Therapeutic targeting of autophagy in cardiovascular disease

Journal of Molecular and Cellular Cardiology

Volumn 95, Issue , 2016, Pages 86-93

  Schiattarella, Gabriele G ^a   Hill, Joseph A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Cardiac hypertrophy; Heart failure; Remodeling

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMIODARONE; ANTINEOPLASTIC AGENT; CLONIDINE; DOXORUBICIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; METFORMIN; MINOXIDIL; NICARDIPINE; NIMODIPINE; RAPAMYCIN; VERAPAMIL;

APOPTOSIS; ATRIAL FIBRILLATION; AUTOPHAGY; CANCER CHEMOTHERAPY; CARDIOMYOPATHY; CARDIOTOXICITY; CARDIOVASCULAR DISEASE; HEART ARRHYTHMIA; HEART DISEASE; HEART FAILURE; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; ISCHEMIC HEART DISEASE; LYSOSOME STORAGE DISEASE; MACROAUTOPHAGY; MITOPHAGY; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; ANIMAL; CARDIAC MUSCLE CELL; CARDIOVASCULAR DISEASES; DRUG EFFECTS; LYSOSOME; METABOLISM; MOLECULARLY TARGETED THERAPY; RISK FACTOR; SIGNAL TRANSDUCTION; TRANSLATIONAL RESEARCH;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CARDIOVASCULAR DISEASES; HUMANS; LYSOSOMES; MOLECULAR TARGETED THERAPY; MYOCYTES, CARDIAC; RISK FACTORS; SIGNAL TRANSDUCTION; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84949681478     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.11.019     Document Type: Review

References (93)

