The role of autophagic degradation in the heart

Journal of Molecular and Cellular Cardiology

Volumn 78, Issue , 2015, Pages 73-79

  Nishida, Kazuhiko ^a   Taneike, Manabu ^a   Otsu, Kinya ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Autophagy; Cardioprotection; Inflammation; Mitochondria; Mitophagy; Reverse remodeling

Indexed keywords

AGING; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CARDIOMYOPATHY; DEGRADATION KINETICS; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HOMEOSTASIS; HUMAN; INFLAMMATION; MACROAUTOPHAGY; MITOPHAGY; MOLECULAR MODEL; NONHUMAN; REVIEW; ANIMAL; CARDIAC MUSCLE; CARDIOMEGALY; CELL AGING; HEART MITOCHONDRION; HEART VENTRICLE REMODELING; METABOLISM;

ANIMALS; AUTOPHAGY; CARDIOMEGALY; CARDIOMYOPATHIES; CELL AGING; HEART FAILURE; HUMANS; MITOCHONDRIA, HEART; MITOCHONDRIAL DEGRADATION; MYOCARDIUM; VENTRICULAR REMODELING;

EID: 84916642028     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.09.029     Document Type: Review

References (71)

1. Lamb C.A., Yoshimori T., Tooze S.A. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 2013, 14:759-774.
2. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 2011, 27:107-132.
3. Mizushima N., Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011, 147:728-741.
4. Kuma A., Hatano M., Matsui M., Yamamoto A., Nakaya H., Yoshimori T., et al. The role of autophagy during the early neonatal starvation period. Nature 2004, 432:1032-1036.
5. Komatsu M., Waguri S., Ueno T., Iwata J., Murata S., Tanida I., et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005, 169:425-434.
6. Palikaras K., Tavernarakis N. Mitochondrial homeostasis: the interplay between mitophagy and mitochondrial biogenesis. Exp Gerontol 2014, 56:182-188.
7. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat Rev Mol Cell Biol 2011, 12:9-14.
8. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008, 27:433-446.
9. Campello S., Strappazzon F., Cecconi F. Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta 1837, 2014:451-460.
10. Gomes L.C., Di Benedetto G., Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 2011, 13:589-598.
11. Hamasaki M., Furuta N., Matsuda A., Nezu A., Yamamoto A., Fujita N., et al. Autophagosomes form at ER-mitochondria contact sites. Nature 2013, 495:389-393.
12. Axe E.L., Walker S.A., Manifava M., Chandra P., Roderick H.L., Habermann A., et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008, 182:685-701.
13. Yamamoto H., Kakuta S., Watanabe T.M., Kitamura A., Sekito T., Kondo-Kakuta C., et al. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012, 198:219-233.
14. Shen H.M., Mizushima N. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends Biochem Sci 2014, 39:61-71.
15. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., et al. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.
16. Itakura E., Kishi-Itakura C., Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 2012, 151:1256-1269.
17. Noda N.N., Ohsumi Y., Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett 2010, 584:1379-1385.
18. Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009, 17:87-97.
19. Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 2009, 17:98-109.
20. Zhang J., Ney P.A. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ 2009, 16:939-946.
21. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 2010, 11:45-51.
22. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson A.B. 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, 287:19094-19104.
23. Liu L., Feng D., Chen G., Chen M., Zheng Q., Song P., et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 2012, 14:177-185.
24. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., et al. Mutations in the Parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392:605-608.
25. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
26. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010, 12:119-131.
27. Gegg M.E., Cooper J.M., Chau K.Y., Rojo M., Schapira A.H., Taanman J.W. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/Parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 2010, 19:4861-4870.
28. Kubli D.A., Gustafsson A.B. Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res 2012, 111:1208-1221.
29. Lee J.Y., Nagano Y., Taylor J.P., Lim K.L., Yao T.P. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J Cell Biol 2010, 189:671-679.
30. Narendra D., Kane L.A., Hauser D.N., Fearnley I.M., Youle R.J. p62/SQSTM1 is required for parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010, 6:1090-1106.
31. Kirkin V., Lamark T., Sou Y.S., Bjorkoy G., Nunn J.L., Bruun J.A., et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009, 33:505-516.
32. Hollville E., Carroll R.G., Cullen S.P., Martin S.J. Bcl-2 family proteins participate in mitochondrial quality control by regulating parkin/PINK1-dependent mitophagy. Mol Cell 2014, 55:451-466.
33. Van Humbeeck C., Cornelissen T., Hofkens H., Mandemakers W., Gevaert K., De Strooper B., et al. Parkin interacts with Ambra1 to induce mitophagy. J Neurosci 2011, 31:10249-10261.
34. Huynh D.P., Dy M., Nguyen D., Kiehl T.R., Pulst S.M. Differential expression and tissue distribution of parkin isoforms during mouse development. Dev Brain Res 2001, 130:173-181.
35. Pawlyk A.C., Giasson B.I., Sampathu D.M., Perez F.A., Lim K.L., Dawson V.L., et al. Novel monoclonal antibodies demonstrate biochemical variation of brain parkin with age. J Biol Chem 2003, 278:48120-48128.
36. Matsuda N., Sato S., Shiba K., Okatsu K., Saisho K., Gautier C.A., et al. PINK1 stabilized by mitochondrial depolarization recruits parkin to damaged mitochondria and activates latent parkin for mitophagy. J Cell Biol 2010, 189:211-221.
37. Schaper J., Meiser E., Stammler G. Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice, and from human hearts. Circ Res 1985, 56:377-391.
38. Nakai A., Yamaguchi O., Takeda T., Higuchi Y., Hikoso S., Taniike M., et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007, 13:619-624.
39. Nishida Y., Arakawa S., Fujitani K., Yamaguchi H., Mizuta T., Kanaseki T., et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009, 461:654-658.
40. Honda S., Arakawa S., Nishida Y., Yamaguchi H., Ishii E., Shimizu S. Ulk1-mediated Atg5-independent macroautophagy mediates elimination of mitochondria from embryonic reticulocytes. Nat Commun 2014, 5:4004.
41. Osterholt M., Nguyen T.D., Schwarzer M., Doenst T. Alterations in mitochondrial function in cardiac hypertrophy and heart failure. Heart Fail Rev 2013, 18:645-656.
42. Levy D., Garrison R.J., Savage D.D., Kannel W.B., Castelli W.P. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 1990, 322:1561-1566.
43. Cao D.J., Wang Z.V., Battiprolu P.K., Jiang N., Morales C.R., Kong Y., et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci U S A 2011, 108:4123-4128.
44. Oyabu J., Yamaguchi O., Hikoso S., Takeda T., Oka T., Murakawa T., et al. Autophagy-mediated degradation is necessary for regression of cardiac hypertrophy during ventricular unloading. Biochem Biophys Res Commun 2013, 441:787-792.
45. Tarazi R.C., Fouad F.M. Reversal of cardiac hypertrophy by medical treatment. Annu Rev Med 1985, 36:407-414.
46. Christakis G.T., Joyner C.D., Morgan C.D., Fremes S.E., Buth K.J., Sever J.Y., et al. Left ventricular mass regression early after aortic valve replacement. Ann Thorac Surg 1996, 62:1084-1089.
47. Zafeiridis A., Jeevanandam V., Houser S.R., Margulies K.B. Regression of cellular hypertrophy after left ventricular assist device support. Circulation 1998, 98:656-662.
