Proteasomal and lysosomal protein degradation and heart disease

Journal of Molecular and Cellular Cardiology

Volumn 71, Issue , 2014, Pages 16-24

  Wang, Xuejun ^a   Robbins, Jeffrey ^b  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Autophagy; Heart disease; Lysosome; Proteasome; Ubiquitin

Indexed keywords

CELL PROTEIN; COP9 SIGNALOSOME; LYSOSOMAL MEMBRANE ASSOCIATED PROTEIN 2A; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AUTOPHAGY; CARDIOMYOPATHY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME DEGRADATION; HEART DISEASE; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; ISCHEMIC HEART DISEASE; LYSOSOME; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; REVIEW; UBIQUITINATION; ANIMAL; METABOLISM;

ANIMALIA;

ANIMALS; HEART DISEASES; HUMANS; LYSOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; UBIQUITIN;

EID: 84899918569     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.11.006     Document Type: Review

References (105)

1. Calamini B., Morimoto R.I. Protein homeostasis as a therapeutic target for diseases of protein conformation. Curr Top Med Chem 2012, 12:2623-2640.
2. Powers E.T., Balch W.E. Diversity in the origins of proteostasis networks - a driver for protein function in evolution. Nat Rev Mol Cell Biol 2013, 14:237-248.
3. Willis M.S., Patterson C. Proteotoxicity and cardiac dysfunction - Alzheimer's disease of the heart?. N Engl J Med 2013, 368:455-464.
4. Wang X., Terpstra E.J. Ubiquitin receptors and protein quality control. J Mol Cell Cardiol 2013, 55:73-84.
5. Gomes A.V., Zong C., Edmondson R.D., Berhane B.T., Wang G.W., Le S., et al. The murine cardiac 26S proteasome: an organelle awaiting exploration. Ann N Y Acad Sci 2005, 1047:197-207.
6. Zong N., Li H., Li H., Lam M.P., Jimenez R.C., Kim C.S., et al. Integration of cardiac proteome biology and medicine by a specialized knowledgebase. Circ Res 2013, 113:1043-1053.
7. Cui Z., Scruggs S.B., Gilda J.E., Gomes A.V. Regulation of cardiac proteasomes by ubiquitination, sumoylation, and beyond. J Mol Cell Cardiol 2014, 71:32-42.
8. Pickering A.M., Davies K.J. Degradation of damaged proteins: the main function of the 20S proteasome. Prog Mol Biol Transl Sci 2012, 109:227-248.
9. Tanahashi N., Murakami Y., Minami Y., Shimbara N., Hendil K.B., Tanaka K. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J Biol Chem 2000, 275:14336-14345.
10. Clague M.J., Urbe S. Ubiquitin: same molecule, different degradation pathways. Cell 2010, 143:682-685.
11. Lee D.Y., Brown E.J. Ubiquilins in the crosstalk among proteolytic pathways. Biol Chem 2012, 393:441-447.
12. Walters K.J., Kleijnen M.F., Goh A.M., Wagner G., Howley P.M. Structural studies of the interaction between ubiquitin family proteins and proteasome subunit S5a. Biochemistry 2002, 41:1767-1777.
13. Liu J., Chen Q., Huang W., Horak K.M., Zheng H., Mestril R., et al. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J 2006, 20:362-364.
14. Depre C., Wang Q., Yan L., Hedhli N., Peter P., Chen L., et al. Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation 2006, 114:1821-1828.
15. Chen Q., Liu J.B., Horak K.M., Zheng H., Kumarapeli A.R., Li J., et al. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ Res 2005, 97:1018-1026.
16. Adams V., Linke A., Gielen S., Erbs S., Hambrecht R., Schuler G. Modulation of Murf-1 and MAFbx expression in the myocardium by physical exercise training. Eur J Cardiovasc Prev Rehabil 2008, 15:293-299.
17. Kloetzel P.M. Generation of major histocompatibility complex class I antigens: functional interplay between proteasomes and TPPII. Nat Immunol 2004, 5:661-669.
18. Preckel T., Fung-Leung W.P., Cai Z., Vitiello A., Salter-Cid L., Winqvist O., et al. Impaired immunoproteasome assembly and immune responses in PA28-/- mice. Science 1999, 286:2162-2165.
