Cardiovascular autophagy: Crossroads of pathology, pharmacology and toxicology

Cardiovascular Toxicology

Volumn 13, Issue 3, 2013, Pages 220-229

  Salabei, Joshua K ^a   Conklin, Daniel J ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Autophagy; Cardiovascular disease; Drug eluting stents; LC3; Rapamycin; Verapamil

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; BAFILOMYCIN A1; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; BORTEZOMIB; CARBAMAZEPINE; CARDIOVASCULAR AGENT; CELL PROTEIN; CHLORAMPHENICOL HEMISUCCINATE; CHLOROQUINE; DOXORUBICIN; GRANULOCYTE COLONY STIMULATING FACTOR; IMATINIB; ISOPRENALINE; LITHIUM; METFORMIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3 II PROTEIN; NORADRENALIN; PACLITAXEL; PROPRANOLOL; RAPAMYCIN; SALBUTAMOL; SPAUTIN 1; SULFAPHENAZOLE; TAMOXIFEN; UNCLASSIFIED DRUG; UROCORTIN; VALPROIC ACID; VERAPAMIL; WORTMANNIN;

ABDOMINAL AORTA ANEURYSM; ANGINA PECTORIS; ANTIDIABETIC ACTIVITY; ANTIHYPERTENSIVE ACTIVITY; ANTIMALARIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTERY MEDIA; ASTHMA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPHAGOSOME; AUTOPHAGY; BLOOD VESSEL TONE; BLOOD VESSEL WALL; BRADYCARDIA; BREAST CANCER; CARDIOMYOCYTE DEGENERATION; CARDIOTOXICITY; CARDIOVASCULAR AUTOPHAGY; CELL DEGENERATION; CELL FUNCTION; CEREBROVASCULAR ACCIDENT; CONGESTIVE CARDIOMYOPATHY; DEVICE THERAPY; DIABETIC CARDIOMYOPATHY; DISEASE COURSE; DRUG EFFICACY; DRUG ELUTING STENT; DRUG INDICATION; DRUG INDUCED DISEASE; DRUG TARGETING; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; KAPOSI SARCOMA; LEFT VENTRICULAR ASSIST DEVICE; LUNG CANCER; MANTLE CELL LYMPHOMA; MITRAL VALVE REGURGITATION; MOOD DISORDER; MULTIPLE MYELOMA; MYELOMA; NEOINTIMA; NEOPLASM; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OVARY CANCER; OVARY POLYCYSTIC DISEASE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REPERFUSION INJURY; RESTENOSIS; REVIEW; SEIZURE; SMOOTH MUSCLE FIBER; TRANSLUMINAL CORONARY ANGIOPLASTY; TRICUSPID VALVE REGURGITATION; UNSPECIFIED SIDE EFFECT; UPREGULATION; VASA VASORUM; VASCULAR RESISTANCE; VASCULAR SMOOTH MUSCLE;

MAMMALIA;

ANIMALS; AUTOPHAGY; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; HUMANS; MYOCARDIUM;

EID: 84884281384     PISSN: 15307905     EISSN: 15590259     Source Type: Journal    
DOI: 10.1007/s12012-013-9200-8     Document Type: Review

References (90)