1. Nabel E.G., Braunwald E. A tale of coronary artery disease and myocardial infarction. N. Engl. J. Med. 2012, 366:54-63.
2. Wilmot K.A., O'Flaherty M., Capewell S., Ford E.S., Vaccarino V. Coronary heart disease mortality declines in the United States from 1979 through 2011: evidence for stagnation in young adults, especially women. Circulation 2015, 132:997-1002.
3. Hill J.A., Olson E.N. Cardiac plasticity. N. Engl. J. Med. 2008, 358:1370-1380.
4. Galluzzi L., Bravo-San Pedro J.M., Kroemer G. Organelle-specific initiation of cell death. Nat. Cell Biol. 2014, 16:728-736.
5. Decker R.S., Poole A.R., Griffin E.E., Dingle J.T., Wildenthal K. Altered distribution of lysosomal cathepsin D in ischemic myocardium. J. Clin. Invest. 1977, 59:911-921.
6. Xie M., Morales C.R., Lavandero S., Hill J.A. Tuning flux: autophagy as a target of heart disease therapy. Curr. Opin. Cardiol. 2011, 26:216-222.
7. Lavandero S., Chiong M., Rothermel B.A., Hill J.A. Autophagy in cardiovascular biology. J. Clin. Invest. 2015, 125:55-64.
8. Wang Z.V., Hill J.A. Protein quality control and metabolism: bidirectional control in the heart. Cell Metab. 2015, 21:215-226.
9. Galluzzi L., Pietrocola F., Levine B., Kroemer G. Metabolic control of autophagy. Cell 2014, 159:1263-1276.
10. Green D.R., Galluzzi L., Kroemer G. Cell biology. Metabolic control of cell death. Science 2014, 345:1250256.
11. Fisch S., Gray S., Heymans S., Haldar S.M., Wang B., Pfister O., et al. Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7074-7079.
12. Xie M., Kong Y., Tan W., May H., Battiprolu P.K., Pedrozo Z., et al. Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation 2014, 129:1139-1151.
13. D, Gatica M, Chiong S, Lavandero DJ, Klionsky. Molecular mechanisms of autophagy in the cardiovascular system. Circ. Res. 116:456-67.
14. D. Mijaljica, M. Prescott, R.J. Devenish, Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy. 7:673-82.
15. Kiffin R., Christian C., Knecht E., Cuervo A.M. Activation of chaperone-mediated autophagy during oxidative stress. Mol. Biol. Cell 2004, 15:4829-4840.
16. Cuervo A.M., Knecht E., Terlecky S.R., Dice J.F. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Phys. 1995, 269:C1200-C1208.
17. Massey A.C., Kaushik S., Sovak G., Kiffin R., Cuervo A.M. Consequences of the selective blockage of chaperone-mediated autophagy. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5805-5810.
18. G. Kroemer, G. Marino, B. Levine, Autophagy and the integrated stress response. Mol. Cell. 40:280-93.
19. Z. Yang, D.J. Klionsky, Eaten alive: a history of macroautophagy. Nat. Cell. Biol. 12:814-22.
20. B. Ravikumar, S. Sarkar, J.E. Davies, M. Futter, M. Garcia-Arencibia, Z.W. Green-Thompson, et al., Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 90:1383-435.
21. D.C. Rubinsztein, P. Codogno, B. Levine, Autophagy modulation as a potential therapeutic target for diverse diseases. Nat. Rev. Drug Discov. 11:709-30.
22. K. Moreau, M. Renna, D.C. Rubinsztein, Connections between SNAREs and autophagy. Trends Biochem Sci. 38:57-63.
23. Y. Zhu, K.M. Pires, K.J. Whitehead, C.D. Olsen, B. Wayment, Y.C. Zhang, et al., Mechanistic target of rapamycin (Mtor) is essential for murine embryonic heart development and growth. PLoS One. 8:e54221.
24. D. Zhang, R. Contu, M.V. Latronico, J. Zhang, R. Rizzi, D. Catalucci, et al., MTORC1 regulates cardiac function and myocyte survival through 4E-BP1 inhibition in mice. J. Clin. Invest. 120:2805-16.
25. M. Sandri, FOXOphagy path to inducing stress resistance and cell survival. Nat. Cell. Biol. 14:786-8.
26. P.K. Battiprolu, B. Hojayev, N. Jiang, Z.V. Wang, X. Luo, M. Iglewski, et al., Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J. Clin. Invest. 122:1109-18.
27. A. Nemchenko, M. Chiong, A. Turer, S. Lavandero, J.A. Hill, Autophagy as a therapeutic target in cardiovascular disease. J. Mol. Cell. Cardiol. 51:584-93.
28. Rothermel B.A., Hill J.A. Autophagy in load-induced heart disease. Circ. Res. 2008, 103:1363-1369.
29. O.F. Rifki, J.A. Hill, ardiac autophagy: good with the bad. J. Cardiovasc. Pharmacol. 60:248-52.
30. M. Chiong, Z.V. Wang, Z. Pedrozo, D.J. Cao, R. Troncoso M. Ibacache et al., Cardiomyocyte death: mechanisms and translational implications. Cell Death Dis. 2:e244.
31. G.G. Schiattarella, J.A. Hill, Inhibition of hypertrophy is a good therapeutic strategy in ventricular pressure overload. Circulation.131:1435-47.
32. 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.
33. 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.
