The interplay between autophagy and apoptosis in the diabetic heart

Journal of Molecular and Cellular Cardiology

Volumn 71, Issue , 2014, Pages 71-80

  Ouyang, Changhan ^a   You, Jieyun ^a   Xie, Zhonglin ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

AMPK; Apoptosis; Autophagy; Diabetic cardiomyopathy

Indexed keywords

ADENYLATE KINASE; GLUCOSE; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

ACETYLATION; APOPTOSIS; AUTOPHAGY; CELL FUNCTION; CELL SURVIVAL; DEACETYLATION; DIABETIC CARDIOMYOPATHY; DISEASE ASSOCIATION; DYSLIPIDEMIA; GLUCOSE BLOOD LEVEL; HEART FAILURE; HEART MUSCLE CELL; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; INSULIN SENSITIVITY; MOLECULAR INTERACTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANIMAL; DIABETES MELLITUS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; AUTOPHAGY; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHIES; HUMANS; MYOCYTES, CARDIAC;

EID: 84899929877     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.10.014     Document Type: Review

References (122)

1. Asrih M., Steffens S. Emerging role of epigenetics and miRNA in diabetic cardiomyopathy. Cardiovasc Pathol 2013, 22:117-125.
2. Frustaci A., Kajstura J., Chimenti C., Jakoniuk I., Leri A., Maseri A., et al. Myocardial cell death in human diabetes. Circ Res 2000, 87:1123-1132.
3. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004, 6:463-477.
4. Rubler S., Dlugash J., Yuceoglu Y.Z., Kumral T., Branwood A.W., Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972, 30:595-602.
5. Kannel W.B., McGee D.L. Diabetes and cardiovascular disease. The Framingham study. JAMA 1979, 241:2035-2038.
6. Schannwell C.M., Schneppenheim M., Perings S., Plehn G., Strauer B.E. Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology 2002, 98:33-39.
7. Carugo S., Giannattasio C., Calchera I., Paleari F., Gorgoglione M.G., Grappiolo A., et al. Progression of functional and structural cardiac alterations in young normotensive uncomplicated patients with type 1 diabetes mellitus. J Hypertens 2001, 19:1675-1680.
8. Boudina S., Abel E.D. Diabetic cardiomyopathy revisited. Circulation 2007, 115:3213-3223.
9. Stratton I.M., Adler A.I., Neil H.A., Matthews D.R., Manley S.E., Cull C.A., et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000, 321:405-412.
10. Francis G.S. Diabetic cardiomyopathy: fact or fiction?. Heart 2001, 85:247-248.
11. Epstein P.N., Overbeek P.A., Means A.R. Calmodulin-induced early-onset diabetes in transgenic mice. Cell 1989, 58:1067-1073.
12. Xie Z., Lau K., Eby B., Lozano P., He C., Pennington B., et al. Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 2011, 60:1770-1778.
13. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce W.M., Klein J.B., et al. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 2004, 287:E896-E905.
14. Cai L., Li W., Wang G., Guo L., Jiang Y., Kang Y.J. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002, 51:1938-1948.
15. Zhou Y.T., Grayburn P., Karim A., Shimabukuro M., Higa M., Baetens D., et al. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci U S A 2000, 97:1784-1789.
16. Shehadeh A., Regan T.J. Cardiac consequences of diabetes mellitus. Clin Cardiol 1995, 18:301-305.
17. Regan T.J., Lyons M.M., Ahmed S.S., Levinson G.E., Oldewurtel H.A., Ahmad M.R., et al. Evidence for cardiomyopathy in familial diabetes mellitus. J Clin Invest 1977, 60:884-899.
18. Fang Z.Y., Prins J.B., Marwick T.H. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 2004, 25:543-567.
19. Galderisi M., Anderson K.M., Wilson P.W., Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol 1991, 68:85-89.
20. Devereux R.B., Roman M.J., Paranicas M., O'Grady M.J., Lee E.T., Welty T.K., et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 2000, 101:2271-2276.
