Autophagy in load-induced heart disease

Circulation Research

Volumn 103, Issue 12, 2008, Pages 1363-1369

  Rothermel, Beverly A ^a   Hill, Joseph A ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Autophagy; Cardiac hypertrophy; Heart failure; Hypertrophy; Signal transduction

Indexed keywords

DESMIN;

AUTOPHAGY; CARDIOMYOPATHY; CELL ACTIVITY; HEART DEVELOPMENT; HEART DISEASE; HEART FAILURE; HEART MUSCLE CELL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; REVIEW; ANIMAL; BLOOD PRESSURE; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; BLOOD PRESSURE; HEART DISEASES; HEART FAILURE; HUMANS;

EID: 58149396003     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.186551     Document Type: Review

References (75)

1. Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, Hailpern SM, Ho M, Howard V, Kissela B, Kittner S, Lloyd-Jones D, McDermott M, Meigs J, Moy C, Nichol G, O'Donnell C, Roger V, Sorlie P, Steinberger J, Thom T, Wilson M, Hong Y. Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2008; 117:e25-e146.
2. Levy D, Larson MG, Vasan RS, Kannel WB, Ho KK. The progression from hypertension to congestive heart failure. JAMA. 1996;275: 1557-1562. (Pubitemid 26154241)
3. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation. 2003;107: 984-991.
4. Frey N, Katus HA, Olson EN, Hill JA. Hypertrophy of the heart: a new therapeutic target? Circulation. 2004;109:1580-1589.
5. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med. 2008;358: 1370-1380.
6. Sybers HD, Ingwall J, DeLuca M. Autophagy in cardiac myocytes. Recent Adv Stud Cardiac Struct Metab. 1976;12:453-463.
7. Decker RS, Wildenthal K. Lysosomal alterations in hypoxic and reoxy-genated hearts. 1. Ultrastructural and cytochemical changes. Am J Pathol. 1980;98:425-444.
8. Decker RS, Decker ML, Herring GH, Morton PC, Wildenthal K. Lysosomal vacuolar apparatus of cardiac myocytes in heart of starved and refed rabbits. J Mol Cell Cardiol. 1980;12:1175-1189.
9. Dammrich J, Pfeifer U. Cardiac hypertrophy in rats after supravalvular aortic constriction. II. Inhibition of cellular autophagy in hypertrophying cardiomyocytes. Virchows Arch B Cell Pathol Incl Mol Pathol. 1983;43: 287-307.
10. Pfeifer U, Fohr J, Wilhelm W, Dammrich J. Short-term inhibition of cardiac cellular autophagy by isoproterenol. J Mol Cell Cardiol. 1987; 19:1179-1184. (Pubitemid 18068092)
11. Yamamoto S, Sawada K, Shimomura H, Kawamura K, James TN. On the nature of cell death during remodeling of hypertrophied human myocardium. J Mol Cell Cardiol. 2000;32:161-175.
12. Knaapen MWM, Davies MJ, De Bie M, Haven AJ, Martinet W, Kockx MM. Apoptotic versus autophagic cell death in heart failure. Cardiovasc Res. 2001;51:304-312.
13. 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.
14. Lockshin RA, Zakeri Z. Caspase-independent cell deaths. Curr Opin Cell Biol. 2002;14:727-733.
15. Kostin S, Pool L, Elsasser A, Hein S, Drexler HC, Arnon E, Hayakawa Y, Zimmermann R, Bauer E, Klovekorn WP, Schaper J. Myocytes die by multiple mechanisms in failing human hearts. Circ Res. 2003;92: 715-724.
16. Elsasser A, Vogt AM, Nef H, Kostin S, Mollmann H, Skwara W, Bode C, Hamm C, Schaper J. Human hibernating myocardium is jeopardized by apoptotic and autophagic cell death. J Am Coll Cardiol. 2004;43: 2191-2199.
17. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8:931-937.
18. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21: 2861-2873.
19. Kundu M, Thompson CB. Autophagy: basic principles and relevance to disease. Annu Rev Pathol. 2008;3:427-455.
20. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intra-cellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600.
21. Lorell BH, Carabello BA. Left ventricular hypertrophy-pathogenesis, detection, and prognosis. Circulation. 2000;102:470-479.