19. Li L., Zhao D., Wei H., Yao L., Dang Y., Amjad A., et al. REGgamma deficiency promotes premature aging via the casein kinase 1 pathway. Proc Natl Acad Sci U S A 2013, 110:11005-11010.
20. Li J., Horak K.M., Su H., Sanbe A., Robbins J., Wang X. Enhancement of proteasomal function protects against cardiac proteinopathy and ischemia/reperfusion injury in mice. J Clin Invest 2011, 121:3689-3700.
21. Li J., Powell S.R., Wang X. Enhancement of proteasome function by PA28 α overexpression protects against oxidative stress. FASEB J 2011, 25:883-893.
22. Gomes A.V., Zong C., Edmondson R.D., Li X., Stefani E., Zhang J., et al. Mapping the murine cardiac 26S proteasome complexes. Circ Res 2006, 99:362-371.
23. Seifert U., Bialy L.P., Ebstein F., Bech-Otschir D., Voigt A., Schroter F., et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 2010, 142:613-624.
24. Hussong S.A., Kapphahn R.J., Phillips S.L., Maldonado M., Ferrington D.A. Immunoproteasome deficiency alters retinal proteasome's response to stress. J Neurochem 2010, 113:1481-1490.
25. Pickering A.M., Koop A.L., Teoh C.Y., Ermak G., Grune T., Davies K.J. The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J 2010, 432:585-594.
26. Huber E.M., Basler M., Schwab R., Heinemeyer W., Kirk C.J., Groettrup M., et al. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 2012, 148:727-738.
27. Scruggs S.B., Zong N.C., Wang D., Stefani E., Ping P. Post-translational modification of cardiac proteasomes: functional delineation enabled by proteomics. Am J Physiol Heart Circ Physiol 2012, 303:H9-H18.
28. Wang D., Fang C., Zong N.C., Liem D.A., Cadeiras M., Scruggs S.B., et al. Regulation of acetylation restores proteolytic function of diseased myocardium in mouse and human. Mol Cell Proteomics 2013, [Epub ahead of print]. 10.1074/mcp.M113.028332.
29. Wang X., Pattison J.S., Su H. Posttranslational modification and quality control. Circ Res 2013, 112:367-381.
30. Day S.M. The ubiquitin proteasome system in human cardiomyopathies and heart failure. Am J Physiol Heart Circ Physiol 2013, 304:H1283-H1293.
31. Wang X., Li J., Zheng H., Su H., Powell S.R. Proteasome functional insufficiency in cardiac pathogenesis. Am J Physiol Heart Circ Physiol 2011, 301:H2207-H2219.
32. Pagan J., Seto T., Pagano M., Cittadini A. Role of the ubiquitin proteasome system in the heart. Circ Res 2013, 112:1046-1058.
33. Predmore J.M., Wang P., Davis F., Bartolone S., Westfall M.V., Dyke D.B., et al. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation 2010, 121:997-1004.
34. Weekes J., Morrison K., Mullen A., Wait R., Barton P., Dunn M.J. Hyperubiquitination of proteins in dilated cardiomyopathy. Proteomics 2003, 3:208-216.
35. Birks E.J., Latif N., Enesa K., Folkvang T., Luong le A., Sarathchandra P., et al. Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res 2008, 79:472-480.
36. Galasso G., De Rosa R., Piscione F., Iaccarino G., Vosa C., Sorriento D., et al. Myocardial expression of FOXO3a-Atrogin-1 pathway in human heart failure. Eur J Heart Fail 2010, 12:1290-1296.
37. Hein S., Arnon E., Kostin S., Schonburg M., Elsasser A., Polyakova V., et al. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 2003, 107:984-991.
38. Schubert U., Anton L.C., Gibbs J., Norbury C.C., Yewdell J.W., Bennink J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
39. Kostin S., Pool L., Elsasser A., Hein S., Drexler H.C., Arnon E., et al. Myocytes die by multiple mechanisms in failing human hearts. Circ Res 2003, 92:715-724.
40. Bennett E.J., Shaler T.A., Woodman B., Ryu K.Y., Zaitseva T.S., Becker C.H., et al. Global changes to the ubiquitin system in Huntington's disease. Nature 2007, 448:704-708.
