The ubiquitin proteasome system in human cardiomyopathies and heart failure

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 10, 2013, Pages

  Day, Sharlene M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cardiomyopathies; Heart failure; Human studies; Protein quality control; Ubiquitin proteasome system

Indexed keywords

BORTEZOMIB; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN;

AUTOPHAGY; BRADYCARDIA; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CLINICAL FEATURE; CONGESTIVE CARDIOMYOPATHY; HEART ATRIUM FIBRILLATION; HEART DISEASE; HEART FAILURE; HEART LEFT VENTRICLE FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MEDICAL RESEARCH; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN QUALITY; QUALITY CONTROL; REVIEW; UBIQUITIN PROTEASOME SYSTEM; UBIQUITINATION;

CARDIOMYOPATHIES; HEART FAILURE; HUMAN STUDIES; PROTEIN QUALITY CONTROL; UBIQUITIN PROTEASOME SYSTEM;

ANIMALS; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; HEART FAILURE; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84878340024     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00249.2012     Document Type: Review

References (106)

1. Ahmad F, Seidman JG, Seidman CE. The genetic basis for cardiac remodeling. Annu Rev Genomics Hum Genet 6: 185-216, 2005.
2. Attaix D, Ventadour S, Codran A, Bechet D, Taillandier D, Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 41: 173-186, 2005.
3. Baar K, Nader G, Bodine S. Resistance exercise, muscle loading/ unloading and the control of muscle mass. Essays Biochem 42: 61-74, 2006.
4. Bahrudin U, Morikawa K, Takeuchi A, Kurata Y, Miake J, Mizuta E, Adachi K, Higaki K, Yamamoto Y, Shirayoshi Y, Yoshida A, Kato M, Yamamoto K, Nanba E, Morisaki H, Morisaki T, Matsuoka S, Ninomiya H, Hisatome I. Impairment of ubiquitin-proteasome system by E334K cMyBPC modifies channel proteins, leading to electrophysiological dysfunction. J Mol Biol 413: 857-878, 2011.
5. Bahrudin U, Morisaki H, Morisaki T, Ninomiya H, Higaki K, Nanba E, Igawa O, Takashima S, Mizuta E, Miake J, Yamamoto Y, Shirayoshi Y, Kitakaze M, Carrier L, Hisatome I. Ubiquitin-proteasome system impairment caused by a missense cardiac myosin-binding protein C mutation and associated with cardiac dysfunction in hypertrophic cardiomyopathy. J Mol Biol 384: 896-907, 2008.
6. Bedford L, Lowe J, Dick LR, Mayer RJ, Brownell JE. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Discov 10: 29-46, 2011.
7. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitinproteasome system by protein aggregation. Science 292: 1552-1555, 2001.
8. Bennett EJ, Bence NF, Jayakumar R, Kopito RR. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell 17: 351-365, 2005.
9. Birks EJ, Latif N, Enesa K, Folkvang T, Luong le A, Sarathchandra P, Khan M, Ovaa H, Terracciano CM, Barton PJ, Yacoub MH, Evans PC. Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res 79: 472-480, 2008.
10. Bose S, Stratford FL, Broadfoot KI, Mason GG, Rivett AJ. Phosphorylation of 20S proteasome alpha subunit C8 (alpha7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by gamma-interferon. Biochem J 378: 177-184, 2004.
11. Bulteau AL, Lundberg KC, Humphries KM, Sadek HA, Szweda PA, Friguet B, Szweda LI. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem 276: 30057-30063, 2001.
12. Carrier L, Schlossarek S, Willis MS, Eschenhagen T. The ubiquitinproteasome system and nonsense-mediated mRNA decay in hypertrophic cardiomyopathy. Cardiovasc Res 85: 330-338, 2010.
13. Carson P, Anand I, O'Connor C, Jaski B, Steinberg J, Lwin A, Lindenfeld J, Ghali J, Barnet JH, Feldman AM, Bristow MR. Mode of death in advanced heart failure: the Comparison of Medical, Pacing, and Defibrillation Therapies in Heart Failure (COMPANION) trial. J Am Coll Cardiol 46: 2329-2334, 2005.
