Ubiquitin-proteasome system and hereditary cardiomyopathies

Journal of Molecular and Cellular Cardiology

Volumn 71, Issue , 2014, Pages 25-31

  Schlossarek, Saskia ^a,b   Frey, Norbert ^b,c   Carrier, Lucie ^a,b,d,e  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d Sorbonne Université   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Dilated cardiomyopathy; Hypertrophic cardiomyopathy; Ubiquitin proteasome system

Indexed keywords

BORTEZOMIB; EPOXOMICIN; PROTEASOME; SILDENAFIL; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE;

AUTOSOMAL DOMINANT DISORDER; CONGESTIVE CARDIOMYOPATHY; DOSE RESPONSE; DRUG EFFECT; DRUG TOLERABILITY; ENZYME ACTIVITY; ENZYME MECHANISM; GENE MUTATION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRAIT; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN UNFOLDING; REVIEW; SARCOMERE; UBIQUITINATION; ANIMAL; AUTOPHAGY; CARDIOMYOPATHY; GENETICS; HEART; HEART MUSCLE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CARDIOMYOPATHIES; HEART; HUMANS; MYOCARDIUM; PROTEASOME ENDOPEPTIDASE COMPLEX; SARCOMERES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84899927666     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.12.016     Document Type: Review

References (108)

1. Friedrich F.W., Carrier L. Genetics of hypertrophic and dilated cardiomyopathy. Curr Pharm Biotechnol 2012, 13:2467-2476.
2. Watkins H., Ashrafian H., Redwood C. Inherited cardiomyopathies. N Engl J Med 2011, 364:1643-1656.
3. Richardson P., McKenna W., Bristow M., Maisch B., Mautner B., O'Connell J., et al. Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies. Circulation 1996, 93:841-842.
4. Zolk O., Schenke C., Sarikas A. The ubiquitin-proteasome system: focus on the heart. Cardiovasc Res 2006, 70:410-421.
5. Mearini G., Schlossarek S., Willis M.S., Carrier L. The ubiquitin-proteasome system in cardiac dysfunction. Biochim Biophys Acta 2008, 1782:749-763.
6. Lilienbaum A. Relationship between the proteasomal system and autophagy. Int J Biochem Mol Biol 2013, 4:1-26.
7. Metzger M.B., Hristova V.A., Weissman A.M. HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci 2012, 125:531-537.
8. Komander D., Rape M. The ubiquitin code. Annu Rev Biochem 2012, 81:203-229.
9. Schlossarek S., Carrier L. The ubiquitin-proteasome system in cardiomyopathies. Curr Opin Cardiol 2011, 26:190-195.
10. Pagan J., Seto T., Pagano M., Cittadini A. Role of the ubiquitin proteasome system in the heart. Circ Res 2013, 112:1046-1058.
11. Spaich S., Will R.D., Just S., Kuhn C., Frank D., Berger I.M., et al. F-box and leucine-rich repeat protein 22 is a cardiac-enriched F-box protein that regulates sarcomeric protein turnover and is essential for maintenance of contractile function in vivo. Circ Res 2012, 111:1504-1516.
12. Tomko R.J., Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 2013, 82:415-445.
13. Kisselev A.F., van der Linden W.A., Overkleeft H.S. Proteasome inhibitors: an expanding army attacking a unique target. Chem Biol 2012, 19:99-115.
14. Salomons F.A., Acs K., Dantuma N.P. Illuminating the ubiquitin/proteasome system. Exp Cell Res 2010, 316:1289-1295.
15. Lindsten K., Menendez-Benito V., Masucci M.G., Dantuma N.P. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol 2003, 21:897-902.
16. Kumarapeli A.R., Horak K.M., Glasford J.W., Li J., Chen Q., Liu J., et al. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J 2005, 19:2051-2053.
17. Lindsten K., Dantuma N.P. Monitoring the ubiquitin/proteasome system in conformational diseases. Ageing Res Rev 2003, 2:433-449.
18. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
19. Weekes J., Morrison K., Mullen A., Wait R., Barton P., Dunn M.J. Hyperubiquitination of proteins in dilated cardiomyopathy. Proteomics 2003, 3:208-216.
20. 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.
