METABOLITE; TWINKLE HELICASE; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNA HELICASE; MATRIX METALLOPROTEINASE; PEO1 PROTEIN, MOUSE; TFAM PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DOSAGE; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE CELL; HEART PROTECTION; HEART VENTRICLE OVERLOAD; MALE; MOUSE; NEWBORN; NONHUMAN; OXIDATION; OXIDATIVE STRESS; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL LINE; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; RAT;

ANIMALIA; MUS; MUS MUSCULUS; RATTUS;

ANIMALS; CELL LINE; DNA HELICASES; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; GENE DOSAGE; HEART FAILURE; HUMANS; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84926382602     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119687     Document Type: Article

References (39)

1. McMurray JJ, Pfeffer MA (2005) Heart failure. Lancet 365: 1877-1889. PMID: 15924986
2. Sano M, Minamino T, Toko H, Miyauchi H, Orimo M, et al. (2007) p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload. Nature 446: 444-448. PMID: 17334357
3. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, et al. (1999) Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 85: 357-363. PMID: 10455064
4. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, et al. (2001) Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88: 529-535. PMID: 11249877
5. Ago T, Kuroda J, Pain J, Fu C, Li H, et al. (2010) Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 106: 1253-1264. doi: 10.1161/CIRCRESAHA.109.213116 PMID: 20185797
6. Suematsu N, Tsutsui H, Wen J, Kang D, Ikeuchi M, et al. (2003) Oxidative stress mediates tumor necrosis factor-alpha-induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 107: 1418-1423. PMID: 12642364
7. Shiomi T, Tsutsui H, Matsusaka H, Murakami K, Hayashidani S, et al. (2004) Overexpression of glutathione peroxidase prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 109: 544-549. PMID: 14744974
8. Kanki T, Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, et al. (2004) Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 24: 9823-9834. PMID: 15509786
9. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, et al. (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13: 935-944. PMID: 15016765
10. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, et al. (1999) Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet 21: 133-137. PMID: 9916807
11. Li H, Wang J, Wilhelmsson H, Hansson A, Thoren P, et al. (2000) Genetic modification of survival in tissue-specific knockout mice with mitochondrial cardiomyopathy. Proc Natl Acad Sci U S A 97: 3467-3472. PMID: 10737799
12. Ikeuchi M, Matsusaka H, Kang D, Matsushima S, Ide T, et al. (2005) Overexpression of mitochondrial transcription factor A ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 112: 683-690. PMID: 16043643
13. Spelbrink JN, Li FY, Tiranti V, Nikali K, Yuan QP, et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat Genet 28: 223-231. PMID: 11431692
14. Ylikallio E, Tyynismaa H, Tsutsui H, Ide T, Suomalainen A (2010) High mitochondrial DNA copy number has detrimental effects in mice. Hum Mol Genet 19: 2695-2705. doi: 10.1093/hmg/ddq163 PMID: 20413656
15. Fujino T, Ide T, Yoshida M, Onitsuka K, Tanaka A, et al. (2012) Recombinant mitochondrial transcription factor A protein inhibits nuclear factor of activated T cells signaling and attenuates pathological hypertrophy of cardiac myocytes. Mitochondrion 12: 449-458. doi: 10.1016/j.mito.2012.06.002 PMID: 22709542
16. Tyynismaa H, Sembongi H, Bokori-Brown M, Granycome C, Ashley N, et al. (2004) Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum Mol Genet 13: 3219-3227. PMID: 15509589
17. Garcia R, Diebold S (1990) Simple, rapid, and effective method of producing aortocaval shunts in the rat. Cardiovasc Res 24: 430-432. PMID: 2142618
18. He BJ, Joiner ML, Singh MV, Luczak ED, Swaminathan PD, et al. (2011) Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat Med 17: 1610-1618. doi: 10.1038/nm.2506 PMID: 22081025
19. Mukhopadhyay P, Rajesh M, Yoshihiro K, Hasko G, Pacher P (2007) Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem and Biophys Res Commun 358: 203-208. PMID: 17475217