22. Dorn GW II, Robbins J, Sugden PH. Phenotyping hypertrophy: eschew obfuscation. Circ Res. 2003;92:1171.
23. Dorn GW II. The fuzzy logic of physiological cardiac hypertrophy. Hypertension. 2007;49:962-970.
24. Rothermel BA, McKinsey TA, Vega RB, Nicol RL, Mammen P, Yang J, Antos CL, Shelton JM, Bassel-Duby R, Olson EN, Williams RS. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2001;98: 3328-3333.
25. Hill JA, Rothermel B, Yoo KD, Cabuay B, Demetroulis E, Weiss RM, Kutschke W, Bassel-Duby R, Williams RS. Targeted inhibition of cal-cineurin in pressure-overload cardiac hypertrophy. Preservation of systolic function. J Biol Chem. 2002;277:10251-10255.
26. Li HH, Kedar V, Zhang C, McDonough H, Arya R, Wang DZ, Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest. 2004;114:1058-1071.
27. Hardt SE, Sadoshima J. Negative regulators of cardiac hypertrophy. Cardiovasc Res. 2004;63:500-509.
28. Olson EN, Backs J, McKinsey TA. Control of cardiac hypertrophy and heart failure by histone acetylation/deacetylation. Novartis Found Symp. 2006;274:3-12.
29. Ni YG, Berenji K, Wang N, Oh M, Sachan N, Dey A, Cheng J, Lu G, Morris DJ, Castrillon DH, Gerard RD, Rothermel BA, Hill JA. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation. 2006;114:1159-1168.
30. Ago T, Sadoshima J. Thioredoxin1 as a negative regulator of cardiac hypertrophy. Antioxid Redox Signal. 2007;9:679-687.
31. Kerkela R, Woulfe K, Force T. Glycogen synthase kinase-3beta-actively inhibiting hypertrophy. Trends Cardiovasc Med. 2007;17:91-96.
32. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem. 2006;281:29776-29787.
33. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. 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.
34. Zhu H, Tannous P, Johnstone JL, Kong Y, Shelton JM, Richardson JA, Le V, Levine B, Rothermel BA, Hill JA. Cardiac autophagy is a mal-adaptive response to hemodynamic stress. J Clin Invest. 2007;117: 1782-1793.
35. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007;13: 619-624.
36. Rothermel BA, Hill JA. Myocyte autophagy in heart disease: friend or foe? Autophagy. 2007;3:632-634.
37. Martinet W, Knaapen MW, Kockx MM, De Meyer GR. Autophagy in cardiovascular disease. Trends Mol Med. 2007;13:482-491.
38. Tannous P, Zhu H, Nemchenko A, Berry JM, Johnstone JL, Shelton JM, Miller FJ Jr, Rothermel BA, Hill JA. Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation. 2008;117: 3070-3078.
39. Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ, Nguyen L, Gerard RD, Levine B, Rothermel BA, Hill JA. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci U S A. 2008;105:9745-9750.
40. Rothermel BA, Hill JA. The heart of autophagy: deconstructing cardiac proteotoxicity. Autophagy. 2008;4:932-935.
41. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463-477.
42. Lum JJ, DeBerardinis RJ, Thompson CB. Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol. 2005;6:439-448.
43. Yuan J, Lipinski M, Degterev A. Diversity in the mechanisms of neuronal cell death. Neuron. 2003;40:401-413.
44. Tsujimoto Y, Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ. 2005;12(suppl 2):1528-1534.
45. Rockman HA, Ross RS, Harris AN, Knowlton KU, Steinhelper ME, Field LJ, Ross J Jr, Chien KR. Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc Natl Acad Sci U S A. 1991;88: 8277-8281.
46. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672-676.
47. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132:27-42.
48. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005;169:425-434.
49. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006; 441:880-884.
50. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegen-erative disease in mice. Nature. 2006;441:885-889.
