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Research Paper

BNIP3L/NIX and FUNDC1-mediated mitophagy is required for mitochondrial network remodeling during cardiac progenitor cell differentiation

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Pages 1182-1198 | Received 30 Oct 2017, Accepted 25 Jan 2019, Published online: 22 Feb 2019

References

  • Writing Group M, Mozaffarian D, Benjamin EJ, et al. Heart disease and stroke statistics-2016 update: a report from the American heart association. Circulation. 2016 Jan 26;133(4):e38–e60.
  • Broughton KM, Sussman MA. Empowering adult stem cells for myocardial regeneration V2.0: success in small steps. Circ Res. 2016 Mar 04;118(5):867–880.
  • Hatzistergos KE, Takeuchi LM, Saur D, et al. cKit+ cardiac progenitors of neural crest origin. Proc Natl Acad Sci U S A. 2015 Oct 20;112(42):13051–13056.
  • Cho GS, Lee DI, Tampakakis E, et al. Neonatal transplantation confers maturation of PSC-derived cardiomyocytes conducive to modeling cardiomyopathy. Cell Rep. 2017 Jan 10;18(2):571–582.
  • Kulandavelu S, Karantalis V, Fritsch J, et al. Pim1 kinase overexpression enhances ckit+ cardiac stem cell cardiac repair following myocardial infarction in Swine. J Am Coll Cardiol. 2016 Dec 06;68(22):2454–2464.
  • Hodgkinson CP, Bareja A, Gomez JA, et al. Emerging concepts in paracrine mechanisms in regenerative cardiovascular medicine and biology. Circ Res. 2016 Jan 08;118(1):95–107.
  • Li X, Tamama K, Xie X, et al. Improving cell engraftment in cardiac stem cell therapy. Stem Cells Int. 2016;2016:7168797.
  • Terrovitis JV, Smith RR, Marban E. Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res. 2010 Feb 19;106(3):479–494.
  • Guo Y, Wysoczynski M, Nong Y, et al. Repeated doses of cardiac mesenchymal cells are therapeutically superior to a single dose in mice with old myocardial infarction. Basic Res Cardiol. 2017 Mar;112(2):18.
  • Orogo AM, Gonzalez ER, Kubli DA, et al. Accumulation of mitochondrial DNA mutations disrupts cardiac progenitor cell function and reduces survival. J Biol Chem. 2015 Sep 4;290(36):22061–22075.
  • Chung S, Dzeja PP, Faustino RS, et al. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med. 2007 Feb;4(Suppl 1):S60–S67.
  • Rodriguez-Colman MJ, Schewe M, Meerlo M, et al. Interplay between metabolic identities in the intestinal crypt supports stem cell function. Nature. 2017 Mar 16;543(7645):424–427.
  • Chen CT, Shih YR, Kuo TK, et al. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells. 2008 Apr;26(4):960–968.
  • Norddahl GL, Pronk CJ, Wahlestedt M, et al. Accumulating mitochondrial DNA mutations drive premature hematopoietic aging phenotypes distinct from physiological stem cell aging. Cell Stem Cell. 2011 May 6;8(5):499–510.
  • Wahlestedt M, Ameur A, Moraghebi R, et al. Somatic cells with a heavy mitochondrial DNA mutational load render induced pluripotent stem cells with distinct differentiation defects. Stem Cells. 2014 May;32(5):1173–1182.
  • Spitkovsky D, Sasse P, Kolossov E, et al. Activity of complex III of the mitochondrial electron transport chain is essential for early heart muscle cell differentiation. Faseb J. 2004 Aug;18(11):1300–1302.
  • Gatica D, Chiong M, Lavandero S, et al. Molecular mechanisms of autophagy in the cardiovascular system. Circ Res. 2015 Jan 30;116(3):456–467.
  • Kubli DA, Gustafsson AB. Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res. 2012 Oct 12;111(9):1208–1221.
  • Ho TT, Warr MR, Adelman ER, et al. Autophagy maintains the metabolism and function of young and old stem cells. Nature. 2017 Mar 09;543(7644):205–210.
  • Vessoni AT, Muotri AR, Okamoto OK. Autophagy in stem cell maintenance and differentiation. Stem Cells Dev. 2012 Mar 01;21(4):513–520.
