Mitochondrial contagion induced by parkin deficiency in drosophila hearts and its containment by suppressing mitofusin

Circulation Research

Volumn 114, Issue 2, 2014, Pages 257-265

  Bhandari, Poonam ^a   Song, Moshi ^a   Chen, Yun ^a   Burelle, Yan ^b   Dorn, Gerald W ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cardiomyopathies; Mitochondrial degradation; Mitochondrial dynamics

Indexed keywords

CALCIUM; MITOFUSIN 1; MITOFUSIN 2; PARKIN; REACTIVE OXYGEN METABOLITE; UBIQUITIN PROTEIN LIGASE E3; DROSOPHILA PROTEIN; MEMBRANE PROTEIN; MFN2 PROTEIN, DROSOPHILA; PARKIN PROTEIN, DROSOPHILA; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM METABOLISM; CELL DISRUPTION; CELL FUSION; CELL INTERACTION; CELL ORGANELLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DROSOPHILA; ENZYME DEFICIENCY; ENZYME REGULATION; ENZYME REPRESSION; GENE INACTIVATION; GENE LOSS; GENETIC TRANSCRIPTION; GERMLINE MUTATION; HEART DEPOLARIZATION; HEART FAILURE; HEART MITOCHONDRION; HEART MUSCLE CELL; KNOCKOUT MOUSE; MITOCHONDRIAL DYNAMICS; MITOPHAGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TERATOLOGY; UPREGULATION; ANIMAL; CALCIUM SIGNALING; CARDIOMYOPATHY; DROSOPHILA MELANOGASTER; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; GENOTYPE; METABOLISM; MUTATION; PATHOLOGY; PHENOTYPE; TIME;

CARDIOMYOPATHIES; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS;

ANIMALS; CALCIUM SIGNALING; CARDIOMYOPATHY, DILATED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENOTYPE; HEART FAILURE; MEMBRANE PROTEINS; MITOCHONDRIA, HEART; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MUTATION; MYOCYTES, CARDIAC; PHENOTYPE; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84897113087     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.302734     Document Type: Article

References (37)

1. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998;392:605-608.
2. Valente EM, Abou-Sleiman PM, Caputo V, et al. Hereditary earlyonset Parkinson's disease caused by mutations in PINK1. Science. 2004;304:1158-1160.
3. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, Martella G, Bonsi P, Zhang C, Pothos EN, Shen J. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A. 2007;104:11441-11446.
4. Billia F, Hauck L, Konecny F, Rao V, Shen J, Mak TW. PTEN-inducible kinase 1 (PINK1)/Park6 is indispensable for normal heart function. Proc Natl Acad Sci U S A. 2011;108:9572-9577.
5. Chen Y, Dorn GW II. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science. 2013;340:471-475.
6. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM, Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 2006;441:1157-1161.
7. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, Yoo SJ, Hay BA, Guo M. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 2006;441:1162-1166.
8. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8:1000298.
9. Sarraf SA, Raman M, Guarani-Pereira V, Sowa ME, Huttlin EL, Gygi SP, Harper JW. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature. 2013;496:372-376.
10. Twig G, Elorza A, Molina AJ, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27:433-446.
11. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A. 2003;100:4078-4083.
12. Deng H, Dodson MW, Huang H, Guo M. The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc Natl Acad Sci U S A. 2008;105:14503-14508.
13. Whitworth AJ, Theodore DA, Greene JC, Benes H, Wes PD, Pallanck LJ. Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson's disease. Proc Natl Acad Sci U S A. 2005;102:8024-8029.
14. Ziviani E, Tao RN, Whitworth AJ. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci U S A. 2010;107:5018-5023.
15. Perez FA, Palmiter RD. Parkin-deficient mice are not a robust model of parkinsonism. Proc Natl Acad Sci U S A. 2005;102:2174-2179.
16. Kubli DA, Zhang X, Lee Y, Hanna RA, Quinsay MN, Nguyen CK, Jimenez R, Petrosyan S, Murphy AN, Gustafsson AB. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem. 2013;288:915-926.
17. McFaline-Figueroa JR, Vevea J, Swayne TC, Zhou C, Liu C, Leung G, Boldogh IR, Pon LA. Mitochondrial quality control during inheritance is associated with lifespan and mother-daughter age asymmetry in budding yeast. Aging Cell. 2011;10:885-895.
18. Gautier CA, Kitada T, Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci U S A. 2008;105:11364-11369.
19. Fernandez HH, Lapane KL. Predictors of mortality among nursing home residents with a diagnosis of Parkinson's disease. Med Sci Monit. 2002;8:241-246.
20. Zesiewicz TA, Strom JA, Borenstein AR, Hauser RA, Cimino CR, Fontanet HL, Cintron GB, Staffetti JF, Dunne PB, Sullivan KL. Heart failure in Parkinson's disease: Analysis of the United States medicare current beneficiary survey. Parkinsonism Relat Disord. 2004;10:417-420.
21. Guo M. Drosophila as a model to study mitochondrial dysfunction in Parkinson's disease. Cold Spring Harb Perspect Med. 2012;2:009944.
22. Von Coelln R, Thomas B, Savitt JM, Lim KL, Sasaki M, Hess EJ, Dawson VL, Dawson TM. Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc Natl Acad Sci U S A. 2004;101:10744-10749.
23. Matkovich SJ, Zhang Y, Van Booven DJ, Dorn GW II. Deep mRNA sequencing for in vivo functional analysis of cardiac transcriptional regulators: Application to Galphaq. Circ Res. 2010;106:1459-1467.
24. Shin JH, Ko HS, Kang H, Lee Y, Lee YI, Pletinkova O, Troconso JC, Dawson VL, Dawson TM. PARIS (ZNF746) repression of PGC-1α contributes to neurodegeneration in Parkinson's disease. Cell. 2011;144:689-702.
25. Dorn GW II, Clark CF, Eschenbacher WH, Kang MY, Engelhard JT, Warner SJ, Matkovich SJ, Jowdy CC. MARF and Opa1 control mitochondrial and cardiac function in Drosophila. Circ Res. 2011; 108:12-17.
26. Eschenbacher WH, Song M, Chen Y, Bhandari P, Zhao P, Jowdy CC, Engelhard JT, Dorn GW II. Two rare human mitofusin 2 mutations alter mitochondrial dynamics and induce retinal and cardiac pathology in Drosophila. PLoS One. 2012;7:44296.
27. Sandebring A, Dehvari N, Perez-Manso M, Thomas KJ, Karpilovski E, Cookson MR, Cowburn RF, Cedazo-Mínguez A. Parkin deficiency disrupts calcium homeostasis by modulating phospholipase C signalling. FEBS J. 2009;276:5041-5052.
28. Calì T, Ottolini D, Negro A, Brini M. Enhanced parkin levels favor ERmitochondria crosstalk and guarantee Ca(2+) transfer to sustain cell bioenergetics. Biochim Biophys Acta. 2013;1832:495-508.
29. Dawson TM, Dawson VL. Molecular pathways of neurodegeneration in Parkinson's disease. Science. 2003;302:819-822.
30. Tanaka A. Parkin-mediated selective mitochondrial autophagy, mitophagy: Parkin purges damaged organelles from the vital mitochondrial network. FEBS Lett. 2010;584:1386-1392.
31. Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal. 2011;15:1583-1606.
32. Chung YM, Lee SB, Kim HJ, Park SH, Kim JJ, Chung JS, Yoo YD. Replicative senescence induced by Romo1-derived reactive oxygen species. J Biol Chem. 2008;283:33763-33771.
33. Chen Y, Liu Y, Dorn GW II. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ Res. 2011;109:1327-1331.
34. Kim TY, Wang D, Kim AK, Lau E, Lin AJ, Liem DA, Zhang J, Zong NC, Lam MP, Ping P. Metabolic labeling reveals proteome dynamics of mouse mitochondria. Mol Cell Proteomics. 2012;11:1586-1594.
35. Harvey BK, Wang Y, Hoffer BJ. Transgenic rodent models of Parkinson's disease. Acta Neurochir Suppl. 2008;101:89-92.
36. Chen Y, Csordás G, Jowdy C, Schneider TG, Csordás N, Wang W, Liu Y, Kohlhaas M, Meiser M, Bergem S, Nerbonne JM, Dorn GW II, Maack C. Mitofusin 2-containing mitochondrial-reticular microdomains direct rapid cardiomyocyte bioenergetic responses via interorganelle Ca(2+) crosstalk. Circ Res. 2012;111:863-875.
37. Kasahara A, Cipolat, Chen Y, Dorn GW II, Scorrano L. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin/notch signaling. Science. 2013;342:734-737.