21. Nunoda S., Genda A., Sugihara N., Nakayama A., Mizuno S., Takeda R. Quantitative approach to the histopathology of the biopsied right ventricular myocardium in patients with diabetes mellitus. Heart Vessels 1985, 1:43-47.
22. Syrovy I., Hodny Z. Non-enzymatic glycosylation of myosin: effects of diabetes and ageing. Gen Physiol Biophys 1992, 11:301-307.
23. Regan T.J., Khan M.I., Jesrani M.U., Oldewurtel H.A., Ettinger P.O. Alterations of myocardial function and metabolism in chronic diabetes mellitus. Recent Adv Stud Cardiac Struct Metab 1973, 3:169-178.
24. Bauters C., Lamblin N., Mc Fadden E.P., Van Belle E., Millaire A., de Groote P. Influence of diabetes mellitus on heart failure risk and outcome. Cardiovasc Diabetol 2003, 2:1.
25. Ziegelhoffer A., Ravingerova T., Styk J., Sebokova J., Waczulikova I., Breier A., et al. Mechanisms that may be involved in calcium tolerance of the diabetic heart. Mol Cell Biochem 1997, 176:191-198.
26. He C., Zhu H., Zhang W., Okon I., Wang Q., Li H., et al. 7-Ketocholesterol induces autophagy in vascular smooth muscle cells through Nox4 and Atg4B. Am J Pathol 2013, 183:626-637.
27. Li Z., Zhang T., Dai H., Liu G., Wang H., Sun Y., et al. Involvement of endoplasmic reticulum stress in myocardial apoptosis of streptozocin-induced diabetic rats. J Clin Biochem Nutr 2007, 41:58-67.
28. Kuethe F., Sigusch H.H., Bornstein S.R., Hilbig K., Kamvissi V., Figulla H.R. Apoptosis in patients with dilated cardiomyopathy and diabetes: a feature of diabetic cardiomyopathy?. Horm Metab Res 2007, 39:672-676.
29. He C., Zhu H., Li H., Zou M.H., Xie Z. Dissociation of Bcl-2-Beclin1 complex by activated AMPK enhances cardiac autophagy and protects against cardiomyocyte apoptosis in diabetes. Diabetes 2013, 62:1270-1281.
30. Xie Z., He C., Zou M.H. AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy 2011, 7:1254-1255.
31. Zou M.H., Xie Z. Regulation of interplay between autophagy and apoptosis in the diabetic heart: new role of AMPK. Autophagy 2013, 9:624-625.
32. Fiordaliso F., Li B., Latini R., Sonnenblick E.H., Anversa P., Leri A., et al. Myocyte death in streptozotocin-induced diabetes in rats in angiotensin II- dependent. Lab Invest 2000, 80:513-527.
33. Chen S., Evans T., Mukherjee K., Karmazyn M., Chakrabarti S. Diabetes-induced myocardial structural changes: role of endothelin-1 and its receptors. J Mol Cell Cardiol 2000, 32:1621-1629.
34. Chiu H.C., Kovacs A., Ford D.A., Hsu F.F., Garcia R., Herrero P., et al. A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest 2001, 107:813-822.
35. Song Y., Wang J., Li Y., Du Y., Arteel G.E., Saari J.T., et al. Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am J Pathol 2005, 167:17-26.
36. Ye G., Metreveli N.S., Ren J., Epstein P.N. Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting reactive oxygen species production. Diabetes 2003, 52:777-783.
37. Klionsky D.J., Cregg J.M., Dunn W.A., Emr S.D., Sakai Y., Sandoval I.V., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003, 5:539-545.
38. Kihara A., Kabeya Y., Ohsumi Y., Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2001, 2:330-335.
39. Zeng X., Overmeyer J.H., Maltese W.A. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 2006, 119:259-270.
40. Stack J.H., DeWald D.B., Takegawa K., Emr S.D. Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J Cell Biol 1995, 129:321-334.
41. Kroemer G., Marino G., Levine B. Autophagy and the integrated stress response. Mol Cell 2010, 40:280-293.
42. Kimura S., Fujita N., Noda T., Yoshimori T. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 2009, 452:1-12.
43. Levine B., Yuan J. Autophagy in cell death: an innocent convict?. J Clin Invest 2005, 115:2679-2688.
44. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728.
45. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171:603-614.
46. Ju J.S., Varadhachary A.S., Miller S.E., Weihl C.C. Quantitation of "autophagic flux" in mature skeletal muscle. Autophagy 2010, 6:929-935.
47. Neufeld T.P. TOR-dependent control of autophagy: biting the hand that feeds. Curr Opin Cell Biol 2010, 22:157-168.
48. Chong Z.Z., Shang Y.C., Maiese K. Cardiovascular disease and mTOR signaling. Trends Cardiovasc Med 2011, 21:151-155.
49. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011, 13:132-141.
50. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
51. Avruch J., Long X., Ortiz-Vega S., Rapley J., Papageorgiou A., Dai N. Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 2009, 296:E592-E602.
52. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007, 8:774-785.
53. Shirwany N.A., Zou M.H. AMPK in cardiovascular health and disease. Acta Pharmacol Sin 2010, 31:1075-1084.
54. Xie Z., Dong Y., Zhang M., Cui M.Z., Cohen R.A., Riek U., et al. Activation of protein kinase C zeta by peroxynitrite regulates LKB1-dependent AMP-activated protein kinase in cultured endothelial cells. J Biol Chem 2006, 281:6366-6375.
55. Xie Z., Dong Y., Zhang J., Scholz R., Neumann D., Zou M.H. Identification of the serine 307 of LKB1 as a novel phosphorylation site essential for its nucleocytoplasmic transport and endothelial cell angiogenesis. Mol Cell Biol 2009, 29:3582-3596.
56. Xie Z., Zhang J., Wu J., Viollet B., Zou M.H. Upregulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes 2008, 57:3222-3230.
57. Xie Z., Dong Y., Scholz R., Neumann D., Zou M.H. Phosphorylation of LKB1 at serine 428 by protein kinase C-zeta is required for metformin-enhanced activation of the AMP-activated protein kinase in endothelial cells. Circulation 2008, 117:952-962.
58. Shaw R.J. LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol (Oxf) 2009, 196:65-80.
59. Shang L., Chen S., Du F., Li S., Zhao L., Wang X. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci U S A 2011, 108:4788-4793.
60. Kim J., Kim Y.C., Fang C., Russell R.C., Kim J.H., Fan W., et al. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 2013, 152:290-303.
61. Nemchenko A., Chiong M., Turer A., Lavandero S., Hill J.A. Autophagy as a therapeutic target in cardiovascular disease. J Mol Cell Cardiol 2011, 51:584-593.
62. Cui M., Yu H., Wang J., Gao J., Li J. Chronic caloric restriction and exercise improve metabolic conditions of dietary-induced obese mice in autophagy correlated manner without involving AMPK. J Diabetes Res 2013, 2013:852754.
63. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.
64. Lee I.H., Finkel T. Regulation of autophagy by the p300 acetyltransferase. J Biol Chem 2009, 284:6322-6328.
65. Lee I.H., Cao L., Mostoslavsky R., Lombard D.B., Liu J., Bruns N.E., et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A 2008, 105:3374-3379.
66. Yi C., Ma M., Ran L., Zheng J., Tong J., Zhu J., et al. Function and molecular mechanism of acetylation in autophagy regulation. Science 2012, 336:474-477.
67. Lin S.Y., Li T.Y., Liu Q., Zhang C., Li X., Chen Y., et al. GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science 2012, 336:477-481.
68. Giricz Z., Mentzer R.M., Gottlieb R.A. Autophagy, myocardial protection, and the metabolic syndrome. J Cardiovasc Pharmacol 2012, 60:125-132.
69. Mizushima N., Yamamoto A., Matsui M., Yoshimori T., Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004, 15:1101-1111.
70. Wohlgemuth S.E., Julian D., Akin D.E., Fried J., Toscano K., Leeuwenburgh C., et al. Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res 2007, 10:281-292.
71. Pfeifer U. Inverted diurnal rhythm of cellular autophagy in liver cells of rats fed a single daily meal. Virchows Arch B Cell Pathol 1972, 10:1-3.