14. 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 97: 1018-1026, 2005.
15. Chiu C, Tebo M, Ingles J, Yeates L, Arthur JW, Lind JM, Semsarian C. Genetic screening of calcium regulation genes in familial hypertrophic cardiomyopathy. J Mol Cell Cardiol 43: 337-343, 2007.
16. Davies KJ. Degradation of oxidized proteins by the 20S proteasome. Biochimie 83: 301-310, 2001.
17. Day SM, Divald A, Wang P, Davis F, Bartolone S, Jones R, Powell SR. Impaired assembly and post-translational regulation of 26S proteasome in human end stage heart failure. Circ Heat Fail. doi:10.1161/ CIRCHEARTFAILURE.112.000119.
18. Dearani JA, Ommen SR, Gersh BJ, Schaff HV, Danielson GK. Surgery insight: Septal myectomy for obstructive hypertrophic cardiomyopathy-the Mayo Clinic experience. Nat Clin Pract Cardiovasc Med 4: 503-512, 2007.
19. Depre C, Wang Q, Yan L, Hedhli N, Peter P, Chen L, Hong C, Hittinger L, Ghaleh B, Sadoshima J, Vatner DE, Vatner SF, Madura K. Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation 114: 1821-1828, 2006.
20. Dolloff NG, Talamo G. Targeted therapy of multiple myeloma. Adv Exp Med Biol 779: 197-221, 2013.
21. Drews O, Tsukamoto O, Liem D, Streicher J, Wang Y, Ping P. Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circ Res 107: 1094-1101, 2010.
22. Drews O, Wildgruber R, Zong C, Sukop U, Nissum M, Weber G, Gomes AV, Ping P. Mammalian proteasome subpopulations with distinct molecular compositions and proteolytic activities. Mol Cell Proteomics 6: 2021-2031, 2007.
23. Enrico O, Gabriele B, Nadia C, Sara G, Daniele V, Giulia C, Antonio S, Mario P. Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol 138: 396-397, 2007.
24. Feldman AM, de Lissovoy G, Bristow MR, Saxon LA, De Marco T, Kass DA, Boehmer J, Singh S, Whellan DJ, Carson P, Boscoe A, Baker TM, Gunderman MR. Cost effectiveness of cardiac resynchronization therapy in the Comparison of Medical Therapy, Pacing, and Defibrillation in Heart Failure (COMPANION) trial. J Am Coll Cardiol 46: 2311-2321, 2005.
25. Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 309: 71-82, 2013.
26. Galasso G, De Rosa R, Piscione F, Iaccarino G, Vosa C, Sorriento D, Piccolo R, Rapacciuolo A, Walsh K, Chiariello M. Myocardial expression of FOXO3a-Atrogin-1 pathway in human heart failure. Eur J Heart Fail 12: 1290-1296, 2010.
27. Gersh BJ, Maron BJ, Bonow RO, Dearani JA, Fifer MA, Link MS, Naidu SS, Nishimura RA, Ommen SR, Rakowski H, Seidman CE, Towbin JA, Udelson JE, Yancy CW. 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy: executive summary: a report of the American College of Cardiology Foundation/ American Heart Association Task Force on Practice Guidelines. Circulation 124: 2761-2796, 2011.
28. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN. Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. J Biol Chem 283: 31813-31822, 2008.
29. Gomes AV, Zong C, Edmondson RD, Li X, Stefani E, Zhang J, Jones RC, Thyparambil S, Wang GW, Qiao X, Bardag-Gorce F, Ping P. Mapping the murine cardiac 26S proteasome complexes. Circ Res 99: 362-371, 2006.
30. 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 107: 984-991, 2003.
31. Herrmann J, Ciechanover A, Lerman LO, Lerman A. The ubiquitinproteasome system in cardiovascular diseases-a hypothesis extended. Cardiovasc Res 61: 11-21, 2004.
32. Herrmann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res 100: 1276-1291, 2007.
33. Hipp AA, Heitkamp HC, Rocker K, Dickhuth HH. Hypertrophic cardiomyopathy-sports-related aspects of diagnosis, therapy, and sports eligibility. Int J Sports Med 25: 20-26, 2004.