41. Reyes-Turcu F.E., Ventii K.H., Wilkinson K.D. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009, 78:363-397.
42. Day S.M., Divald A., Wang P., Davis F., Bartolone S., Jones R., et al. Impaired assembly and post-translational regulation of 26S proteasome in human end-stage heart failure. Circ Heart Fail 2013, 6:544-549.
43. Kassiotis C., Ballal K., Wellnitz K., Vela D., Gong M., Salazar R., et al. Markers of autophagy are downregulated in failing human heart after mechanical unloading. Circulation 2009, 120:S191-S197.
44. Sanbe A., Osinska H., Saffitz J.E., Glabe C.G., Kayed R., Maloyan A., et al. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci U S A 2004, 101:10132-10136.
45. Liu J., Tang M., Mestril R., Wang X. Aberrant protein aggregation is essential for a mutant desmin to impair the proteolytic function of the ubiquitin-proteasome system in cardiomyocytes. J Mol Cell Cardiol 2006, 40:451-454.
46. Wang X., Su H., Ranek M.J. Protein quality control and degradation in cardiomyocytes. J Mol Cell Cardiol 2008, 45:11-27.
47. Kumarapeli A.R., Horak K.M., Glasford J.W., Li J., Chen Q., Liu J., et al. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J 2005, 19:2051-2053.
48. Lindsten K., Menendez-Benito V., Masucci M.G., Dantuma N.P. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol 2003, 21:897-902.
49. Schlossarek S., Englmann D.R., Sultan K.R., Sauer M., Eschenhagen T., Carrier L. Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res Cardiol 2012, 107:235.
50. Cattin M.E., Bertrand A.T., Schlossarek S., Le Bihan M.C., Skov Jensen S., Neuber C., et al. Heterozygous LmnadelK32 mice develop dilated cardiomyopathy through a combined pathomechanism of haploinsufficiency and peptide toxicity. Hum Mol Genet 2013, 22:3152-3164.
51. Tian Z., Zheng H., Li J., Li Y.F., Su H., Wang X. Genetically induced moderate inhibition of the proteasome in cardiomyocytes exacerbates myocardial ischemia-reperfusion injury in mice. Circ Res 2012, 111:532-542.
52. Tsukamoto O., Minamino T., Okada K., Shintani Y., Takashima S., Kato H., et al. Depression of proteasome activities during the progression of cardiac dysfunction in pressure-overloaded heart of mice. Biochem Biophys Res Commun 2006, 340:1125-1133.
53. Rajagopalan V., Zhao M., Reddy S., Fajardo G., Wang X., Dewey S., et al. Altered ubiquitin-proteasome signaling in right ventricular hypertrophy and failure. Am J Physiol Heart Circ Physiol 2013, 305:H551-H562.
54. Tang M., Li J., Huang W., Su H., Liang Q., Tian Z., et al. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res 2010, 88:424-433.
55. Herrmann J., Wohlert C., Saguner A.M., Flores A., Nesbitt L.L., Chade A., et al. Primary proteasome inhibition results in cardiac dysfunction. Eur J Heart Fail 2013, 15:614-623.
56. Wang X. Repeated intermittent administration of a ubiquitous proteasome inhibitor leads to restrictive cardiomyopathy. Eur J Heart Fail 2013, 15:597-598.
57. Enrico O., Gabriele B., Nadia C., Sara G., Daniele V., Giulia C., et al. Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol 2007, 138:396-397.
58. Bockorny M., Chakravarty S., Schulman P., Bockorny B., Bona R. Severe heart failure after bortezomib treatment in a patient with multiple myeloma: a case report and review of the literature. Acta Haematol 2012, 128:244-247.
59. Gupta A., Pandey A., Sethi S. Bortezomib-induced congestive cardiac failure in a patient with multiple myeloma. Cardiovasc Toxicol 2012, 12:184-187.
60. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 2008, 9:679-690.
61. Ranek M.J., Terpstra E.J.M., Li J., Kass D.A., Wang X. Protein kinase G positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 2013, 128:365-376.