  • Zhang Y, Goldman S, Baerga R, et al. Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):19860–19865.
  • Sin J, Andres AM, Taylor DJ, et al. Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts. Autophagy. 2016;12(2):369–380.
  • Gong G, Song M, Csordas G, et al. Parkin-mediated mitophagy directs perinatal cardiac metabolic maturation in mice. Science. 2015 Dec 4;350(6265):aad2459.
  • Ma T, Li J, Xu Y, et al. Atg5-independent autophagy regulates mitochondrial clearance and is essential for iPSC reprogramming. Nat Cell Biol. 2015 Nov;17(11):1379–1387.
  • Liu K, Zhao Q, Liu P, et al. ATG3-dependent autophagy mediates mitochondrial homeostasis in pluripotency acquirement and maintenance. Autophagy. 2016 Nov;12(11):2000–2008.
  • Vazquez-Martin A, Van Den Haute C, Cufi S, et al. Mitophagy-driven mitochondrial rejuvenation regulates stem cell fate. Aging (Albany NY). 2016 Jul;8(7):1330–1352.
  • Mizushima N. Autophagy: process and function. Genes Dev. 2007 Nov 15;21(22):2861–2873.
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19(21):5720–5728. PubMed PMID: 133.
  • Yoshimori T, Yamamoto A, Moriyama Y, et al. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem. 1991 Sep 15;266(26):17707–17712. PubMed PMID: 1832676; eng.
  • Kang R, Zeh HJ, Lotze MT, et al. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011 Apr;18(4):571–580.
  • Bjorkoy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005 Nov 21;171(4):603–614. PubMed PMID: 16286508.
  • Kujoth GC, Hiona A, Pugh TD, et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science. 2005 Jul 15;309(5733):481–484.
  • Rojansky R, Cha MY, Chan DC. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. eLife. 2016 Nov 17;5.
  • Eiyama A, Okamoto K. PINK1/Parkin-mediated mitophagy in mammalian cells. Curr Opin Cell Biol. 2015 Apr;33:95–101.
  • Narendra D, Tanaka A, Suen DF, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008 Dec 1;183(5):795–803.
  • Kubli DA, Zhang X, Lee Y, et al. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem. 2013 Jan 11;288(2):915–926.
  • Monsanto MM, White KS, Kim T, et al. Concurrent isolation of 3 distinct cardiac stem cell populations from a single human heart biopsy. Circ Res. 2017 Jul 7;121(2):113–124.
  • Hentze MW, Castello A, Schwarzl T, et al. A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol. 2018 May;19(5):327–341.
  • Castaldi A, Dodia RM, Orogo AM, et al. Decline in cellular function of aged mouse c-kit+ cardiac progenitor cells. J Physiol. 2017 Oct 01;595(19):6249–6262.
  • Hong KU. c-kit+ cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PloS one. 2014;9(5):e96725.
  • Wanet A, Arnould T, Najimi M, et al. Connecting mitochondria, metabolism, and stem cell fate. Stem Cells Dev. 2015 Sep 01;24(17):1957–1971.
  • Kasahara A, Cipolat S, Chen Y, et al. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling. Science. 2013 Nov 8;342(6159):734–737.
  • Kashatus JA, Nascimento A, Myers LJ, et al. Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol Cell. 2015 Feb 5;57(3):537–551.
  • Din S, Mason M, Volkers M, et al. Pim-1 preserves mitochondrial morphology by inhibiting dynamin-related protein 1 translocation. Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):5969–5974.
  • Fischer KM, Din S, Gude N, et al. Cardiac progenitor cell commitment is inhibited by nuclear Akt expression. Circ Res. 2011 Apr 15;108(8):960–970.
  • Fischer KM, Cottage CT, Wu W, et al. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation. 2009 Nov 24;120(21):2077–2087.
  • Khan M, Mohsin S, Avitabile D, et al. beta-Adrenergic regulation of cardiac progenitor cell death versus survival and proliferation. Circ Res. 2013 Feb 1;112(3):476–486.
