Enhancement of proteasomal function protects against cardiac proteinopathy and ischemia/reperfusion injury in mice

Journal of Clinical Investigation

Volumn 121, Issue 9, 2011, Pages 3689-3700

  Li, Jie ^a   Horak, Kathleen M ^a   Su, Huabo ^a   Sanbe, Atsushi ^b   Robbins, Jeffrey ^b   Wang, Xuejun ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOMYOCYTE RESTRICTED OVEREXPRESSION OF PROTEASOME 28 SUBUNIT ALPHA; DESMIN; MUTANT PROTEIN; PROTEASOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREEDING; CARDIAC PROTEINOPATHY; CONTROLLED STUDY; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; ENZYME DEFICIENCY; ENZYME DEGRADATION; GENE OVEREXPRESSION; GENE SILENCING; HEART CELL CULTURE; HEART DISEASE; HEART FUNCTION; HEART HYPERTROPHY; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HOMEOSTASIS; LIFESPAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEASOME FUNCTIONAL INSUFFICIENCY; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; REPERFUSION INJURY; TRANSGENIC MOUSE; UPREGULATION;

ALPHA-CRYSTALLIN B CHAIN; ANIMALS; CARDIOMYOPATHIES; FEMALE; HEART; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MICE; MICE, TRANSGENIC; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; RNA, SMALL INTERFERING;

EID: 80052386730     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45709     Document Type: Article

References (48)

