Drp1-dependent mitochondrial autophagy plays a protective role against pressure overload-induced mitochondrial dysfunction and heart failure

Circulation

Volumn 133, Issue 13, 2016, Pages 1249-1263

  Shirakabe, Akihiro ^a   Zhai, Peiyong ^a   Ikeda, Yoshiyuki ^a,b   Saito, Toshiro ^a   Maejima, Yasuhiro ^a   Hsu, Chiao Po ^d   Nomura, Masatoshi ^c   Egashira, Kensuke ^e,f   Levine, Beth ^g   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e KYUSHU UNIVERSITY HOSPITAL   (Japan)

^f KYUSHU UNIVERSITY   (Japan)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

autophagy; Drp1 protein, mouse; hypertrophy; mitochondria

Indexed keywords

BECLIN 1; DRP1 PROTEIN; GUANOSINE TRIPHOSPHATASE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; DNM1L PROTEIN, MOUSE; DYNAMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BECLIN 1 GENE; CONTROLLED STUDY; DISEASE EXACERBATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; DRP1 GENE; ELECTRON MICROSCOPY; HAPLOINSUFFICIENCY; HEART EJECTION FRACTION; HEART FAILURE; HEART LEFT VENTRICLE OVERLOAD; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN TISSUE; MITOCHONDRIAL TARGETING SIGNAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY; PRESSURE; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; AUTOPHAGY; DYNAMINS; HEART FAILURE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PRESSURE;

EID: 84959213319     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.115.020502     Document Type: Article

References (31)