62. Brodsky J.L., Skach W.R. Protein folding and quality control in the endoplasmic reticulum: recent lessons from yeast and mammalian cell systems. Curr Opin Cell Biol 2011, 23:464-475.
63. Connell P., Ballinger C.A., Jiang J., Wu Y., Thompson L.J., Hohfeld J., et al. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 2001, 3:93-96.
64. Fredrickson E.K., Rosenbaum J.C., Locke M.N., Milac T.I., Gardner R.G. Exposed hydrophobicity is a key determinant of nuclear quality control degradation. Mol Biol Cell 2011, 22:2384-2395.
65. Bengtson M.H., Joazeiro C.A. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 2010, 467:470-473.
66. Fang N.N., Ng A.H., Measday V., Mayor T. Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat Cell Biol 2011, 13:1344-1352.
67. Vilchez D., Morantte I., Liu Z., Douglas P.M., Merkwirth C., Rodrigues A.P., et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 2012, 489:263-268.
68. Divald A., Kivity S., Wang P., Hochhauser E., Roberts B., Teichberg S., et al. Myocardial ischemic preconditioning preserves postischemic function of the 26S proteasome through diminished oxidative damage to 19S regulatory particle subunits. Circ Res 2010, 106:1829-1838.
69. Campos J.C., Queliconi B.B., Dourado P.M., Cunha T.F., Zambelli V.O., Bechara L.R., et al. Exercise training restores cardiac protein quality control in heart failure. PLoS One 2012, 7:e52764.
70. van der Meer S., Zwerink M., van Brussel M., van der Valk P., Wajon E., van der Palen J. Effect of outpatient exercise training programmes in patients with chronic heart failure: a systematic review. Eur J Prev Cardiol 2012, 19:795-803.
71. Stansfield W.E., Moss N.C., Willis M.S., Tang R., Selzman C.H. Proteasome inhibition attenuates infarct size and preserves cardiac function in a murine model of myocardial ischemia-reperfusion injury. Ann Thorac Surg 2007, 84:120-125.
72. Pye J., Ardeshirpour F., McCain A., Bellinger D.A., Merricks E., Adams J., et al. Proteasome inhibition ablates activation of NF-kappa B in myocardial reperfusion and reduces reperfusion injury. Am J Physiol Heart Circ Physiol 2003, 284:H919-H926.
73. Meiners S., Dreger H., Fechner M., Bieler S., Rother W., Gunther C., et al. Suppression of cardiomyocyte hypertrophy by inhibition of the ubiquitin-proteasome system. Hypertension 2008, 51:302-308.
74. Hedhli N., Lizano P., Hong C., Fritzky L.F., Dhar S.K., Liu H., et al. Proteasome inhibition decreases cardiac remodeling after initiation of pressure overload. Am J Physiol Heart Circ Physiol 2008, 295:H1385-H1393.
75. Stansfield W.E., Tang R.H., Moss N.C., Baldwin A.S., Willis M.S., Selzman C.H. Proteasome inhibition promotes regression of left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 2008, 294:H645-H650.
76. Demasi M., Laurindo F.R. Physiological and pathological role of the ubiquitin-proteasome system in the vascular smooth muscle cell. Cardiovasc Res 2012, 95:183-193.
77. Takaoka M., Okamoto H., Ito M., Nishioka M., Kita S., Matsumura Y. Antihypertensive effect of a proteasome inhibitor in DOCA-salt hypertensive rats. Life Sci 1998, 63:PL65-PL70.
78. Li S., Wang X., Li Y., Kost C.K., Martin D.S. Bortezomib, a proteasome inhibitor, attenuates angiotensin II-induced hypertension and aortic remodeling in rats. PLoS ONE 2013, 8:e78564. 10.1371/journal.pone.0078564.
79. Li W.W., Li J., Bao J.K. Microautophagy: lesser-known self-eating. Cell Mol Life Sci 2012, 69:1125-1136.
80. Kaushik S., Cuervo A.M. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012, 22:407-417.
81. Lavandero S., Troncoso R., Rothermel B.A., Martinet W., Sadoshima J., Hill J.A. Cardiovascular autophagy: concepts, controversies and perspectives. Autophagy 2013, 9:1455-1466.