34. Ho CY. Hypertrophic cardiomyopathy in 2012. Circulation 125: 1432-1438, 2012.
35. Jefferies JL, Towbin JA. Dilated cardiomyopathy. Lancet 375: 752-762, 2010.
36. Jessup M, Abraham WT, Casey DE, Feldman AM, Francis GS, Ganiats TG, Konstam MA, Mancini DM, Rahko PS, Silver MA, Stevenson LW, Yancy CW. 2009 focused update: ACCF/AHA Guidelines for the Diagnosis and Management of Heart Failure in Adults: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines: developed in collaboration with the International Society for Heart and Lung Transplantation. Circulation 119: 1977-2016, 2009.
37. Kassiotis C, Ballal K, Wellnitz K, Vela D, Gong M, Salazar R, Frazier OH, Taegtmeyer H. Markers of autophagy are downregulated in failing human heart after mechanical unloading. Circulation 120, suppl 11: S191-S197, 2009.
38. Kendall GC, Mokhonova EI, Moran M, Sejbuk NE, Wang DW, Silva O, Wang RT, Martinez L, Lu QL, Damoiseaux R, Spencer MJ, Nelson SF, Miceli MC. Dantrolene enhances antisense-mediated exon skipping in human and mouse models of duchenne muscular dystrophy. Sci Transl Med 4: 164ra160, 2012.
39. 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 92: 715-724, 2003.
40. Kriegenburg F, Ellgaard L, Hartmann-Petersen R. Molecular chaperones in targeting misfolded proteins for ubiquitin-dependent degradation. FEBS J 279: 532-542, 2012.
41. Lamark T, Johansen T. Autophagy: links with the proteasome. Curr Opin Cell Biol 22: 192-198, 2010.
42. Li J, Horak KM, 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 121: 3689-3700, 2011.
43. Li J, Powell SR, Wang X. Enhancement of proteasome function by PA28β overexpression protects against oxidative stress. FASEB J 25: 883-893, 2011.
44. Liu J, Chen Q, Huang W, Horak KM, Zheng H, Mestril R, Wang X. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J 20: 362-364, 2006.
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 40: 451-454, 2006.
46. Lu H, Zong C, Wang Y, Young GW, Deng N, Souda P, Li X, Whitelegge J, Drews O, Yang PY, Ping P. Revealing the dynamics of 20S proteasome phosphoproteome: a combined CID and ETD approach. Mol Cell Proteomics 7: 2073-2089, 2008.
47. Maloyan A, Gulick J, Glabe CG, Kayed R, Robbins J. Exercise reverses preamyloid oligomer and prolongs survival in alphaB-crystallinbased desmin-related cardiomyopathy. Proc Natl Acad Sci USA 104: 5995-6000, 2007.
48. Maron BJ. Hypertrophic cardiomyopathy and other causes of sudden cardiac death in young competitive athletes, with considerations for preparticipation screening and criteria for disqualification. Cardiol Clin 25: 399-414, vi, 2007.
49. Maron BJ. Hypertrophic cardiomyopathy: a systematic review. JAMA 287: 1308-1320, 2002.
50. Maron BJ, Ackerman MJ, Nishimura RA, Pyeritz RE, Towbin JA, Udelson JE. Task Force 4: HCM and other cardiomyopathies, mitral valve prolapse, myocarditis, and Marfan syndrome. J Am Coll Cardiol 45: 1340-1345, 2005.
51. Maron BJ, Chaitman BR, Ackerman MJ, Bayes de Luna A, Corrado D, Crosson JE, Deal BJ, Driscoll DJ, Estes NA 3rd, Araujo CG, Liang DH, Mitten MJ, Myerburg RJ, Pelliccia A, Thompson PD, Towbin JA, Van Camp SP. Recommendations for physical activity and recreational sports participation for young patients with genetic cardiovascular diseases. Circulation 109: 2807-2816, 2004.