1. Gatica D, Chiong M, Lavandero S, Klionsky DJ, Molecular mechanisms of autophagy in the cardiovascular system. Circ Res 2015 116 456 467. doi: 10.1161/CIRCRESAHA.114.303788.
2. Maejima Y, Kyoi S, Zhai P, Liu T, Li H, Ivessa A, Sciarretta S, Del Re DP, Zablocki DK, Hsu CP, Lim DS, Isobe M, Sadoshima J, Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat Med 2013 19 1478 1488. doi: 10.1038/nm.3322.
3. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K, The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007 13 619 624. doi: 10.1038/nm1574.
4. Saito T, Sadoshima J, Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circ Res 2015 116 1477 1490. doi: 10.1161/CIRCRESAHA.116.303790.
5. Youle RJ, Narendra DP, Mechanisms of mitophagy. Nat Rev Mol Cell Biol 2011 12 9 14. doi: 10.1038/nrm3028.
6. Ikeda Y, Shirakabe A, Maejima Y, Zhai P, Sciarretta S, Toli J, Nomura M, Mihara K, Egashira K, Ohishi M, Abdellatif M, Sadoshima J, Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress. Circ Res 2015 116 264 278. doi: 10.1161/CIRCRESAHA.116.303356.
7. Zhu H, Tannous P, Johnstone JL, Kong Y, Shelton JM, Richardson JA, Le V, Levine B, Rothermel BA, Hill JA, Cardiac autophagy is a maladaptive response to hemodynamic stress. J Clin Invest 2007 117 1782 1793. doi: 10.1172/JCI27523.
8. Hariharan N, Zhai P, Sadoshima J, Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011 14 2179 2190. doi: 10.1089/ars.2010.3488.
9. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J, Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 2007 100 914 922. doi: 10.1161/01.RES.0000261924.76669.36.
10. Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A, A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol 2011 18 1042 1052. doi: 10.1016/j.chembiol.2011.05.013.
11. Shoji-Kawata S, Sumpter R, Leveno M, Campbell GR, Zou Z, Kinch L, Wilkins AD, Sun Q, Pallauf K, MacDuff D, Huerta C, Virgin HW, Helms JB, Eerland R, Tooze SA, Xavier R, Lenschow DJ, Yamamoto A, King D, Lichtarge O, Grishin NV, Spector SA, Kaloyanova DV, Levine B, Identification of a candidate therapeutic autophagy-inducing peptide. Nature 2013 494 201 206. doi: 10.1038/nature11866.
12. Iwai-Kanai E, Yuan H, Huang C, Sayen MR, Perry-Garza CN, Kim L, Gottlieb RA, A method to measure cardiac autophagic flux in vivo. Autophagy 2008 4 322 329
13. Doroudgar S, Völkers M, Thuerauf DJ, Khan M, Mohsin S, Respress JL, Wang W, Gude N, Müller OJ, Wehrens XH, Sussman MA, Glembotski CC, Hrd1 and ER-associated protein degradation, ERAD, are critical elements of the adaptive ER stress response in cardiac myocytes. Circ Res 2015 117 536 546. doi: 10.1161/CIRCRESAHA.115.306993.
14. Rogers GW, Brand MD, Petrosyan S, Ashok D, Elorza AA, Ferrick DA, Murphy AN, High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS One 2011 6 e21746. doi: 10.1371/journal.pone.0021746.
15. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J, Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ Res 2010 107 1470 1482. doi: 10.1161/CIRCRESAHA.110.227371.
16. Maejima Y, Kyoi S, Zhai P, Liu T, Li H, Ivessa A, Sciarretta S, Del Re DP, Zablocki DK, Hsu CP, Lim DS, Isobe M, Sadoshima J, Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat Med 2013 19 1478 1488. doi: 10.1038/nm.3322.
17. 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. doi: 10.1074/jbc.M112.411363.
18. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P, Scorrano L, Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci U S A 2008 105 15803 15808. doi: 10.1073/pnas.0808249105.
19. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K, Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 2007 282 11521 11529. doi: 10.1074/jbc.M607279200.
20. Hariharan N, Ikeda Y, Hong C, Alcendor RR, Usui S, Gao S, Maejima Y, Sadoshima J, Autophagy plays an essential role in mediating regression of hypertrophy during unloading of the heart. PLoS One 2013 8 e51632. doi: 10.1371/journal.pone.0051632.
21. Prosser BL, Ward CW, Lederer WJ, X-ROS signaling: rapid mechano-chemo transduction in heart. Science 2011 333 1440 1445. doi: 10.1126/science.1202768.
22. Sciarretta S, Zhai P, Shao D, Zablocki D, Nagarajan N, Terada LS, Volpe M, Sadoshima J, Activation of NADPH oxidase 4 in the endoplasmic reticulum promotes cardiomyocyte autophagy and survival during energy stress through the protein kinase RNA-activated-like endoplasmic reticulum kinase/eukaryotic initiation factor 2α/activating transcription factor 4 pathway. Circ Res 2013 113 1253 1264. doi: 10.1161/CIRCRESAHA.113.301787.
23. Sciarretta S, Zhai P, Shao D, Maejima Y, Robbins J, Volpe M, Condorelli G, Sadoshima J, Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation 2012 125 1134 1146. doi: 10.1161/CIRCULATIONAHA.111.078212.
24. Sciarretta S, Volpe M, Sadoshima J, Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ Res 2014 114 549 564. doi: 10.1161/CIRCRESAHA.114.302022.
25. Hirota Y, Yamashita S, Kurihara Y, Jin X, Aihara M, Saigusa T, Kang D, Kanki T, Mitophagy is primarily due to alternative autophagy and requires the MAPK1 and MAPK14 signaling pathways. Autophagy 2015 11 332 343. doi: 10.1080/15548627.2015.1023047.
26. Song M, Mihara K, Chen Y, Scorrano L, Dorn GW 2nd, Mitochondrial fission and fusion factors reciprocally orchestrate mitophagic culling in mouse hearts and cultured fibroblasts. Cell Metab 2015 21 273 285. doi: 10.1016/j.cmet.2014.12.011.
27. Chen H, Ren S, Clish C, Jain M, Mootha V, McCaffery JM, Chan DC, Titration of mitochondrial fusion rescues Mff-deficient cardiomyopathy. J Cell Biol 2015 211 795 805. doi: 10.1083/jcb.201507035.
28. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S, Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009 461 654 658. doi: 10.1038/nature08455.
29. Han XJ, Lu YF, Li SA, Kaitsuka T, Sato Y, Tomizawa K, Nairn AC, Takei K, Matsui H, Matsushita M, CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J Cell Biol 2008 182 573 585. doi: 10.1083/jcb.200802164.
30. Cribbs JT, Strack S, Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 2007 8 939 944. doi: 10.1038/sj.embor.7401062.
31. Wang Z, Jiang H, Chen S, Du F, Wang X, The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012 148 228 243. doi: 10.1016/j.cell.2011.11.030.