20. Mito F, Kitagawa K, Yamasaki T, Shirahama C, Oishi T, et al. (2011) Oxygen concentration dependence of lipid peroxidation and lipid-derived radical generation: application of profluorescent nitroxide switch. Free Radic Res 45: 1103-1110. doi: 10.3109/10715762.2011.595410 PMID: 21736483
21. Matsuoka Y, Yamato M, Yamasaki T, Mito F, Yamada K (2012) Rapid and convenient detection of ascorbic acid using a fluorescent nitroxide switch. Free Radic Bio Med 53: 2112-2118. doi: 10.1016/j.freeradbiomed.2012.09.032 PMID: 23026412
22. Kang D, Kim SH, Hamasaki N (2007) Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Mitochondrion 7: 39-44. PMID: 17280879
23. Ohgaki K, Kanki T, Fukuoh A, Kurisaki H, Aoki Y, et al. (2007) The C-terminal tail of mitochondrial transcription factor A markedly strengthens its general binding to DNA. J Biochem 141: 201-211. PMID: 17167045
24. Tanaka A, Ide T, Fujino T, Onitsuka K, Ikeda M, et al. (2013) The overexpression of Twinkle helicase ameliorates the progression of cardiac fibrosis and heart failure in pressure overload model in mice. PLoS One 8: e67642. doi: 10.1371/journal.pone.0067642 PMID: 23840758
25. Mishra PK, Tyagi N, Sen U, Givvimani S, Tyagi SC (2010) H2S ameliorates oxidative and proteolytic stresses and protects the heart against adverse remodeling in chronic heart failure. Am J Physiol Heart Circ Physiol 298: H451-456. doi: 10.1152/ajpheart.00682.2009 PMID: 19933416
26. Spinale FG (2007) Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 87: 1285-1342. PMID: 17928585
27. Hutchinson KR, Stewart JA Jr., Lucchesi PA (2010) Extracellular matrix remodeling during the progression of volume overload-induced heart failure. J Mol Cell Cardiol 48: 564-569. doi: 10.1016/j.yjmcc.2009.06.001 PMID: 19524591
28. Spinale FG, Janicki JS, Zile MR (2013) Membrane-associated matrix proteolysis and heart failure. Circ Res 112: 195-208. doi: 10.1161/CIRCRESAHA.112.266882 PMID: 23287455
29. Moshal KS, Tyagi N, Henderson B, Ovechkin AV, Tyagi SC (2005) Protease-activated receptor and endothelial-myocyte uncoupling in chronic heart failure. Am J Physiol Heart Circ Physiol 288: H2770-2777. PMID: 15681708
30. Ovechkin AV, Tyagi N, Rodriguez WE, Hayden MR, Moshal KS, et al. (2005) Role of matrix metallopro-teinase-9 in endothelial apoptosis in chronic heart failure in mice. J Appl Physiol 99: 2398-2405. PMID: 16081621
31. Hayashi Y, Yoshida M, Yamato M, Ide T, Wu Z, et al. (2008) Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor A in mice. J Neurosci 28: 8624-8634. doi: 10.1523/JNEUROSCI.1957-08.2008 PMID: 18716221
32. Li H, Liu D, Lu J, Bai Y (2012) Physiology and pathophysiology of mitochondrial DNA. Adv Exp Med Biol 942: 39-51. doi: 10.1007/978-94-007-2869-1-2 PMID: 22399417
33. Karamanlidis G, Nascimben L, Couper GS, Shekar PS, del Monte F, et al. (2010) Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ Res 106: 1541-1548. doi: 10.1161/CIRCRESAHA.109.212753 PMID: 20339121
34. Ahuja P, Wanagat J, Wang Z, Wang Y, Liem DA, et al. (2013) Divergent mitochondrial biogenesis responses in human cardiomyopathy. Circulation 127: 1957- 1967. doi: 10.1161/CIRCULATIONAHA.112.001219 PMID: 23589024
35. Tsutsui H, Kinugawa S, Matsushima S (2011) Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 301: H2181-2190. doi: 10.1152/ajpheart.00554.2011 PMID: 21949114
36. Nickel A, Kohlhaas M, Maack C (2014) Mitochondrial reactive oxygen species production and elimination. J Mol Cell Cardiol 74:26-33.
37. Pohjoismaki JL, Williams SL, Boettger T, Goffart S, Kim J, et al. (2013) Overexpression of Twinkle helicase protects cardiomyocytes from genotoxic stress caused by reactive oxygen species. Proc Natl Acad Sci U S A 110: 19408-19413. doi: 10.1073/pnas.1303046110 PMID: 24218554
38. Stuart JA, Bourque BM, de Souza-Pinto NC, Bohr VA (2005) No evidence of mitochondrial respiratory dysfunction in OGG1-null mice deficient in removal of 8-oxodeoxyguanine from mitochondrial DNA. Free Radic Biol Med 38: 737-745. PMID: 15721984
39. Gladden JD, Zelickson BR, Wei CC, Ulasova E, Zheng J, et al. (2011) Novel insights into interactions between mitochondria and xanthine oxidase in acute cardiac volume overload. Free Radic Biol Med 51: 1975-1984. doi: 10.1016/j.freeradbiomed.2011.08.022 PMID: 21925594