52. Maron MS, Olivotto I, Zenovich AG, Link MS, Pandian NG, Kuvin JT, Nistri S, Cecchi F, Udelson JE, Maron BJ. Hypertrophic cardiomyopathy is predominantly a disease of left ventricular outflow tract obstruction. Circulation 114: 2232-2239, 2006.
53. Mearini G, Gedicke C, Schlossarek S, Witt CC, Kramer E, Cao P, Gomes MD, Lecker SH, Labeit S, Willis MS, Eschenhagen T, Carrier L. Atrogin-1 and MuRF1 regulate cardiac MyBP-C levels via different mechanisms. Cardiovasc Res 85: 357-366, 2010.
54. Mearini G, Schlossarek S, Willis MS, Carrier L. The ubiquitinproteasome system in cardiac dysfunction. Biochim Biophys Acta 1782: 749-763, 2008.
55. Meiners S, Dreger H, Fechner M, Bieler S, Rother W, Gunther C, Baumann G, Stangl V, Stangl K. Suppression of cardiomyocyte hypertrophy by inhibition of the ubiquitin-proteasome system. Hypertension 51: 302-308, 2008.
56. Morrow AG, Brockenbrough EC. Surgical treatment of idiopathic hypertrophic subaortic stenosis: technic and hemodynamic results of subaortic ventriculomyotomy. Ann Surg 154: 181-189, 1961.
57. Movsesian MA, Bristow MR. Alterations in cAMP-mediated signaling and their role in the pathophysiology of dilated cardiomyopathy. Curr Top Dev Biol 68: 25-48, 2005.
58. Nishimura RA, Holmes DR Jr. Clinical practice. Hypertrophic obstructive cardiomyopathy. N Engl J Med 350: 1320-1327, 2004.
59. Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107: 4907-4916, 2006.
60. Ommen SR, Maron BJ, Olivotto I, Maron MS, Cecchi F, Betocchi S, Gersh BJ, Ackerman MJ, McCully RB, Dearani JA, Schaff HV, Danielson GK, Tajik AJ, Nishimura RA. Long-term effects of surgical septal myectomy on survival in patients with obstructive hypertrophic cardiomyopathy. J Am Coll Cardiol 46: 470-476, 2005.
61. Otsuka K, Terasaki F, Shimomura H, Tsukada B, Horii T, Isomura T, Suma H, Shibayama Y, Kitaura Y. Enhanced expression of the ubiquitin-proteasome system in the myocardium from patients with dilated cardiomyopathy referred for left ventriculoplasty: an immunohistochemical study with special reference to oxidative stress. Heart Vessels 25: 474-484, 2010.
62. Patel MB, Majetschak M. Distribution and interrelationship of ubiquitin proteasome pathway component activities and ubiquitin pools in various porcine tissues. Physiol Res 56: 341-350, 2007.
63. Patterson C, Ike C, Willis PWt Stouffer GA, Willis MS. The bitter end: the ubiquitin-proteasome system and cardiac dysfunction. Circulation 115: 1456-1463, 2007.
64. Pattison JS, Sanbe A, Maloyan A, Osinska H, Klevitsky R, Robbins J. Cardiomyocyte expression of a polyglutamine preamyloid oligomer causes heart failure. Circulation 117: 2743-2751, 2008.
65. Pelliccia A, Fagard R, Bjornstad HH, Anastassakis A, Arbustini E, Assanelli D, Biffi A, Borjesson M, Carre F, Corrado D, Delise P, Dorwarth U, Hirth A, Heidbuchel H, Hoffmann E, Mellwig KP, Panhuyzen-Goedkoop N, Pisani A, Solberg EE, van-Buuren F, Vanhees L, Blomstrom-Lundqvist C, Deligiannis A, Dugmore D, Glikson M, Hoff PI, Hoffmann A, Hoffmann E, Horstkotte D, Nordrehaug JE, Oudhof J, McKenna WJ, Penco M, Priori S, Reybrouck T, Senden J, Spataro A, Thiene G. Recommendations for competitive sports participation in athletes with cardiovascular disease: a consensus document from the Study Group of Sports Cardiology of the Working Group of Cardiac Rehabilitation and Exercise Physiology and the Working Group of Myocardial and Pericardial Diseases of the European Society of Cardiology. Eur Heart J 26: 1422-1445, 2005.
66. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J 432: 585-594, 2010.
67. Powell SR. The ubiquitin-proteasome system in cardiac physiology and pathology. Am J Physiol Heart Circ Physiol 291: H1-H19, 2006.
68. Powell SR, Divald A. The ubiquitin-proteasome system in myocardial ischaemia and preconditioning. Cardiovasc Res 85: 303-311, 2010.
69. Powell SR, Gurzenda EM, Wahezi SE. Actin is oxidized during myocardial ischemia. Free Radic Biol Med 30: 1171-1176, 2001.
70. Powell SR, Samuel SM, Wang P, Divald A, Thirunavukkarasu M, Koneru S, Wang X, Maulik N. Upregulation of myocardial 11Sactivated proteasome in experimental hyperglycemia. J Mol Cell Cardiol 44: 618-621, 2008.
71. Powell SR, Wang P, Katzeff H, Shringarpure R, Teoh C, Khaliulin I, Das DK, Davies KJ, Schwalb H. Oxidized and ubiquitinated proteins may predict recovery of postischemic cardiac function: essential role of the proteasome. Antioxid Redox Signal 7: 538-546, 2005.
72. Predmore JM, Wang P, Davis F, Bartolone S, Westfall MV, Dyke DB, Pagani F, Powell SR, Day SM. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation 121: 997-1004, 2010.
73. Razeghi P, Baskin KK, Sharma S, Young ME, Stepkowski S, Essop MF, Taegtmeyer H. Atrophy, hypertrophy, and hypoxemia induce transcriptional regulators of the ubiquitin proteasome system in the rat heart. Biochem Biophys Res Commun 342: 361-364, 2006.
74. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 107: 2227-2232, 2003.
75. Rivera DA, Bristow MR. Cardiac resynchronization-a heart failure perspective. Ann Noninvasive Electrocardiol 10: 16-23, 2005.
76. Ruggeri B, Miknyoczki S, Dorsey B, Hui AM. The development and pharmacology of proteasome inhibitors for the management and treatment of cancer. Adv Pharmacol 57: 91-135, 2009.
77. 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 USA 101: 10132-10136, 2004.
78. Sarikas A, Carrier L, Schenke C, Doll D, Flavigny J, Lindenberg KS, Eschenhagen T, Zolk O. Impairment of the ubiquitin-proteasome system by truncated cardiac myosin binding protein C mutants. Cardiovasc Res 66: 33-44, 2005.
79. Schlossarek S, Carrier L. The ubiquitin-proteasome system in cardiomyopathies. Curr Opin Cardiol 26: 190-195, 2011.
80. Schlossarek S, Englmann DR, Sultan KR, Sauer M, Eschenhagen T, Carrier L. Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res Cardiol 107: 1-13, 2012.
81. Schlossarek S, Schuermann F, Geertz B, Mearini G, Eschenhagen T, Carrier L. Adrenergic stress reveals septal hypertrophy and proteasome impairment in heterozygous Mybpc3-targeted knock-in mice. J Muscle Res Cell Motil 33: 5-15, 2012.
82. Shringarpure R, Grune T, Mehlhase J, Davies KJ. Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem 278: 311-318, 2003.
83. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol Cell 27: 731-744, 2007.
84. Stansfield WE, Tang RH, Moss NC, Baldwin AS, Willis MS, Selzman CH. Proteasome inhibition promotes regression of left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 294: H645-H650, 2008.
85. Su H, Wang X. p62 Stages an interplay between the ubiquitin-proteasome system and autophagy in the heart of defense against proteotoxic stress. Trends Cardiovasc Med 21: 224-228, 2011.
86. Su H, Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 85: 253-262, 2010.
87. Tanahashi N, Murakami Y, Minami Y, Shimbara N, Hendil KB, Tanaka Hybrid proteasomes K. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J Biol Chem 275: 14336-14345, 2000.
88. Tang M, Li J, Huang W, Su H, Liang Q, Tian Z, Horak KM, Molkentin JD, Wang X. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res 88: 424-433, 2010.
