Dynamics of mitochondrial DNA nucleoids regulated by mitochondrial fission is essential for maintenance of homogeneously active mitochondria during neonatal heart development

Molecular and Cellular Biology

Volumn 35, Issue 1, 2015, Pages 211-223

  Ishihara, Takaya ^a   Ban Ishihara, Reiko ^a   Maeda, Maki ^a,b   Matsunaga, Yui ^b   Ichimura, Ayaka ^a   Kyogoku, Sachiko ^c   Aoki, Hiroki ^a   Katada, Shun ^d   Nakada, Kazuto ^d   Nomura, Masatoshi ^e   Mizushima, Noboru ^b,f   Mihara, Katsuyoshi ^a,g   Ishihara, Naotada ^a,b  

^a KURUME UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

^g KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MITOCHONDRIAL DNA; DNM1L PROTEIN, MOUSE; DYNAMIN; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; HEART DEVELOPMENT; HEART HYPERTROPHY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOSAICISM; MOUSE; MUSCLE FIBRIL; NONHUMAN; RESPIRATORY FAILURE; ANIMAL; CELL CULTURE; CONGESTIVE CARDIOMYOPATHY; CYTOLOGY; DISEASE MODEL; ELECTRON MICROSCOPY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART MITOCHONDRION; KNOCKOUT MOUSE; METABOLISM; MUSCLE CELL; OXYGEN CONSUMPTION;

MUS;

ANIMALS; CARDIOMYOPATHY, DILATED; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; DYNAMINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MITOCHONDRIA, HEART; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUSCLE CELLS; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES;

EID: 84920060443     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01054-14     Document Type: Article

References (40)