72. Shinmura K., Tamaki K., Saito K., Nakano Y., Tobe T., Bolli R. Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase. Circulation 2007, 116:2809-2817.
73. Xu X., Hua Y., Nair S., Zhang Y., Ren J. Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J Mol Cell Biol 2013, 5:61-63.
74. 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.
75. Akazawa H., Komazaki S., Shimomura H., Terasaki F., Zou Y., Takano H., et al. Diphtheria toxin-induced autophagic cardiomyocyte death plays a pathogenic role in mouse model of heart failure. J Biol Chem 2004, 279:41095-41103.
76. Gustafsson A.B.., Gottlieb R.A. Autophagy in ischemic heart disease. Circ Res 2009, 104:150-158.
77. Yan L., Vatner D.E., Kim S.J., Ge H., Masurekar M., Massover W.H., et al. Autophagy in chronically ischemic myocardium. Proc Natl Acad Sci U S A 2005, 102:13807-13812.
78. 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.
79. 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.
80. 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.
81. Kobayashi S., Xu X., Chen K., Liang Q. Suppression of autophagy is protective in high glucose-induced cardiomyocyte injury. Autophagy 2012, 8:577-592.
82. 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, 88:18077-18092.
83. Yang L., Li P., Fu S., Calay E.S., Hotamisligil G.S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 2010, 11:467-478.
84. Ebato C., Uchida T., Arakawa M., Komatsu M., Ueno T., Komiya K., et al. Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab 2008, 8:325-332.
85. Fujitani Y., Kawamori R., Watada H. The role of autophagy in pancreatic beta-cell and diabetes. Autophagy 2009, 5:280-282.
86. Marsh B.J., Soden C., Alarcon C., Wicksteed B.L., Yaekura K., Costin A.J., et al. Regulated autophagy controls hormone content in secretory-deficient pancreatic endocrine beta-cells. Mol Endocrinol 2007, 21:2255-2269.
87. Sciarretta S., Zhai P., Shao D., Maejima Y., Robbins J., Volpe M., et al. Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation 2012, 125:1134-1146.
88. Li Z.L., Woollard J.R., Ebrahimi B., Crane J.A., Jordan K.L., Lerman A., et al. Transition from obesity to metabolic syndrome is associated with altered myocardial autophagy and apoptosis. Arterioscler Thromb Vasc Biol 2012, 32:1132-1141.
89. Mellor K.M., Bell J.R., Young M.J., Ritchie R.H., Delbridge L.M. Myocardial autophagy activation and suppressed survival signaling is associated with insulin resistance in fructose-fed mice. J Mol Cell Cardiol 2011, 50:1035-1043.
90. Masini M., Bugliani M., Lupi R., del Guerra S., Boggi U., Filipponi F., et al. Autophagy in human type 2 diabetes pancreatic beta cells. Diabetologia 2009, 52:1083-1086.
91. Masini M., Lupi R., Bugliani M., Boggi U., Filipponi F., Masiello P., et al. A role for autophagy in beta-cell life and death. Islets 2009, 1:157-159.
92. Yan J., Feng Z., Liu J., Shen W., Wang Y., Wertz K., et al. Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate. J Nutr Biochem 2012, 23:716-724.
93. Li H., Xu M., Lee J., He C., Xie Z. Leucine supplementation increases SIRT1 expression and prevents mitochondrial dysfunction and metabolic disorders in high-fat diet-induced obese mice. Am J Physiol Endocrinol Metab 2012, 303:E1234-E1244.
94. Glazer H.P., Osipov R.M., Clements R.T., Sellke F.W., Bianchi C. Hypercholesterolemia is associated with hyperactive cardiac mTORC1 and mTORC2 signaling. Cell Cycle 2009, 8:1738-1746.
95. Koga H., Kaushik S., Cuervo A.M. Altered lipid content inhibits autophagic vesicular fusion. FASEB J 2010, 24:3052-3065.
96. Mellor K.M., Reichelt M.E., Delbridge L.M. Autophagic predisposition in the insulin resistant diabetic heart. Life Sci 2013, 92:616-620.