48. Schmieder R.E., Martus P., Klingbeil A. Reversal of left ventricular hypertrophy in essential hypertension. A meta-analysis of randomized double-blind studies. JAMA 1996, 275:1507-1513.
49. Hariharan N., Ikeda Y., Hong C., Alcendor R.R., Usui S., Gao S., et al. Autophagy plays an essential role in mediating regression of hypertrophy during unloading of the heart. PLoS One 2013, 8:e51632.
50. Cao D.J., Jiang N., Blagg A., Johnstone J.L., Gondalia R., Oh M., et al. Mechanical unloading activates FoxO3 to trigger Bnip3-dependent cardiomyocyte atrophy. J Am Heart Assoc 2013, 2:e000016.
51. Vanbilsen M., Smeets P., Gilde A., Vandervusse G. Metabolic remodelling of the failing heart: the cardiac burn-out syndrome?. Cardiovasc Res 2004, 61:218-226.
52. Nishida K., Kyoi S., Yamaguchi O., Sadoshima J., Otsu K. The role of autophagy in the heart. Cell Death Differ 2009, 16:31-38.
53. Oka T., Hikoso S., Yamaguchi O., Taneike M., Takeda T., Tamai T., et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485:251-255.
54. Zhu H., Tannous P., Johnstone J.L., Kong Y., Shelton J.M., Richardson J.A., et al. Cardiac autophagy is a maladaptive response to hemodynamic stress. J Clin Invest 2007, 117:1782-1793.
55. Rothermel B.A., Hill J.A. Autophagy in load-induced heart disease. Circ Res 2008, 103:1363-1369.
56. Danon M.J., Oh S.J., DiMauro S., Manaligod J.R., Eastwood A., Naidu S., et al. Lysosomal glycogen storage disease with normal acid maltase. Neurology 1981, 31:51-57.
57. Cheng Z., Fang Q. Danon disease: focusing on heart. J Hum Genet 2012, 57:407-410.
58. Tanaka Y., Guhde G., Suter A., Eskelinen E.L., Hartmann D., Lullmann-Rauch R., et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000, 406:902-906.
59. Nishino I., Fu J., Tanji K., Yamada T., Shimojo S., Koori T., et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 2000, 406:906-910.
60. Tannous P., Zhu H., Johnstone J.L., Shelton J.M., Rajasekaran N.S., Benjamin I.J., et al. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci U S A 2008, 105:9745-9750.
61. Pattison J.S., Osinska H., Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res 2011, 109:151-160.
62. Bhuiyan M.S., Pattison J.S., Osinska H., James J., Gulick J., McLendon P.M., et al. Enhanced autophagy ameliorates cardiac proteinopathy. J Clin Invest 2013, 123:5284-5297.
63. Kobayashi S., Liang Q. Autophagy and mitophagy in diabetic cardiomyopathy. Biochim Biophys Acta 2014, [in press].
64. Xu X., Kobayashi S., Chen K., Timm D., Volden P., Huang Y., et al. Diminished autophagy limits cardiac injury in mouse models of type 1 diabetes. J Biol Chem 2013, 288:18077-18092.
65. Dutta D., Calvani R., Bernabei R., Leeuwenburgh C., Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ Res 2012, 110:1125-1138.
66. Taneike M., Yamaguchi O., Nakai A., Hikoso S., Takeda T., Mizote I., et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy 2010, 6:600-606.
67. Pyo J.O., Yoo S.M., Ahn H.H., Nah J., Hong S.H., Kam T.I., et al. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat Commun 2013, 4:2300.
68. Hammerling B.C., Gustafsson A.B. Mitochondrial quality control in the myocardium: cooperation between protein degradation and mitophagy. J Mol Cell Cardiol 2014, 75:122-130.
69. Hoshino A., Mita Y., Okawa Y., Ariyoshi M., Iwai-Kanai E., Ueyama T., et al. Cytosolic p53 inhibits parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat Commun 2013, 4:2308.
70. Kubli D.A., Zhang X., Lee Y., Hanna R.A., Quinsay M.N., Nguyen C.K., et al. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 2013, 288:915-926.
71. Rodriguez-Navarro J.A., Casarejos M.J., Menendez J., Solano R.M., Rodal I., Gomez A., et al. Mortality, oxidative stress and tau accumulation during ageing in parkin null mice. J Neurochem 2007, 103:98-114.