21. Sanbe A., Osinska H., Saffitz J.E., Glabe C.G., Kayed R., Maloyan A., et al. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci U S A 2004, 101:10132-10136.
22. Gianni D., Li A., Tesco G., McKay K.M., Moore J., Raygor K., et al. Protein aggregates and novel presenilin gene variants in idiopathic dilated cardiomyopathy. Circulation 2010, 121:1216-1226.
23. Birks E.J., Latif N., Enesa K., Folkvang T., Luong le A., Sarathchandra P., et al. Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res 2008, 79:472-480.
24. Predmore J.M., Wang P., Davis F., Bartolone S., Westfall M.V., Dyke D.B., et al. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation 2010, 121:997-1004.
25. Baumgarten A., Bang C., Tschirner A., Engelmann A., Adams V., von Haehling S., et al. TWIST1 regulates the activity of ubiquitin proteasome system via the miR-199/214 cluster in human end-stage dilated cardiomyopathy. Int J Cardiol 2013, 168:1447-1452.
26. Elliott P., Andersson B., Arbustini E., Bilinska Z., Cecchi F., Charron P., et al. Classification of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 2008, 29:270-276.
27. Gersh B.J., Maron B.J., Bonow R.O., Dearani J.A., Fifer M.A., Link M.S., et al. 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Thorac Cardiovasc Surg 2011, 142:e153-e203.
28. Frey N., Luedde M., Katus H.A. Mechanisms of disease: hypertrophic cardiomyopathy. Nat Rev Cardiol 2012, 9:91-100.
29. Schlossarek S., Mearini G., Carrier L. Cardiac myosin-binding protein C in hypertrophic cardiomyopathy: mechanisms and therapeutic opportunities. J Mol Cell Cardiol 2011, 50:613-620.
30. Charron P., Carrier L., Dubourg O., Tesson F., Desnos M., Richard P., et al. Penetrance of familial hypertrophic cardiomyopathy. Genet Couns 1997, 8:107-114.
31. Friedrich F.W., Wilding B.R., Reischmann S., Crocini C., Lang P., Charron P., et al. Evidence for FHL1 as a novel disease gene for isolated hypertrophic cardiomyopathy. Hum Mol Genet 2012, 21:3237-3254.
32. Flavigny J., Souchet M., Sebillon P., Berrebi-Bertrand I., Hainque B., Mallet A., et al. COOH-terminal truncated cardiac myosin-binding protein C mutants resulting from familial hypertrophic cardiomyopathy mutations exhibit altered expression and/or incorporation in fetal rat cardiomyocytes. J Mol Biol 1999, 294:443-456.
33. Sarikas A., Carrier L., Schenke C., Doll D., Flavigny J., Lindenberg K.S., et al. Impairment of the ubiquitin-proteasome system by truncated cardiac myosin binding protein C mutants. Cardiovasc Res 2005, 66:33-44.
34. Mearini G., Gedicke C., Schlossarek S., Witt C.C., Kramer E., Cao P., et al. Atrogin-1 and MuRF1 regulate cardiac MyBP-C levels via different mechanisms. Cardiovasc Res 2010, 85:357-366.
35. Bahrudin U., Morisaki H., Morisaki T., Ninomiya H., Higaki K., Nanba E., et al. 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 2008, 384:896-907.
36. Bahrudin U., Morikawa K., Takeuchi A., Kurata Y., Miake J., Mizuta E., et al. Impairment of ubiquitin-proteasome system by E334K cMyBPC modifies channel proteins, leading to electrophysiological dysfunction. J Mol Biol 2011, 413:857-878.
37. Olivotto I., Girolami F., Ackerman M.J., Nistri S., Bos J.M., Zachara E., et al. Myofilament protein gene mutation screening and outcome of patients with hypertrophic cardiomyopathy. Mayo Clin Proc 2008, 83:630-638.
38. Vignier N., Schlossarek S., Fraysse B., Mearini G., Kramer E., Pointu H., et al. Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ Res 2009, 105:239-248.
39. Fraysse B., Weinberger F., Bardswell S.C., Cuello F., Vignier N., Geertz B., et al. Increased myofilament Ca(2+) sensitivity and diastolic dysfunction as early consequences of Mybpc3 mutation in heterozygous knock-in mice. J Mol Cell Cardiol 2012, 52:1299-1307.