97. Morales C.R., Pedrozo Z., Lavandero S., Hill J.A. Oxidative stress and autophagy in cardiovascular homeostasis. Antioxid Redox Signal 2013, (in press).
98. Luo C., Li Y., Wang H., Feng Z., Li Y., Long J., et al. Mitochondrial accumulation under oxidative stress is due to defects in autophagy. J Cell Biochem 2013, 114:212-219.
99. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007, 26:1749-1760.
100. Su J., Zhou L., Kong X., Yang X., Xiang X., Zhang Y., et al. Endoplasmic reticulum is at the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in the pathogenesis of diabetes mellitus. J Diabetes Res 2013, 2013:193461.
101. Salminen A., Kaarniranta K., Kauppinen A. Beclin 1 interactome controls the crosstalk between apoptosis, autophagy and inflammasome activation: Impact on the aging process. Ageing Res Rev 2013, 12:520-534.
102. Zhou F., Yang Y., Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 2011, 278:403-413.
103. Maiuri M.C., Criollo A., Kroemer G. Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO J 2010, 29:515-516.
104. Djavaheri-Mergny M., Maiuri M.C., Kroemer G. Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene 2010, 29:1717-1719.
105. Kang R., Zeh H.J., Lotze M.T., Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011, 18:571-580.
106. Lamparska-Przybysz M., Gajkowska B., Motyl T. BID-deficient breast cancer MCF-7 cells as a model for the study of autophagy in cancer therapy. Autophagy 2006, 2:47-48.
107. Park J.H., Lee J.E., Shin I.C., Koh H.C. Autophagy regulates chlorpyrifos-induced apoptosis in SH-SY5Y cells. Toxicol Appl Pharmacol 2013, 268:55-67.
108. He W., Wang Q., Xu J., Xu X., Padilla M.T., Ren G., et al. Attenuation of TNFSF10/TRAIL-induced apoptosis by an autophagic survival pathway involving T. Autophagy 2012, 8:1811-1821.
109. Takagi H., Matsui Y., Hirotani S., Sakoda H., Asano T., Sadoshima J. AMPK mediates autophagy during myocardial ischemia in vivo. Autophagy 2007, 3:405-407.
110. Valentim L., Laurence K.M., Townsend P.A., Carroll C.J., Soond S., Scarabelli T.M., et al. Urocortin inhibits Beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury. J Mol Cell Cardiol 2006, 40:846-852.
111. Matsui Y., Kyoi S., Takagi H., Hsu C.P., Hariharan N., Ago T., et al. Molecular mechanisms and physiological significance of autophagy during myocardial ischemia and reperfusion. Autophagy 2008, 4:409-415.
112. Lavandero S., Troncoso R., Rothermel B.A., Martinet W., Sadoshima J., Hill J.A. Cardiovascular autophagy: concepts, controversies and perspectives. Autophagy 2013, 8:1334-1344.
113. Miyata S., Takemura G., Kawase Y., Li Y., Okada H., Maruyama R., et al. Autophagic cardiomyocyte death in cardiomyopathic hamsters and its prevention by granulocyte colony-stimulating factor. Am J Pathol 2006, 168:386-397.
114. 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.
115. Oberstein A., Jeffrey P.D., Shi Y. Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 2007, 282:13123-13132.
116. Levine B., Sinha S., Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008, 4:600-606.
117. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
118. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007, 8:741-752.
119. Wei Y., Pattingre S., Sinha S., Bassik M., Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 2008, 30:678-688.
120. Wirawan E., Vande W.L., Kersse K., Cornelis S., Claerhout S., Vanoverberghe I., et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 2010, 1:e18.
121. Yousefi S., Perozzo R., Schmid I., Ziemiecki A., Schaffner T., Scapozza L., et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006, 8:1124-1132.
122. Betin V.M., Lane J.D. Atg4D at the interface between autophagy and apoptosis. Autophagy 2009, 5:1057-1059.