1. Roger, (2011). Heart disease and stroke statistics-2011 Update: A report from the American Heart Association (vol 123, pg e18, 2011). Circulation, 123(6), E240-E240.
2. Mizushima, N., et al. (1998). A protein conjugation system essential for autophagy. Nature, 395(6700), 395-398.
3. Tanida, I., et al. (1999). Apg7p/Cvt2p: A novel protein-activating enzyme essential for autophagy. Molecular Biology of the Cell, 10(5), 1367-1379.
4. Tanida, I., et al. (2004). HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3- and GABAA receptor-associated protein-phospholipid conjugates. Journal of Biological Chemistry, 279(35), 36268-36276.
5. Tanida, I., et al. (2002). Human Apg3p/Aut1p homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP-LC3, and facilitates the conjugation of hApg12p to hApg5p. Journal of Biological Chemistry, 277(16), 13739-13744.
6. Mehrpour, M., et al. (2010). Autophagy in health and disease. 1. Regulation and significance of autophagy: an overview. American Journal of Physiology-Cell Physiology, 298(4), C776-C785.
7. Morselli, E., et al. (2010). Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Disease, 1, e10.
8. Madeo, F., Tavernarakis, N., & Kroemer, G. (2010). Can autophagy promote longevity? Nature Cell Biology, 12(9), 842-846.
9. Hansen, M., et al. (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. Plos Genetics, 4(2).
10. Stromhaug, P. E., & Klionsky, D. J. (2001). Approaching the molecular mechanism of autophagy. Traffic, 2(8), 524-531.
11. Wang, C. W., & Klionsky, D. J. (2003). The molecular mechanism of autophagy. Molecular Medicine, 9(3-4), 65-76.
12. Yang, Z. F., & Klionsky, D. J. (2009). An overview of the molecular mechanism of autophagy. Autophagy in Infection and Immunity, 335, 1-32.
13. He, C. C., & Klionsky, D. J. (2009). Regulation mechanisms and signaling pathways of autophagy. Annual Review of Genetics, 43, 67-93.
14. Longatti, A., & Tooze, S. A. (2009). Vesicular trafficking and autophagosome formation. Cell Death and Differentiation, 16(7), 956-965.
15. Nakatogawa, H., et al. (2009). Dynamics and diversity in autophagy mechanisms: Lessons from yeast. Nature Reviews Molecular Cell Biology, 10(7), 458-467.
16. Nakai, A., et al. (2007). The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nature Medicine, 13(5), 619-624.
17. Qipshidze, N., et al. (2012). Autophagy mechanism of right ventricular remodeling in murine model of pulmonary artery constriction. American Journal of Physiology-Heart and Circulatory Physiology, 302(3), H688-H696.
18. Hua, Y. N., et al. (2011). Chronic akt activation accentuates aging-induced cardiac hypertrophy and myocardial contractile dysfunction: Role of autophagy. Basic Research in Cardiology, 106(6), 1173-1191.
19. Yamamoto, S., et al. (2000). On the nature of cell death during remodeling of hypertrophied human myocardium. Journal of Molecular and Cellular Cardiology, 32(1), 161-175.
20. McMullen, J. R., et al. (2004). Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation, 109(24), 3050-3055.
21. Shioi, T., et al. (2003). Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation, 107(12), 1664-1670.
22. Garcia, L., et al. (2012). Impaired cardiac autophagy in patients developing postoperative atrial fibrillation. Journal of Thoracic and Cardiovascular Surgery, 143(2), 451-474.
23. Chen, M. C., et al. (2011). Autophagy as a mechanism for myolysis of cardiomyocytes in mitral regurgitation. European Journal of Clinical Investigation, 41(3), 299-307.
24. Sybers, H. D., Ingwall, J., & DeLuca, M. (1976). Autophagy in cardiac myocytes. Recent Advances in Studies on Cardiac Structure and Metabolism, 12, 453-463.
25. Matsui, Y., et al. (2007). Distinct roles of autophagy in the heart during ischemia and reperfusion: Roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circulation Research, 100(6), 914-922.
26. Valentim, L., et al. (2006). Urocortin inhibits Beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury. Journal of Molecular and Cellular Cardiology, 40(6), 846-852.
27. Hamacher-Brady, A., Brady, N. R., & Gottlieb, R. A. (2006). Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. Journal of Biological Chemistry, 281(40), 29776-29787.
28. Khan, S., et al. (2006). Rapamycin confers preconditioning-like protection against ischemia-reperfusion injury in isolated mouse heart and cardiomyocytes. Journal of Molecular and Cellular Cardiology, 41(2), 256-264.
29. Sala-Mercado, J. A., et al. (2010). Profound cardioprotection with chloramphenicol succinate in the swine model of myocardial ischemia-reperfusion injury. Circulation, 122(11 Suppl), S179-S184.
30. Shimomura, H., et al. (2001). Autophagic degeneration as a possible mechanism of myocardial cell death in dilated cardiomyopathy. Japanese Circulation Journal-English Edition, 65(11), 965-968.
31. Kostin, S., et al. (2003). Myocytes die by multiple mechanisms in failing human hearts. Circulation Research, 92(7), 715-724.