34. 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.
35. Eisenberg-Lerner A., Bialik S., Simon H.U., Kimchi A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 2009, 16:966-975.
36. 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.
37. Levine B., Sinha S., Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008, 4:600-606.
38. Mattson M.P., Kroemer G. Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol. Med. 2003, 9:196-205.
39. Nishida K., Yamaguchi O., Otsu K. Crosstalk between autophagy and apoptosis in heart disease. Circ. Res. 2008, 103:343-351.
40. 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.
41. Kehat I., Accornero F., Aronow B.J., Molkentin J.D. Modulation of chromatin position and gene expression by HDAC4 interaction with nucleoporins. J. Cell Biol. 2011, 193:21-29.
42. Granger A., Abdullah I., Huebner F., Stout A., Wang T., Huebner T., et al. Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J. 2008, 22:3549-3560.
43. Qian J., Ren X., Wang X., Zhang P., Jones W.K., Molkentin J.D., et al. Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. Circ. Res. 2009, 105:1223-1231.
44. Zhang H., Bosch-Marce M., Shimoda L.A., Tan Y.S., Baek J.H., Wesley J.B., et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 2008, 283:10892-10903.
45. 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.
46. Gurusamy N., Lekli I., Gorbunov N.V., Gherghiceanu M., Popescu L.M., Das D.K. Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein. J. Cell. Mol. Med. 2009, 13:373-387.
47. C. Huang, S. Yitzhaki, CN. Perry, W. Liu, Z. Giricz, RM. Mentzer, Jr., et al. Autophagy induced by ischemic preconditioning is essential for cardioprotection. J. Cardiovasc. Transl. Res. 3:365-73.
48. X. Ma, H. Liu, S.R. Foyil, R.J. Godar, C.J. Weinheimer, J.A. Hill, et al., Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation. 125: 3170-81.
49. M. Xie, Y. Kong, W. Tan, H. May, P.K. Battiprolu, Z. Pedrozo, et al., Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation. 129:1139-51.
50. X. Yin, C. Peng, W. Ning, C. Li, Z. Ren, J. Zhang, et al., miR-30a downregulation aggravates pressure overload-induced cardiomyocyte hypertrophy. Mol. Cell. Biochem. 379:1-6.
51. L.Q. Weng, W.B. Zhang, Y. Ye, P.P. Yin, J. Yuan, X.X. Wang, et al., Aliskiren ameliorates pressure overload-induced heart hypertrophy and fibrosis in mice. Acta Pharmacol. Sin. 35:1005-14.
52. G. Marino, F. Pietrocola, T. Eisenberg, Y. Kong, S.A. Malik, S.A. Andryushkova, et al., Regulation of autophagy by cytosolic acetyl-coenzyme A. Mol. Cell. 53:710-25.
53. D.J. Cao, Z.V. Wang, P.K. Battiprolu, N. Jiang, C.R. Morales, Y. Kong, et al., Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc. Natl. Acad. Sci. U. S. A. 108:4123-8.
54. Raben N., Shea L., Hill V., Plotz P. Monitoring autophagy in lysosomal storage disorders. Methods Enzymol. 2009, 453:417-449.
55. N. Raben, C. Schreiner, R. Baum, S. Takikita, S. Xu, T. Xie, et al. Suppression of autophagy permits successful enzyme replacement therapy in a lysosomal storage disorder-murine Pompe disease. Autophagy. 6:1078-89.
56. K.K. Raval, R. Tao, B.E. White, W.J. De Lange, C.H. Koonce, J. Yu, et al., Pompe disease results in a Golgi-based glycosylation deficit in human induced pluripotent stem cell-derived cardiomyocytes. J. Biol. Chem. 290:3121-36.
57. Settembre C., Fraldi A., Jahreiss L., Spampanato C., Venturi C., Medina D., et al. A block of autophagy in lysosomal storage disorders. Hum. Mol. Genet. 2008, 17:119-129.
58. Tessitore A., Pirozzi M., Auricchio A. Abnormal autophagy, ubiquitination, inflammation and apoptosis are dependent upon lysosomal storage and are useful biomarkers of mucopolysaccharidosis VI. PathoGenetics 2009, 2:4.
59. Schiattarella G.G., Cerulo G., De Pasquale V., Cocchiaro P., Paciello O., Avallone L., et al. The murine model of mucopolysaccharidosis IIIB develops cardiopathies over time leading to heart failure. PLoS ONE 2015, 10.
60. R.S. D'Souza, C. Levandowski, D. Slavov, S.L. Graw, L.A. Allen, E. Adler, et al., Danon disease: clinical features, evaluation, and management. Circ. Heart Fail. 7:843-9.
61. Mizushima N., Klionsky D.J. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 2007, 27:19-40.
62. C. Perrino, G.G. Schiattarella, F. Magliulo, F. Ilardi, G. Carotenuto, G. Gargiulo et al., Cardiac side effects of chemotherapy: state of art and strategies for a correct management. Curr. Vasc. Pharmacol. 12:106-16.
63. Singal P.K., Deally C.M., Weinberg L.E. Subcellular effects of adriamycin in the heart: a concise review. J. Mol. Cell. Cardiol. 1987, 19:817-828.