40. Carrier L., Knoell R., Vignier N., Keller D.I., Bausero P., Prudhon B., et al. Asymmetric septal hypertrophy in heterozygous cMyBP-C null mice. Cardiovasc Res 2004, 63:293-304.
41. Schlossarek S., Englmann D.R., Sultan K.R., Sauer M., Eschenhagen T., Carrier L. Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res Cardiol 2012, 107:1-13.
42. 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 2012, 33:5-15.
43. Crocini C., Arimura T., Reischmann S., Eder A., Braren I., Hansen A., et al. Impact of ANKRD1 mutations associated with hypertrophic cardiomyopathy on contraction parameters of engineered heart tissue. Basic Res Cardiol 2013, 108:349.
44. Witt C.C., Witt S.H., Lerche S., Labeit D., Back W., Labeit S. Cooperative control of striated muscle mass and metabolism by MuRF1 and MuRF2. EMBO J 2008, 27:350-360.
45. Chen S.N., Czernuszewicz G., Tan Y., Lombardi R., Jin J., Willerson J.T., et al. Human molecular genetic and functional studies identify TRIM63, encoding Muscle RING Finger Protein 1, as a novel gene for human hypertrophic cardiomyopathy. Circ Res 2012, 111:907-919.
46. McNally E.M., Golbus J.R., Puckelwartz M.J. Genetic mutations and mechanisms in dilated cardiomyopathy. J Clin Invest 2013, 123:19-26.
47. Herman D.S., Lam L., Taylor M.R., Wang L., Teekakirikul P., Christodoulou D., et al. Truncations of titin causing dilated cardiomyopathy. N Engl J Med 2012, 366:619-628.
48. Vicart P., Caron A., Guicheney P., Li Z., Prevost M.C., Faure A., et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 1998, 20:92-95.
49. Goldfarb L.G., Dalakas M.C. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest 2009, 119:1806-1813.
50. Wang X., Osinska H., Klevitsky R., Gerdes A.M., Nieman M., Lorenz J., et al. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ Res 2001, 89:84-91.
51. Chen Q., Liu J.B., Horak K.M., Zheng H., Kumarapeli A.R., Li J., et al. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ Res 2005, 97:1018-1026.
52. Wang X., Osinska H., Dorn G.W., Nieman M., Lorenz J.N., Gerdes A.M., et al. Mouse model of desmin-related cardiomyopathy. Circulation 2001, 103:2402-2407.
53. Liu J., Chen Q., Huang W., Horak K.M., Zheng H., Mestril R., et al. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J 2006, 20:362-364.
54. Cattin M.E., Muchir A., Bonne G. 'State-of-the-heart' of cardiac laminopathies. Curr Opin Cardiol 2013, 28:297-304.
55. Cattin M.E., Bertrand A.T., Schlossarek S., Le Bihan M.C., Skov Jensen S., Neuber C., et al. Heterozygous LmnadelK32 mice develop dilated cardiomyopathy through a combined pathomechanism of haploinsufficiency and peptide toxicity. Hum Mol Genet 2013, 22:3152-3164.
56. Costa M.W., Guo G., Wolstein O., Vale M., Castro M.L., Wang L., et al. Functional characterization of a novel mutation in NKX2-5 associated with congenital heart disease and adult-onset cardiomyopathy. Circ Cardiovasc Genet 2013, 6:238-247.
57. Ivandic B.T., Mastitsky S.E., Schonsiegel F., Bekeredjian R., Eils R., Frey N., et al. Whole-genome analysis of gene expression associates the ubiquitin-proteasome system with the cardiomyopathy phenotype in disease-sensitized congenic mouse strains. Cardiovasc Res 2012, 94:87-95.
58. Carrier L., Schlossarek S., Willis M.S., Eschenhagen T. The ubiquitin-proteasome system and nonsense-mediated mRNA decay in hypertrophic cardiomyopathy. Cardiovasc Res 2010, 85:330-338.
59. Marston S., Copeland O., Gehmlich K., Schlossarek S., Carrier L. How do MYBPC3 mutations cause hypertrophic cardiomyopathy?. J Muscle Res Cell Motil 2012, 33:75-80.
60. van Dijk S.J., Dooijes D., Dos Remedios C., Michels M., Lamers J.M., Winegrad S., et al. Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy. Haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation 2009, 119:1473-1483.