32. Biederbick, A., Kern, H. F., & Elsasser, H. P. (1995). Monodansylcadaverine (Mdc) Is a specific in-vivo marker for autophagic vacuoles. European Journal of Cell Biology, 66(1), 3-14.
33. Kassiotis, C., et al. (2009). Markers of autophagy are downregulated in failing human heart after mechanical unloading. Circulation, 120(11), S191-S197.
34. Weissberg, P. L., & Bennett, M. R. (1999). Atherosclerosis - an inflammatory disease. New England Journal of Medicine, 340(24), 1928-1929.
35. Liao, X. H., et al. (2012). Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metabolism, 15(4), 545-553.
36. Razani, B., et al. (2012). Autophagy links inflammasomes to atherosclerotic progression. Cell Metabolism, 15(4), 534-544.
37. Jia, G. H., Cheng, G., & Agrawal, D. K. (2007). Autophagy of vascular smooth muscle cells in atherosclerotic lesions. Autophagy, 3(1), 63-64.
38. Liao, X., et al. (2012). Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metabolism, 15(4), 545-553.
39. Debnath, J., Baehrecke, E. H., & Kroemer, G. (2005). Does autophagy contribute to cell death? Autophagy, 1(2), 66-74.
40. Newby, A. C., & Zaltsman, A. B. (2000). Molecular mechanisms in intimal hyperplasia. Journal of Pathology, 190(3), 300-309.
41. Billinger, M., et al. (2012) Long-term clinical and angiographic outcomes of diabetic patients after revascularization with early generation drug-eluting stents. American Heart Journal, 163(5), p. 876- +.
42. Grube, E., & Buellesfeld, L. (2004). Rapamycin analogs for stent-based local drug delivery - Everolimus- and tacrolimus-eluting stents. Herz, 29(2), 162-166.
43. Zheng, Y. H., et al. (2012). Osteopontin stimulates autophagy via integrin/cd44 and p38 mapk signaling pathways in vascular smooth muscle cells. Journal of Cellular Physiology, 227(1), 127-135.
44. Georgiev, B., et al. (2004). Use of calcium channel blockers in hypertension treatment in primary care. Journal of Hypertension, 22, S198-s222.
45. Pepine, C. J., et al. (2003). A calcium antagonist vs a non-calcium antagonist hypertension treatment strategy for patients with coronary artery disease - the international verapamil-trandolapril study (invest): A randomized controlled trial. Jama-Journal of the American Medical Association, 290(21), 2805-2816.
46. Elliott, W. J., & Ram, C. V. S. (2011). Calcium channel blockers. Journal of Clinical Hypertension, 13(9), 687-689.
47. Stams, T. R. G., et al. (2012). Verapamil as an antiarrhythmic agent in congestive heart failure: Hopping from rabbit to human? British Journal of Pharmacology, 166(2), 554-556.
48. Salabei, J.K., et al. (2012) Verapamil stereoisomers induce antiproliferative effects in vascular smooth muscle cells via autophagy. Toxicol Appl Pharmacol, 262(3), 265-272.
49. Bahro, M., & Pfeifer, U. (1987). Short-term stimulation by propranolol and verapamil of cardiac cellular autophagy. Journal of Molecular and Cellular Cardiology, 19(12), 1169-1178.
50. Sheiban, I., et al. (2002). Drug-eluting stent: The emerging technique for the prevention of restenosis. Minerva Cardioangiologica, 50(5), 443-453.
51. Hayashi, S., et al. (2009). The stent-eluting drugs sirolimus and paclitaxel suppress healing of the endothelium by induction of autophagy. American Journal of Pathology, 175(5), 2226-2234.
52. Buss, S. J., et al. (2009). Beneficial effects of Mammalian target of rapamycin inhibition on left ventricular remodeling after myocardial infarction. Journal of the American College of Cardiology, 54(25), 2435-2446.
53. Aranguiz-Urroz, P., et al. (2011). Beta(2)-adrenergic receptor regulates cardiac fibroblast autophagy and collagen degradation. Biochimica Et Biophysica Acta-Molecular Basis of Disease, 1812(1), 23-31.
54. Pfeifer, U., et al. (1987). Short-term inhibition of cardiac cellular autophagy by isoproterenol. Journal of Molecular and Cellular Cardiology, 19(12), 1179-1184.
55. Dammrich, J., & Pfeifer, U. (1981). Acute effects of isoproterenol on cellular autophagy - inhibition in myocardium but stimulation in liver parenchyma. Virchows Archiv B-Cell Pathology Including Molecular Pathology, 38(2), 209-218.
56. Xie, Z. L., et al. (2011). Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 Mice. Diabetes, 60(6), 1770-1778.
57. Sasaki, H., et al. (2008). Activation of myocardial AMP-activated protein kinase by metformin prevents progression of heart failure in dogs Involvement of eNOS Activation. Circulation, 118(18), S286-S287.
58. Sasaki, H., et al. (2009). Metformin prevents progression of heart failure in dogs role of amp-activated protein kinase. Circulation, 119(19), 2568-2574.
59. Burgert, T. S., et al. (2007). Short-term metabolic and cardiovascular effects of metformin in markedly obese adolescents with normal glucose tolerance. Diabetes, 56, A471-A471.