89. Tsukamoto O, Minamino T, Okada K, Shintani Y, Takashima S, Kato H, Liao Y, Okazaki H, Asai M, Hirata A, Fujita M, Asano Y, Yamazaki S, Asanuma H, Hori M, Kitakaze M. Depression of proteasome activities during the progression of cardiac dysfunction in pressure-overloaded heart of mice. Biochem Biophys Res Commun 340: 1125-1133, 2006.
90. Vignier N, Schlossarek S, Fraysse B, Mearini G, Kramer E, Pointu H, Mougenot N, Guiard J, Reimer R, Hohenberg H, Schwartz K, Vernet M, Eschenhagen T, Carrier L. Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ Res 105: 239-248, 2009.
91. Wang D, Zong C, Koag MC, Wang Y, Drews O, Fang C, Scruggs SB, Ping P. Proteome dynamics and proteome function of cardiac 19S proteasomes. Mol Cell Proteomics 10: M110.006122, 2011.
92. Wang X, Li J, Zheng H, Su H, Powell SR. Proteasome functional insufficiency in cardiac pathogenesis. Am J Physiol Heart Circ Physiol 301: H2207-H2219, 2011.
93. Wang X, Pattison JS, Su H. Posttranslational modification and quality control. Circ Res 112: 367-381, 2013.
94. Wang X, Robbins J. Heart failure and protein quality control. Circ Res 99: 1315-1328, 2006.
95. Wang X, Su H, Ranek MJ. Protein quality control and degradation in cardiomyocytes. J Mol Cell Cardiol 45: 11-27, 2008.
96. Watkins H, Ashrafian H, Redwood C. Inherited cardiomyopathies. N Engl J Med 364: 1643-1656, 2011.
97. Weekes J, Morrison K, Mullen A, Wait R, Barton P, Dunn MJ. Hyperubiquitination of proteins in dilated cardiomyopathy. Proteomics 3: 208-216, 2003.
98. Willis MS, Ike C, Li L, Wang DZ, Glass DJ, Patterson C. Muscle ring finger 1, but not muscle ring finger 2, regulates cardiac hypertrophy in vivo. Circ Res 100: 456-459, 2007.
99. Willis MS, Rojas M, Li L, Selzman CH, Tang RH, Stansfield WE, Rodriguez JE, Glass DJ, Patterson C. Muscle ring finger 1 mediates cardiac atrophy in vivo. Am J Physiol Heart Circ Physiol 296: H997-H1006, 2009.
100. Willis MS, Schisler JC, Portbury AL, Patterson C. Build it up-Tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 81: 439-448, 2009.
101. Willis MS, Townley-Tilson WH, Kang EY, Homeister JW, Patterson C. Sent to destroy: the ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res 106: 463-478, 2010.
102. Wohlschlaeger J, Sixt SU, Stoeppler T, Schmitz KJ, Levkau B, Tsagakis K, Vahlhaus C, Schmid C, Peters J, Schmid KW, Milting H, Baba HA. Ventricular unloading is associated with increased 20s proteasome protein expression in the myocardium. J Heart Lung Transplant 29: 125-132, 2010.
103. Xu Y, Lu L, Greyson C, Rizeq M, Nunley K, Wyatt B, Bristow MR, Long CS, Schwartz GG. The PPAR-β activator fenofibrate fails to provide myocardial protection in ischemia and reperfusion in pigs. Am J Physiol Heart Circ Physiol 290: H1798-H1807, 2006.
104. Yu X, Kem DC. Proteasome inhibition during myocardial infarction. Cardiovasc Res 85: 312-320, 2010.
105. Zheng Q, Su H, Tian Z, Wang X. Proteasome malfunction activates macroautophagy in the heart. Am J Cardiovasc Dis 1: 214-226, 2011.
106. Zong C, Gomes AV, Drews O, Li X, Young GW, Berhane B, Qiao X, French SW, Bardag-Gorce F, Ping P. Regulation of murine cardiac 20S proteasomes: role of associating partners. Circ Res 99: 372-380, 2006.