82. Iwai-Kanai E., Yuan H., Huang C., Sayen M.R., Perry-Garza C.N., Kim L., et al. A method to measure cardiac autophagic flux in vivo. Autophagy 2008, 4:322-329.
83. Su H., Li J., Menon S., Liu J., Kumarapeli A.R., Wei N., et al. Perturbation of cullin deneddylation via conditional Csn8 ablation impairs the ubiquitin-proteasome system and causes cardiomyocyte necrosis and dilated cardiomyopathy in mice. Circ Res 2011, 108:40-50.
84. Su H., Li J., Osinska H., Li F., Robbins J., Liu J., et al. The COP9 signalosome is required for autophagy, proteasome-mediated proteolysis, and cardiomyocyte survival in adult mice. Circ Heart Fail 2013, 6:1049-1057.
85. Su H., Li F., Ranek M.J., Wei N., Wang X. COP9 signalosome regulates autophagosome maturation. Circulation 2011, 124:2117-2128.
86. Zheng Q., Su H., Tian Z., Wang X. Proteasome malfunction activates macroautophagy in the heart. Am J Cardiovasc Dis 2011, 1:214-226.
87. Tannous P., Zhu H., Nemchenko A., Berry J.M., Johnstone J.L., Shelton J.M., et al. Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation 2008, 117:3070-3078.
88. Zheng Q., Su H., Ranek M.J., Wang X. Autophagy and p62 in cardiac proteinopathy. Circ Res 2011, 109:296-308.
89. 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.
90. Pattison J.S., Osinska H., Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res 2011, 109:151-160.
91. 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.
92. Maron B.J., Roberts W.C., Arad M., Haas T.S., Spirito P., Wright G.B., et al. Clinical outcome and phenotypic expression in LAMP2 cardiomyopathy. JAMA 2009, 301:1253-1259.
93. 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.
94. Sun M., Ouzounian M., de Couto G., Chen M., Yan R., Fukuoka M., et al. Cathepsin-L ameliorates cardiac hypertrophy through activation of the autophagy-lysosomal dependent protein processing pathways. J Am Heart Assoc 2013, 2:e000191.
95. Tang Q., Cai J., Shen D., Bian Z., Yan L., Wang Y.X., et al. Lysosomal cysteine peptidase cathepsin L protects against cardiac hypertrophy through blocking AKT/GSK3beta signaling. J Mol Med (Berl) 2009, 87:249-260.
96. Ma X., Liu H., Foyil S.R., Godar R.J., Weinheimer C.J., Diwan A. Autophagy is impaired in cardiac ischemia-reperfusion injury. Autophagy 2012, 8:1394-1396.
97. Ma X., Liu H., Foyil S.R., Godar R.J., Weinheimer C.J., Hill J.A., et al. Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation 2012, 125:3170-3181.
98. Matsui Y., Takagi H., Qu X., Abdellatif M., Sakoda H., Asano T., et al. 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.
99. Hariharan N., Zhai P., Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011, 14:2179-2190.
100. Settembre C., Zoncu R., Medina D.L., Vetrini F., Erdin S., Huynh T., et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012, 31:1095-1108.
101. Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., et al. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
102. Chaanine A.H., Gordon R.E., Kohlbrenner E., Benard L., Jeong D., Hajjar R.J. Potential role of BNIP3 in cardiac remodeling, myocardial stiffness, and endoplasmic reticulum: mitochondrial calcium homeostasis in diastolic and systolic heart failure. Circ Heart Fail 2013, 6:572-583.
103. Lee Y., Lee H.Y., Hanna R.A., Gustafsson A.B. Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am J Physiol Heart Circ Physiol 2011, 301:H1924-H1931.
104. Rikka S., Quinsay M.N., Thomas R.L., Kubli D.A., Zhang X., Murphy A.N., et al. Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ 2011, 18:721-731.
105. Ma X., Godar R.J., Liu H., Diwan A. Enhancing lysosome biogenesis attenuates BNIP3-induced cardiomyocyte death. Autophagy 2012, 8:297-309.