60. Evia-Viscarra, M. L., et al. (2012). The effects of metformin on inflammatory mediators in obese adolescents with insulin resistance: Controlled randomized clinical trial. Journal of Pediatric Endocrinology and Metabolism, 25(1-2), 41-49.
61. Fitch, K., et al. (2012). Effects of lifestyle modification and metformin on atherosclerotic indices among HIV-infected patients with the metabolic syndrome. Aids, 26(5), 587-597.
62. Adams, J., & Kauffman, M. (2004). Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Investigation, 22(2), 304-311.
63. Hu, W., et al. (2012). Mechanistic investigation of imatinib-induced cardiac toxicity and the involvement of c-Abl kinase. Toxicological Sciences, 129(1), 188-199.
64. Nowis, D., et al. (2010). Cardiotoxicity of the anticancer therapeutic agent bortezomib. American Journal of Pathology, 176(6), 2658-2668.
65. Liu, J. L., et al. (2011). Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell, 147(1), 223-234.
66. Yamamoto, A., et al. (1998). Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Structure and Function, 23(1), 33-42.
67. Solomon, V. R., & Lee, H. (2009). Chloroquine and its analogs: A new promise of an old drug for effective and safe cancer therapies. European Journal of Pharmacology, 625(1-3), 220-233.
68. Nave, B. T., et al. (1999). Mammalian target of rapamycin is a direct target for protein kinase B: Identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochemical Journal, 344, 427-431.
69. Jung, C. H., et al. (2010). mTOR regulation of autophagy. FEBS Letters, 584(7), 1287-1295.
70. Kim, J., et al. (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nature Cell Biology, 13(2), 132-222.
71. Egan, D. F., et al. (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science, 331(6016), 456-461.
72. Gwinn, D. M., et al. (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Molecular Cell, 30(2), 214-226.
73. Stephan, J. S., & Herman, P. K. (2006). The regulation of autophagy in eukaryotic cells: Do all roads pass through Atg1? Autophagy, 2(2), 146-148.
74. He, H., et al. (2003). Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. Journal of Biological Chemistry, 278(31), 29278-29287.
75. Kabeya, Y., et al. (2003). LC3, a mammalian homolog of yeast Apg8p, is localized in autophagosome membranes after processing (vol 19, pg 5720, 2000). EMBO Journal, 22(17), 4577-4622.
76. Schlossarek, S., et al. (2012) Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Research in Cardiology, 107(1).
77. Nemchenko, A., et al. (2011). Autophagy as a therapeutic target in cardiovascular disease. Journal of Molecular and Cellular Cardiology, 51(4), 584-593.
78. Yamamoto, S., et al. (2000). On the nature of cell death during remodeling of hypertrophied human myocardium. Journal of Molecular and Cellular Cardiology, 32(1), 161-175.
79. McMullen, J. R., et al. (2004). Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation, 109(24), 3050-3055.
80. Gao, X. M., et al. (2006). Inhibition of mTOR reduces chronic pressure-overload cardiac hypertrophy and fibrosis. Journal of Hypertension, 24(8), 1663-1670.
81. Matsui, Y., et al. (2007). Distinct roles of autophagy in the heart during ischemia and reperfusion -Roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circulation Research, 100(6), 914-922.
82. Valentim, L., et al. (2006). Urocortin inhibits Beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury. Journal of Molecular and Cellular Cardiology, 40(6), 846-852.
83. Hamacher-Brady, A., Brady, N. R., & Gottlieb, R. A. (2006). Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. Journal of Biological Chemistry, 281(40), 29776-29787.
84. Martinet, W., et al. (2008). Interactions between cell death induced by statins and 7-ketocholesterol in rabbit aorta smooth muscle cells. British Journal of Pharmacology, 154(6), 1236-1246.
85. Curcio, A., Torella, D., & Indolfi, C. (2011). Mechanisms of smooth muscle cell proliferation and endothelial regeneration after vascular injury and stenting-approach to therapy. Circulation Journal, 75(6), 1287-1296.
86. Burgert, T. S., et al. (2008). Short-term metabolic and cardiovascular effects of metformin in markedly obese adolescents with normal glucose tolerance. Pediatric Diabetes, 9(6), 567-576.
87. Takemura, G., et al. (2006). Autophagic degeneration and death of cardiomyocytes in heart failure. Autophagy, 2(3), 212-214.
88. Miyata, S., et al. (2006). Autophagic cardiomyocyte death in cardiomyopathic hamsters and its prevention by granulocyte colony-stimulating factor. American Journal of Pathology, 168(2), 386-397.
89. Huang, C., et al. (2010). Autophagy and protein kinase C are required for cardioprotection by sulfaphenazole. American Journal of Physiology. Heart and Circulatory Physiology, 298(2), H570-H579.
90. Ross, T. K., et al. (2000). Differential effects of chloroquine on cardiolipin biosynthesis in hepatocytes and H9c2 cardiac cells. Molecular and Cellular Biochemistry, 207(1-2), 115-122.