Parkin-mediated mitophagy directs perinatal cardiac metabolic maturation in mice

Science

Volumn 350, Issue 6265, 2015, Pages

  Gong, Guohua ^a   Song, Moshi ^a   Csordas, Gyorgy ^b   Kelly, Daniel P ^c   Matkovich, Scot J ^a   Dorn, Gerald W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLCARNITINE; MITOFUSIN 2; PALMITOYLCARNITINE; PARKIN; PHOSPHOTRANSFERASE; PTEN INDUCED PUTATIVE KINASE 1; UNCLASSIFIED DRUG; GUANOSINE TRIPHOSPHATASE; MFN2 PROTEIN, MOUSE; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN PROTEIN LIGASE;

CARDIOVASCULAR SYSTEM; FATTY ACID; GENE EXPRESSION; METABOLISM; MITOCHONDRION; PROTEIN; RESPIRATION; RODENT; SURVIVAL;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIRTH; CARDIOMYOPATHY; CELL MATURATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FETUS; GENE DELETION; GENE TRANSLOCATION; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART MUSCLE METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MITOPHAGY; MOUSE; NONHUMAN; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SURVIVAL; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; EMBRYOLOGY; GENETICS; HEART; HEART MITOCHONDRION; KNOCKOUT MOUSE; METABOLISM; NUCLEAR REPROGRAMMING; PHYSIOLOGY; ULTRASTRUCTURE;

MUS;

ANIMALS; CELLULAR REPROGRAMMING; GTP PHOSPHOHYDROLASES; HEART; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN KINASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84948991793     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aad2459     Document Type: Article

References (37)