  • Durcan TM, Fon EA. The three ‘P’s of mitophagy: PARKIN, PINK1, and post-translational modifications. Genes Dev. 2015 May 15;29(10):989–999.
  • Li W, Zhang X, Zhuang H, et al. MicroRNA-137 is a novel hypoxia-responsive microRNA that inhibits mitophagy via regulation of two mitophagy receptors FUNDC1 and NIX. J Biol Chem. 2014 Apr 11;289(15):10691–10701.
  • Sandoval H, Thiagarajan P, Dasgupta SK, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature. 2008 Jul 10;454(7201):232–235.
  • Schweers RL, Zhang J, Randall MS, et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19500–19505.
  • Esteban-Martinez L, Sierra-Filardi E, McGreal RS, et al. Programmed mitophagy is essential for the glycolytic switch during cell differentiation. Embo J. 2017 Jun 14;36(12):1688–1706.
  • Liu L, Feng D, Chen G, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol. 2012 Feb;14(2):177–185.
  • Long Q, Zhao D, Fan W, et al. Modeling of mitochondrial donut formation. Biophys J. 2015 Sep 1;109(5):892–899.
  • Miyazono Y, Hirashima S, Ishihara N, et al. Uncoupled mitochondria quickly shorten along their long axis to form indented spheroids, instead of rings, in a fission-independent manner. Sci Rep. 2018 Jan 10;8(1):350.
  • Ding WX, Li M, Biazik JM, et al. Electron microscopic analysis of a spherical mitochondrial structure. J Biol Chem. 2012 Dec 7;287(50):42373–42378.
  • Hoque A, Sivakumaran P, Bond ST, et al. Mitochondrial fission protein Drp1 inhibition promotes cardiac mesodermal differentiation of human pluripotent stem cells. Cell Death Discov. 2018;4:39.
  • Jezek J, Cooper KF, Strich R. Reactive oxygen species and mitochondrial dynamics: the yin and yang of mitochondrial dysfunction and cancer progression. Antioxidants. 2018 Jan 16;7(1):13.
  • Ong SB, Subrayan S, Lim SY, et al. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation. 2010 May 11;121(18):2012–2022.
  • Song M, Mihara K, Chen Y, et al. Mitochondrial fission and fusion factors reciprocally orchestrate mitophagic culling in mouse hearts and cultured fibroblasts. Cell Metab. 2015 Feb 3;21(2):273–285.
  • Ikeda Y, Shirakabe A, Maejima Y, et al. Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress. Circ Res. 2015 Jan 16;116(2):264–278.
  • Whelan RS, Konstantinidis K, Wei AC, et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci U S A. 2012 Apr 24;109(17):6566–6571.
  • Papanicolaou KN, Khairallah RJ, Ngoh GA, et al. Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol Cell Biol. 2011 Mar;31(6):1309–1328.
  • Li-Harms X, Milasta S, Lynch J, et al. Mito-protective autophagy is impaired in erythroid cells of aged mtDNA-mutator mice. Blood. 2015 Jan 1;125(1):162–174.
  • Goldberg MS, Fleming SM, Palacino JJ, et al. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem. 2003 Oct 31;278(44):43628–43635.
  • Hanna RA, Quinsay MN, Orogo AM, et al. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem. 2012 Apr 13;287(23):19094–19104.
  • Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–1108. PubMed PMID: 18546601; eng.
  • Macosko EZ, Basu A, Satija R, et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell. 2015 May 21;161(5):1202–1214.
  • Gao E, Koch WJ. A novel and efficient model of coronary artery ligation in the mouse. Methods Mol Biol. 2013;1037:299–311.
  • Castaldi A, Dodia RM, Orogo AM, et al. Decline in cellular function of aged mouse c-kit+ cardiac progenitor cells. J Physiol. 2017 Jul 24;595:6249–6262.
  • Moc C, Taylor AE, Chesini GP, et al. Physiological activation of Akt by PHLPP1 deletion protects against pathological hypertrophy. Cardiovasc Res. 2015 Feb 01;105(2):160–170.
  • Rikka S, Quinsay MN, Thomas RL, et al. Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ. 2011 Nov 19;18(4):721–731.

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