61. van Dijk S.J., Paalberends E.R., Najafi A., Michels M., Sadayappan S., Carrier L., et al. Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function. Circ Heart Fail 2012, 5:36-46.
62. Laporte D., Salin B., Daignan-Fornier B., Sagot I. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol 2008, 181:737-745.
63. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000, 10:524-530.
64. 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 2006, 40:451-454.
65. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000, 29:222-230.
66. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001, 83:301-310.
67. Drews O., Tsukamoto O., Liem D., Streicher J., Wang Y., Ping P. Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circ Res 2010, 107:1094-1101.
68. Day S.M., Divald A., Wang P., Davis F., Bartolone S., Jones R., et al. Impaired assembly and post-translational regulation of 26S proteasome in human end-stage heart failure. Circ Heart Fail 2013, 6:544-549.
69. Lu H., Zong C., Wang Y., Young G.W., Deng N., Souda P., et al. Revealing the dynamics of the 20S proteasome phosphoproteome: a combined CID and electron transfer dissociation approach. Mol Cell Proteomics 2008, 7:2073-2089.
70. Asai M., Tsukamoto O., Minamino T., Asanuma H., Fujita M., Asano Y., et al. PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts. J Mol Cell Cardiol 2009, 46:452-462.
71. Lohse M.J., Engelhardt S., Eschenhagen T. What is the role of beta-adrenergic signaling in heart failure?. Circ Res 2003, 93:896-906.
72. Eschenhagen T. Beta-adrenergic signaling in heart failure-adapt or die. Nat Med 2008, 14:485-487.
73. Movsesian M.A., Bristow M.R. Alterations in cAMP-mediated signaling and their role in the pathophysiology of dilated cardiomyopathy. Curr Top Dev Biol 2005, 68:25-48.
74. Sequeira V., Wijnker P.J., Nijenkamp L.L., Kuster D.W., Najafi A., Witjas-Paalberends E.R., et al. Perturbed length-dependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res 2013, 112:1491-1505.
75. El-Armouche A., Pohlmann L., Schlossarek S., Starbatty J., Yeh Y.H., Nattel S., et al. Decreased phosphorylation levels of cardiac myosin-binding protein-C in human and experimental heart failure. J Mol Cell Cardiol 2007, 43:223-229.
76. Kuster D.W., Bawazeer A.C., Zaremba R., Goebel M., Boontje N.M., van der Velden J. Cardiac myosin binding protein C phosphorylation in cardiac disease. J Muscle Res Cell Motil 2012, 33:43-52.
77. Nastasi T., Bongiovanni A., Campos Y., Mann L., Toy J.N., Bostrom J., et al. Ozz-E3, a muscle-specific ubiquitin ligase, regulates beta-catenin degradation during myogenesis. Dev Cell 2004, 6:269-282.
78. Li H.H., Kedar V., Zhang C., McDonough H., Arya R., Wang D.Z., et al. 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.
79. Haupt Y., Maya R., Kazaz A., Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997, 387:296-299.
80. Tang M., Li J., Huang W., Su H., Liang Q., Tian Z., et al. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res 2010, 88:424-433.
81. Groenendyk J., Sreenivasaiah P.K., Kim do H., Agellon L.B., Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ Res 2010, 107:1185-1197.
82. Jager R., Bertrand M.J., Gorman A.M., Vandenabeele P., Samali A. The unfolded protein response at the crossroads of cellular life and death during endoplasmic reticulum stress. Biol Cell 2012, 104:259-270.
83. Fu H.Y., Minamino T., Tsukamoto O., Sawada T., Asai M., Kato H., et al. Overexpression of endoplasmic reticulum-resident chaperone attenuates cardiomyocyte death induced by proteasome inhibition. Cardiovasc Res 2008, 79:600-610.
84. Zheng Q., Wang X. Autophagy and the ubiquitin-proteasome system in cardiac dysfunction. Panminerva Med 2010, 52:9-25.
85. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
86. Ding W.X., Yin X.M. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 2008, 4:141-150.
87. Lamark T., Johansen T. Autophagy: links with the proteasome. Curr Opin Cell Biol 2010, 22:192-198.
88. Zheng Q., Su H., Ranek M.J., Wang X. Autophagy and p62 in cardiac proteinopathy. Circ Res 2011, 109:296-308.
89. Zheng Q., Su H., Tian Z., Wang X. Proteasome malfunction activates macroautophagy in the heart. Am J Cardiovasc Dis 2011, 1:214-226.
90. Depre C., Wang Q., Yan L., Hedhli N., Peter P., Chen L., et al. Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation 2006, 114:1821-1828.
91. Meiners S., Dreger H., Fechner M., Bieler S., Rother W., Gunther C., et al. Suppression of cardiomyocyte hypertrophy by inhibition of the ubiquitin-proteasome system. Hypertension 2008, 51:302-308.
92. Hedhli N., Lizano P., Hong C., Fritzky L.F., Dhar S.K., Liu H., et al. Proteasome inhibition decreases cardiac remodeling after initiation of pressure overload. Am J Physiol Heart Circ Physiol 2008, 295:H1385-H1393.
93. Stansfield W.E., Tang R.H., Moss N.C., Baldwin A.S., Willis M.S., Selzman C.H. Proteasome inhibition promotes regression of left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 2008, 294:H645-H650.
94. Herrmann J., Wohlert C., Saguner A.M., Flores A., Nesbitt L.L., Chade A., et al. Primary proteasome inhibition results in cardiac dysfunction. Eur J Heart Fail 2013, 15:614-623.
95. Enrico O., Gabriele B., Nadia C., Sara G., Daniele V., Giulia C., et al. Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol 2007, 138:396-397.
96. Hacihanefioglu A., Tarkun P., Gonullu E. Acute severe cardiac failure in a myeloma patient due to proteasome inhibitor bortezomib. Int J Hematol 2008, 88:219-222.
97. Bockorny M., Chakravarty S., Schulman P., Bockorny B., Bona R. Severe heart failure after bortezomib treatment in a patient with multiple myeloma: a case report and review of the literature. Acta Haematol 2012, 128:244-247.
98. Richardson P.G., Sonneveld P., Schuster M.W., Irwin D., Stadtmauer E.A., Facon T., et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005, 352:2487-2498.
99. Weissman A.M., Yang Y., Kitagaki J., Sasiela C.A., Beutler J.A., O'Keefe B.R. Inhibiting Hdm2 and ubiquitin-activating enzyme: targeting the ubiquitin conjugating system in cancer. Ernst Schering Found Symp Proc 2008, 171-190.
100. Hauck L., Harms C., An J., Rohne J., Gertz K., Dietz R., et al. Protein kinase CK2 links extracellular growth factor signaling with the control of p27(Kip1) stability in the heart. Nat Med 2008, 14:315-324.
101. Wu L., Grigoryan A.V., Li Y., Hao B., Pagano M., Cardozo T.J. Specific small molecule inhibitors of Skp2-mediated p27 degradation. Chem Biol 2012, 19:1515-1524.
102. Tsukamoto O., Minamino T., Okada K., Shintani Y., Takashima S., Kato H., et al. Depression of proteasome activities during the progression of cardiac dysfunction in pressure-overloaded heart of mice. Biochem Biophys Res Commun 2006, 340:1125-1133.
103. Li J., Horak K.M., 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 2011, 121:3689-3700.
104. Lee B.H., Lee M.J., Park S., Oh D.C., Elsasser S., Chen P.C., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 2010, 467:179-184.
105. Takimoto E., Champion H.C., Li M., Belardi D., Ren S., Rodriguez E.R., et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 2005, 11:214-222.
106. Guazzi M., Vicenzi M., Arena R., Guazzi M.D. PDE5 inhibition with sildenafil improves left ventricular diastolic function, cardiac geometry, and clinical status in patients with stable systolic heart failure: results of a 1-year, prospective, randomized, placebo-controlled study. Circ Heart Fail 2011, 4:8-17.
107. Bishu K., Hamdani N., Mohammed S.F., Kruger M., Ohtani T., Ogut O., et al. Sildenafil and B-type natriuretic peptide acutely phosphorylate titin and improve diastolic distensibility in vivo. Circulation 2011, 124:2882-2891.
108. Ranek M.J., Terpstra E.J., Li J., Kass D.A., Wang X. Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 2013, 128:365-376.