1. G. A. Porter Jr. et al., Bioenergetics, mitochondria, and cardiac myocyte differentiation. Prog. Pediatr. Cardiol. 31, 75-81 (2011). doi: 10.1016/j.ppedcard.2011.02.002; pmid: 21603067
2. B. Bartelds et al., Perinatal changes in myocardial metabolism in lambs. Circulation 102, 926-931 (2000). doi: 10.1161/01. CIR.102.8.926; pmid: 10952964
3. H. D. Kim et al., Human fetal heart development after mid-term: Morphometry and ultrastructural study. J. Mol. Cell. Cardiol. 24, 949-965 (1992). doi: 10.1016/0022-2828(92)91862-Y; pmid: 1433323
4. W. C. Stanley, F. A. Recchia, G. D. Lopaschuk, Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev. 85, 1093-1129 (2005). doi: 10.1152/physrev.00006.2004; pmid: 15987803
5. H. Taegtmeyer, S. Sen, D. Vela, Return to the fetal gene program: A suggested metabolic link to gene expression in the heart. Ann. N.Y. Acad. Sci. 1188, 191-198 (2010). doi: 10.1111/j.1749-6632.2009.05100.x; pmid: 20201903
6. M. Song, G. W. Dorn 2nd, Mitoconfusion: Noncanonical functioning of dynamism factors in static mitochondria of the heart. Cell Metab. 21, 195-205 (2015). doi: 10.1016/j.cmet.2014.12.019; pmid: 25651174
7. O. S. Shirihai, M. Song, G. W. Dorn 2nd, How mitochondrial dynamism orchestrates mitophagy. Circ. Res. 116, 1835-1849 (2015). doi: 10.1161/CIRCRESAHA.116.306374; pmid: 25999423
8. R. J. Youle, A. M. van der Bliek, Mitochondrial fission, fusion, and stress. Science 337, 1062-1065 (2012). doi: 10.1126/science.1219855; pmid: 22936770
9. D. A. Kubli et al., Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J. Biol. Chem. 288, 915-926 (2013). doi: 10.1074/jbc.M112.411363; pmid: 23152496
10. Y. Lee, V. L. Dawson, T. M. Dawson, Animal models of Parkinson's disease: Vertebrate genetics. Cold Spring Harb. Perspect. Med. 2, a009324 (2012). doi: 10.1101/cshperspect.a009324; pmid: 22960626
11. J. H. Shin et al., PARIS (ZNF746) repression of PGC-1a contributes to neurodegeneration in Parkinson's disease. Cell 144, 689-702 (2011). doi: 10.1016/j.cell.2011.02.010; pmid: 21376232
12. Y. Chen, G. W. Dorn 2nd, PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340, 471-475 (2013). doi: 10.1126/science.1231031; pmid: 23620051
13. S. Lee et al., Mitofusin 2 is necessary for striatal axonal projections of midbrain dopamine neurons. Hum. Mol. Genet. 21, 4827-4835 (2012). doi: 10.1093/hmg/dds352; pmid: 22914740
14. D. P. Narendra et al., PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLOS Biol. 8, e1000298 (2010). doi: 10.1371/journal.pbio.1000298; pmid: 20126261
15. L. A. Scarffe, D. A. Stevens, V. L. Dawson, T. M. Dawson, Parkin and PINK1: Much more than mitophagy. Trends Neurosci. 37, 315-324 (2014). doi: 10.1016/j.tins.2014.03.004; pmid: 24735649
16. T. Koshiba et al., Structural basis of mitochondrial tethering by mitofusin complexes. Science 305, 858-862 (2004). doi: 10.1126/science.1099793; pmid: 15297672
17. G. Twig et al., Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446 (2008). doi: 10.1038/sj.emboj.7601963; pmid: 18200046
18. W. H. Eschenbacher et al., Two rare human mitofusin 2 mutations alter mitochondrial dynamics and induce retinal and cardiac pathology in Drosophila. PLOS ONE 7, e44296 (2012). doi: 10.1371/journal.pone.0044296; pmid: 22957060
19. A. Misko, S. Jiang, I. Wegorzewska, J. Milbrandt, R. H. Baloh, Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 30, 4232-4240 (2010). doi: 10.1523/JNEUROSCI.6248-09.2010; pmid: 20335458
20. F. Syed et al., Physiological growth synergizes with pathological genes in experimental cardiomyopathy. Circ. Res. 95, 1200-1206 (2004). doi: 10.1161/01.RES.0000150366.08972.7f; pmid: 15539635
21. M. Song et al., Interdependence of Parkin-mediated mitophagy and mitochondrial fission in adult mouse hearts. Circ. Res. 117, 346-351 (2015). doi: 10.1161/CIRCRESAHA.117.306859; pmid: 26038571
22. Y. Chen et al., Mitofusin 2-containing mitochondrial-reticular microdomains direct rapid cardiomyocyte bioenergetic responses via interorganelle Ca(2+) crosstalk. Circ. Res. 111, 863-875 (2012). doi: 10.1161/CIRCRESAHA.112.266585; pmid: 22777004
23. O. M. de Brito, L. Scorrano, Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610 (2008). doi: 10.1038/nature07534; pmid: 19052620
24. G. D. Lopaschuk, M. A. Spafford, D. R. Marsh, Glycolysis is predominant source of myocardial ATP production immediately after birth. Am. J. Physiol. 261, H1698-H1705 (1991). pmid: 1750528
25. P. Razeghi et al., Metabolic gene expression in fetal and failing human heart. Circulation 104, 2923-2931 (2001). doi: 10.1161/hc4901.100526; pmid: 11739307
26. J. J. Lehman et al., Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106, 847-856 (2000). doi: 10.1172/JCI10268; pmid: 11018072
27. N. V. Dudkina, R. Kouril, K. Peters, H. P. Braun, E. J. Boekema, Structure and function of mitochondrial supercomplexes. Biochim. Biophys. Acta 1797, 664-670 (2010). doi: 10.1016/j.bbabio.2009.12.013; pmid: 20036212
28. E. Lapuente-Brun et al., Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567-1570 (2013). doi: 10.1126/science.1230381; pmid: 23812712
29. Y. Chen, Y. Liu, G. W. Dorn 2nd, Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 109, 1327-1331 (2011). doi: 10.1161/CIRCRESAHA.111.258723; pmid: 22052916
30. H. R. Christofk et al., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233 (2008). doi: 10.1038/nature06734; pmid: 18337823
31. M. G. Vander Heiden, L. C. Cantley, C. B. Thompson, Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 324, 1029-1033 (2009). doi: 10.1126/science.1160809; pmid: 19460998
32. P. Bhandari, M. Song, Y. Chen, Y. Burelle, G. W. Dorn 2nd, Mitochondrial contagion induced by Parkin deficiency in Drosophila hearts and its containment by suppressing mitofusin. Circ. Res. 114, 257-265 (2014). doi: 10.1161/CIRCRESAHA.114.302734; pmid: 24192653
33. J. A. Williams et al., Chronic deletion and acute knockdown of Parkin have differential responses to acetaminophen-induced mitophagy and liver injury in mice. J. Biol. Chem. 290, 10934-10946 (2015). doi: 10.1074/jbc.M114.602284; pmid: 25752611
34. Y. Kageyama et al., Parkin-independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain. EMBO J. 33, 2798-2813 (2014). doi: 10.15252/embj.201488658; pmid: 25349190
35. M. Song et al., Super-suppression of mitochondrial reactive oxygen species signaling impairs compensatory autophagy in primary mitophagic cardiomyopathy. Circ. Res. 115, 348-353 (2014). doi: 10.1161/CIRCRESAHA.115.304384; pmid: 24874428
36. A. M. Pickrell, R. J. Youle, The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85, 257-273 (2015). doi: 10.1016/j.neuron.2014.12.007; pmid: 25611507
37. G. W. Dorn 2nd, Mitochondrial dynamism and heart disease: Changing shape and shaping change. EMBO Mol. Med. 7, 865-877 (2015). doi: 10.15252/emmm.201404575; pmid: 25861797