64. Lipshultz S.E., Colan S.D., Gelber R.D., Perez-Atayde A.R., Sallan S.E., Sanders S.P. Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N. Engl. J. Med. 1991, 324:808-815.
65. Octavia Y., Tocchetti C.G., Gabrielson K.L., Janssens S., Crijns H.J., Moens A.L. Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J. Mol. Cell. Cardiol. 2012, 52:1213-1225.
66. Zhang S., Liu X., Bawa-Khalfe T., Lu L.S., Lyu Y.L., Liu L.F., et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med. 2012, 18:1639-1642.
67. Suliman H.B., Carraway M.S., Ali A.S., Reynolds C.M., Welty-Wolf K.E., Piantadosi C.A. The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy. J. Clin. Invest. 2007, 117:3730-3741.
68. Ichikawa Y., Ghanefar M., Bayeva M., Wu R., Khechaduri A., Naga Prasad S.V., et al. Cardiotoxicity of doxorubicin is mediated through mitochondrial iron accumulation. J. Clin. Invest. 2014, 124:617-630.
69. Singal P.K., Iliskovic N. Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 1998, 339:900-905.
70. Kobayashi S., Volden P., Timm D., Mao K., Xu X., Liang Q. Transcription factor GATA4 inhibits doxorubicin-induced autophagy and cardiomyocyte death. J. Biol. Chem. 2010, 285:793-804.
71. Lu L., Wu W., Yan J., Li X., Yu H., Yu X. Adriamycin-induced autophagic cardiomyocyte death plays a pathogenic role in a rat model of heart failure. Int. J. Cardiol. 2009, 134:82-90.
72. Garcia L., Verdejo H.E., Kuzmicic J., Zalaquett R., Gonzalez S., Lavandero S., et al. Impaired cardiac autophagy in patients developing postoperative atrial fibrillation. J. Thorac. Cardiovasc. Surg. 2012, 143:451-459.
73. X. Xu, S. Kobayashi, K. Chen, D. Timm, P. Volden, Y. Huang et al., Diminished autophagy limits cardiac injury in mouse models of type 1 diabetes. J. Biol. Chem. 288:18077-92.
74. 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.
75. S. Sciarretta, P. Zhai, D. Shao, Y. Maejima, J. Robbins, M. Volpe, et al., Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation. 125:1134-46.
76. A. Fierabracci, The putative role of proteolytic pathways in the pathogenesis of Type 1 diabetes mellitus: the 'autophagy' hypothesis. Med. Hypotheses. 82:553-7.
77. 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.
78. Fujitani Y., Ebato C., Uchida T., Kawamori R., Watada H. Beta-cell autophagy: a novel mechanism regulating beta-cell function and mass: lessons from beta-cell-specific Atg7-deficient mice. Islets 2009, 1:151-153.
79. X. Xu, Y. Hua, S. Nair, Y. Zhang, J. Ren, Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J. Mol. Cell. Biol. 5:61-3.
80. 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.
81. Shimomura H., Terasaki F., Hayashi T., Kitaura Y., Isomura T., Suma H. Autophagic degeneration as a possible mechanism of myocardial cell death in dilated cardiomyopathy. Jpn. Circ. J. 2001, 65:965-968.
82. 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.
83. Thoreen C.C., Kang S.A., Chang J.W., Liu Q., Zhang J., Gao Y., et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 2009, 284:8023-8032.
84. B.D. Gogas, M. McDaniel, H. Samady, S.B. King, 3rd. Novel drug-eluting stents for coronary revascularization. Trends Cardiovasc Med. 24:305-13.
85. C. Soderlund, G. Radegran, Immunosuppressive therapies after heart transplantation - the balance between under- and over-immunosuppression. Transplant Rev (Orlando). 29:181-9.
86. Balgi A.D., Fonseca B.D., Donohue E., Tsang T.C., Lajoie P., Proud C.G., et al. Screen for chemical modulators of autophagy reveals novel therapeutic inhibitors of mTORC1 signaling. PLoS ONE 2009, 4.
87. Gillette T.G., Hill J.A. Readers, writers, and erasers: chromatin as the whiteboard of heart disease. Circ. Res. 2015, 116:1245-1253.
88. Antos C.L., McKinsey T.A., Dreitz M., Hollingsworth L.M., Zhang C.L., Schreiber K., et al. Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J. Biol. Chem. 2003, 278:28930-28937.
89. Kong Y., Tannous P., Lu G., Berenji K., Rothermel B.A., Olson E.N., et al. Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation 2006, 113:2579-2588.
90. 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.
91. Sarkar S., Floto R.A., Berger Z., Imarisio S., Cordenier A., Pasco M., et al. Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 2005, 170:1101-1111.
92. Williams A., Sarkar S., Cuddon P., Ttofi E.K., Saiki S., Siddiqi F.H., et al. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat. Chem. Biol. 2008, 4:295-305.
93. Jiang P., Mizushima N. Autophagy and human diseases. Cell Res. 2014, 24:69-79.