51. Nishida K, Yamaguchi O, Otsu K. Crosstalk between autophagy and apoptosis in heart disease. Circ Res. 2008;103:343-351.
52. Moreira PI, Santos MS, Moreno A, Oliveira C. Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci Rep. 2001;21:789-800.
53. Kayed R, Sokolov Y, Edmonds B, McIntire TM, Milton SC, Hall JE, Glabe CG. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J Biol Chem. 2004;279:46363-46366.
54. Thundimadathil J, Roeske RW, Jiang HY, Guo L. Aggregation and porin-like channel activity of a beta sheet peptide. Biochemistry. 2005; 44:10259-10270.
55. Taylor JP, Hardy J, Fischbeck KH. Toxic proteins in neurodegenerative disease. Science. 2002;296:1991-1995.
56. Rubinsztein DC, Difiglia M, Heintz N, Nixon RA, Qin ZH, Ravikumar B, Stefanis L, Tolkovsky A. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy. 2005;1:11-22.
57. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000;10:524-530.
58. Ross CA, Poirier MA. Opinion: what is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol. 2005;6:891-898.
59. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, Ravikumar B, Rubinsztein DC. Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol. 2006;76: 89-101.
60. Rubinsztein DC. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature. 2006;443:780-786.
61. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T. The autophagy-related protein beclin 1 shows reduced expression in early, Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest. 2008;118:2190-2199.
62. Heling A, Zimmermann R, Kostin S, Maeno Y, Hein S, Devaux B, Bauer E, Klovekorn WP, Schlepper M, Schaper W, Schaper J. Increased expression of cytoskeletal, linkage, and extracellular proteins in failing human myocardium. Circ Res. 2000;86:846-853.
63. Weekes J, Morrison K, Mullen A, Wait R, Barton P, Dunn MJ. Hyperu-biquitination of proteins in dilated cardiomyopathy. Proteomics. 2003;3: 208-216.
64. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, Chateau D, Chapon F, Tome F, Dupret JM, Paulin D, Fardeau M. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet. 1998;20:92-95.
65. Wang X, Osinska H, Klevitsky R, Gerdes AM, Nieman M, Lorenz J, Hewett T, Robbins J. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ Res. 2001;89:84-91.
66. Omary MB, Coulombe PA, McLean WH. Intermediate filament proteins and their associated diseases. N Engl J Med. 2004;351:2087-2100.
67. Rajasekaran NS, Connell P, Christians ES, Yan LJ, Taylor RP, Orosz A, Zhang XQ, Stevenson TJ, Peshock RM, Leopold JA, Barry WH, Loscalzo J, Odelberg SJ, Benjamin IJ. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell. 2007;130:427-439.
68. Wang X, Osinska H, Dorn GW II, Nieman M, Lorenz JN, Gerdes AM, Witt S, Kimball T, Gulick J, Robbins J. Mouse model of desmin-related cardiomyopathy. Circulation. 2001;103:2402-2407.
69. Sanbe A, Osinska H, Saffitz JE, Glabe CG, Kayed R, Maloyan A, Robbins J. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci U S A. 2004;101:10132-10136.
70. Maloyan A, Sanbe A, Osinska H, Westfall M, Robinson D, Imahashi K, Murphy E, Robbins J. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in alpha-B-crystallin desmin-related cardiomyop-athy. Circulation. 2005;112:3451-3461.
71. Chen Q, Liu JB, Horak KM, Zheng H, Kumarapeli AR, Li J, Li F, Gerdes AM, Wawrousek EF, Wang X. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ Res. 2005;97:1018-1026.
72. Johnston JA, Ward CL, Kopito RR. Aggresomes: a cellular response to misfolded proteins. J Cell Biol. 1998;143:1883-1898.
73. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature. 2004;431:805-810.
74. Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys. 2007;462:245-253.
75. Yu L, Strandberg L, Lenardo MJ. The selectivity of autophagy and its role in cell death and survival. Autophagy. 2008;4:567-573.