1. Ishihara N, Otera H, Oka T, Mihara K. 2013. Regulation and physiologic functions of GTPases in mitochondrial fusion and fission in mammals. Antioxid Redox Signal 19:389-399. http://dx.doi.org/10.1089/ars.2012.4830.
2. McBride HM, Neuspiel M, Wasiak S. 2006. Mitochondria: more than just a powerhouse. Curr Biol 16:R551-R560. http://dx.doi.org/10.1016/j.cub.2006.06.054.
3. Nunnari J, Suomalainen A. 2012. Mitochondria: in sickness and in health. Cell 148:1145-1159. http://dx.doi.org/10.1016/j.cell.2012.02.035.
4. Chen H, Chomyn A, Chan DC. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280:26185-26192. http://dx.doi.org/10.1074/jbc. M503062200.
5. Chen H, McCaffery JM, Chan DC. 2007. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130:548-562. http://dx.doi.org/10.1016/j.cell.2007.06.026.
6. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141:280-289. http://dx.doi.org/10.1016/j.cell.2010.02.026.
7. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, Otera H, Nakanishi Y, Nonaka I, Goto Y, Taguchi N, Morinaga H, Maeda M, Takayanagi R, Yokota S, Mihara K. 2009. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11:958-966. http://dx.doi.org/10.1038/ncb1907.
8. Kageyama Y, Zhang Z, Roda R, Fukaya M, Wakabayashi J, Wakabayashi N, Kensler TW, Reddy PH, Iijima M, Sesaki H. 2012. Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J Cell Biol 197:535-551. http://dx.doi.org/10.1083/jcb.201110034.
9. Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, Fukaya M, Kensler TW, Iijima M, Sesaki H. 2009. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186:805-816. http://dx.doi.org/10.1083/jcb.200903065.
10. Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, Leonard JV. 2007. A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356:1736-1741. http://dx.doi.org/10.1056/NEJMoa064436.
11. Holt IJ, He J, Mao CC, Boyd-Kirkup JD, Martinsson P, Sembongi H, Reyes A, Spelbrink JN. 2007. Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7:311-321. http://dx.doi.org/10.1016/j.mito.2007.06.004.
12. Kang D, Kim SH, Hamasaki N. 2007. Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Mitochondrion 7:39-44. http://dx.doi.org/10.1016/j.mito.2006.11.017.
13. Ban-Ishihara R, Ishihara T, Sasaki N, Mihara K, Ishihara N. 2013. Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc Natl Acad Sci U S A 110:11863-11868. http://dx.doi.org/10.1073/pnas.1301951110.
14. Dorn GW, II. 2013. Mitochondrial dynamics in heart disease. Biochim Biophys Acta 1833:233-241. http://dx.doi.org/10.1016/j.bbamcr.2012.03.008.
15. Olson EN. 2004. A decade of discoveries in cardiac biology. Nat Med 10:467-474. http://dx.doi.org/10.1038/nm0504-467.
16. Huang X, Sun L, Ji S, Zhao T, Zhang W, Xu J, Zhang J, Wang Y, Wang X, Franzini-Armstrong C, Zheng M, Cheng H. 2013. Kissing and nanotunneling mediate intermitochondrial communication in the heart. Proc Natl Acad Sci U S A 110:2846-2851. http://dx.doi.org/10.1073/pnas.1300741110.
17. Pham AH, McCaffery JM, Chan DC. 2012. Mouse lines with photoactivatable mitochondria to study mitochondrial dynamics. Genesis 50: 833-843. http://dx.doi.org/10.1002/dvg.22050.
18. Piquereau J, Caffin F, Novotova M, Lemaire C, Veksler V, Garnier A, Ventura-Clapier R, Joubert F. 2013. Mitochondrial dynamics in the adult cardiomyocytes: which roles for a highly specialized cell? Front Physiol 4:102. http://dx.doi.org/10.3389/fphys.2013.00102.
19. Chen Y, Liu Y, Dorn GW, II. 2011. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ Res 109:1327-1331. http://dx.doi.org/10.1161/CIRCRESAHA.111.258723.
20. Papanicolaou KN, Kikuchi R, Ngoh GA, Coughlan KA, Dominguez I, Stanley WC, Walsh K. 2012. Mitofusins 1 and 2 are essential for postnatal metabolic remodeling in heart. Circ Res 111:1012-1026. http://dx.doi.org/10.1161/CIRCRESAHA.112.274142.
21. Chen Y, Dorn GW, II. 2013. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340:471-475. http://dx.doi.org/10.1126/science.1231031.
22. Ashrafian H, Docherty L, Leo V, Towlson C, Neilan M, Steeples V, Lygate CA, Hough T, Townsend S, Williams D, Wells S, Norris D, Glyn-Jones S, Land J, Barbaric I, Lalanne Z, Denny P, Szumska D, Bhattacharya S, Griffin JL, Hargreaves I, Fernandez-Fuentes N, Cheeseman M, Watkins H, Dear TN. 2010. A mutation in the mitochondrial fission gene Dnm1l leads to cardiomyopathy. PLoS Genet 6:e1001000. http://dx.doi.org/10.1371/journal.pgen.1001000.
23. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. 2010. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121:2012-2022. http://dx.doi.org/10.1161/CIRCULATIONAHA.109.906610.
24. Sharp WW, Fang YH, Han M, Zhang HJ, Hong Z, Banathy A, Morrow E, Ryan JJ, Archer SL. 2014. Dynamin-related protein 1 (Drp1)-mediated diastolic dysfunction in myocardial ischemia-reperfusion injury: therapeutic benefits of Drp1 inhibition to reduce mitochondrial fission. FASEB J 28:316-326. http://dx.doi.org/10.1096/fj.12-226225.
25. Sreejit P, Kumar S, Verma RS. 2008. An improved protocol for primary culture of cardiomyocyte from neonatal mice. In Vitro Cell Dev Biol Anim 44:45-50. http://dx.doi.org/10.1007/s11626-007-9079-4.
26. Nakada K, Inoue K, Ono T, Isobe K, Ogura A, Goto YI, Nonaka I, Hayashi JI. 2001. Inter-mitochondrial complementation: mitochondria- specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat Med 7:934-940. http://dx.doi.org/10.1038/90976.
27. Oba T, Yasukawa H, Hoshijima M, Sasaki K, Futamata N, Fukui D, Mawatari K, Nagata T, Kyogoku S, Ohshima H, Minami T, Nakamura K, Kang D, Yajima T, Knowlton KU, Imaizumi T. 2012. Cardiac-specific deletion of SOCS-3 prevents development of left ventricular remodeling after acute myocardial infarction. J Am Coll Cardiol 59:838-852. http://dx.doi.org/10.1016/j.jacc.2011.10.887.
28. Shitara H, Hayashi JI, Takahama S, Kaneda H, Yonekawa H. 1998. Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage. Genetics 148:851-857.
29. Smirnova E, Shurland DL, Ryazantsev SN, van der Bliek AM. 1998. A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143:351-358. http://dx.doi.org/10.1083/jcb.143.2.351.
30. Leu M, Ehler E, Perriard JC. 2001. Characterisation of postnatal growth of the murine heart. Anat Embryol 204:217-224. http://dx.doi.org/10.1007/s004290100206.
31. Li F, Wang X, Capasso JM, Gerdes AM. 1996. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 28:1737-1746. http://dx.doi.org/10.1006/jmcc.1996.0163.
32. Piquereau J, Novotova M, Fortin D, Garnier A, Ventura-Clapier R, Veksler V, Joubert F. 2010. Postnatal development of mouse heart: formation of energetic microdomains. J Physiol 588:2443-2454. http://dx.doi.org/10.1113/jphysiol.2010.189670.
33. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR. 1998. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without alter- ing glucose tolerance. Mol Cell 2:559-569. http://dx.doi.org/10.1016/S1097-2765(00)80155-0.
34. Wang J, Wilhelmsson H, GraffC, Li H, Oldfors A, Rustin P, Bruning JC, Kahn CR, Clayton DA, Barsh GS, Thoren P, Larsson NG. 1999. Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet 21:133-137. http://dx.doi.org/10.1038/5089.
35. Sheldon CA, Friedman WF, Sybers HD. 1976. Scanning electron microscopy of fetal and neonatal lamb cardiac cells. J Mol Cell Cardiol 8:853-862. http://dx.doi.org/10.1016/0022-2828(76)90068-7.
36. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ. 2004. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15:5001-5011. http://dx.doi.org/10.1091/mbc. E04-04-0294.
37. Sesaki H, Jensen RE. 1999. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol 147:699-706. http://dx.doi.org/10.1083/jcb.147.4.699.
38. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160:189-200. http://dx.doi.org/10.1083/jcb.200211046.
39. Murley A, Lackner LL, Osman C, West M, Voeltz GK, Walter P, Nunnari J. 2013. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2:e00422. http://dx.doi.org/10.7554/eLife.00422.
40. Ashley N, Poulton J. 2009. Anticancer DNA intercalators cause p53-dependent mitochondrial DNA nucleoid re-modelling. Oncogene 28: 3880-3891. http://dx.doi.org/10.1038/onc.2009.242.