1. Wang X., Robbins J. Heart failure and protein quality control. Circ Res. 2006;99(12):1315-1328. (Pubitemid 44949667)
2. Scruggs S.B., Ping P., Zong C. Heterogeneous cardiac proteasomes: Mandated by diverse substrates? Physiology (Bethesda). 2011;26(2):106-114.
3. Willis M.S., Townley-Tilson W.H., Kang E.Y., Homeister J.W., Patterson C. Sent to destroy: The ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res. 2010;106(3):463-478.
4. Su H., Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: A quality control perspective. Cardiovasc Res. 2010;85(2):253-262.
5. Goldfarb L.G., Dalakas M.C. Tragedy in a heartbeat: Malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest. 2009;119(7):1806- 1813.
6. Tannous P., et al. Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation. 2008;117(24):3070-3078.
7. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 2001;292(5521):1552-1555. (Pubitemid 32493425)
8. Sanbe A., et al. Desmin-related cardiomyopathy in transgenic mice: A cardiac amyloidosis. Proc Natl Acad Sci U S A. 2004;101(27):10132-10136. (Pubitemid 38891207)
9. Gianni D., et al. Protein aggregates and novel presenilin gene variants in idiopathic dilated cardiomyopathy. Circulation. 2010;121(10):1216-1226.
10. Kumarapeli A.R., et al. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. Faseb J. 2005;19(14):2051-2053. (Pubitemid 41759762)
11. Gilon T., Chomsky O., Kulka R.G. Degradation signals recognized by the Ubc6p-Ubc7p ubiquitinconjugating enzyme pair. Mol Cell Biol. 2000; 20(19):7214-7219.
12. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol. 2008;9(9):679-690.
13. Liu J., et al. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. Faseb J. 2006;20(2):362-364. (Pubitemid 46671172)
14. Chen Q., et al. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ Res. 2005;97(10):1018-1028.
15. Wang X., et al. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ Res. 2001;89(1):84-91. (Pubitemid 34135496)
16. Wang X., et al. Mouse model of desmin-related cardiomyopathy. Circulation. 2001;103(19):2402-2407. (Pubitemid 32448807)
17. Liu J., Tang M., Mestril R., Wang X. Aberrant protein aggregation is essential for a mutant desmin to impair the proteolytic function of the ubiquitinproteasome system in cardiomyocytes. J Mol Cell Cardiol. 2006;40(4):451-454.
18. Bahrudin U., et al. Ubiquitin-proteasome system impairment caused by a missense cardiac myosinbinding protein C mutation and associated with cardiac dysfunction in hypertrophic cardiomyopathy. J Mol Biol. 2008;384(4):896-907.
19. Mearini G., Schlossarek S., Willis M.S., Carrier L. The ubiquitin-proteasome system in cardiac dysfunction. Biochim Biophys Acta. 2008;1782(12):749-763.
20. Divald A., et al. Myocardial ischemic preconditioning preserves postischemic function of the 26S proteasome through diminished oxidative damage to 19S regulatory particle subunits. Circ Res. 2010; 106(12):1829-1838.
21. Bulteau A.L., et al. Oxidative modification and inactivation of the proteasome during coronary occlusion/ reperfusion. J Biol Chem. 2001;276(32):30057-30063.
22. Predmore J.M., et al. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation. 2010;121(8):997-1004.
23. Li J., Powell S.R., Wang X. Enhancement of proteasome function by PA28a overexpression protects against oxidative stress. FASEB J. 2011;25(3):883-893.
24. Lee B.H., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature. 2010;467(7312):179-184.
25. Cascio P., Call M., Petre B.M., Walz T., Goldberg A.L. Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. Embo J. 2002;21(11):2636-2645. (Pubitemid 34619379)
26. Realini C., et al. Characterization of recombinant REGalpha, REGbeta, and REGgamma proteasome activators. J Biol Chem. 1997;272(41):25483-25492. (Pubitemid 27438854)
27. Zhang Z., Krutchinsky A., Endicott S., Realini C., Rechsteiner M., Standing KG. Proteasome activator REG or PA28: Recombinant REG alpha/REG beta hetero-oligomers are heptamers. Biochemistry. 1999;38(17):5651-5658.
28. Kloetzel P.M. Generation of major histocompatibility complex class I antigens: Functional interplay between proteasomes and TPPII. Nat Immunol. 2004;5(7):661-669. (Pubitemid 39023294)
29. Preckel T., et al. Impaired immunoproteasome assembly and immune responses in PA28-/- mice. Science. 1999;286(5447):2162-2165. (Pubitemid 129516292)
30. Chen X., Barton L.F., Chi Y., Clurman B.E., Roberts J.M. Ubiquitin-independent degradation of cellcycle inhibitors by the REGgamma proteasome. Mol Cell. 2007;26(6):843-852. (Pubitemid 46921008)
31. Sanbe A., Gulick J., Hanks M.C., Liang Q., Osinska H., Robbins J. Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ Res. 2003;92(6):609-616. (Pubitemid 36417694)
32. 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(9):1094-1101.
33. Zheng H., et al. Doxycycline attenuates protein aggregation in cardiomyocytes and improves survival of a mouse model of cardiac proteinopathy. J Am Coll Cardiol. 2010;56(17):1418-1426.
34. Takagi H., et al. Activation of PKN mediates survival of cardiac myocytes in the heart during ischemia/ reperfusion. Circ Res. 2010;107(5):642-649.
35. Turer A.T., Hill J.A. Pathogenesis of myocardial ischemia- reperfusion injury and rationale for therapy. Am J Cardiol. 2010;106(3):360-368.
36. Bova M.P., et al. Mutation R120G in alphaB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone- like function. Proc Natl Acad Sci U S A. 1999; 96(11):6137-6142. (Pubitemid 29256632)
37. Maloyan A., et al. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in alpha-B-crystallin desmin-related cardiomyopathy. Circulation. 2005;112(22):3451-3461. (Pubitemid 43739561)
38. Rajasekaran N.S., et al. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell. 2007; 130(3):427-439. (Pubitemid 47208522)
39. Tang M., et al. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res. 2010; 88(3):424-433.
40. Su H., et al. Perturbation of cullin deneddylation via conditional Csn8 ablation impairs the ubiquitin- proteasome system and causes cardiomyocyte necrosis and dilated cardiomyopathy in mice. Circ Res. 2011;108(1):40-50.
41. Tanahashi N., Murakami Y., Minami Y., Shimbara N., Hendil K.B., Tanaka K. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J Biol Chem. 2000; 275(19):14336-14345. (Pubitemid 30339716)
42. Stohwasser R., Salzmann U., Giesebrecht J., Kloetzel P.M., Holzhutter H.G. Kinetic evidences for facilitation of peptide channelling by the proteasome activator PA28. Eur J Biochem. 2000;267(20):6221-6230.
43. Murata S., et al. Immunoproteasome assembly and antigen presentation in mice lacking both PA28alpha and PA28beta. Embo J. 2001; 20(21):5898-5907. (Pubitemid 33049265)
44. Chen J., Liu X. The role of interferon gamma in regulation of CD4+ T-cells and its clinical implications. Cell Immunol. 2009;254(2):85-90.
45. Seifert U., et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell. 2010;142(4):613-624.
46. Kobayashi S., et al. Diminished GATA4 protein levels contribute to hyperglycemia-induced cardiomyocyte injury. J Biol Chem. 2007;282(30):21945- 21952. (Pubitemid 47195736)
47. Zheng Q., Su H., Ranek M.J., Wang X. Autophagy and p62 in cardiac proteinopathy [published online ahead of print June 9, 2011]. Circ Res. 2011; 109(3):296-308.
48. Bohl S., Medway D.J., Schulz-Menger J., Schneider J.E., Neubauer S., Lygate C.A. Refined approach for quantification of in vivo ischemia-reperfusion injury in the mouse heart. Am J Physiol Heart Circ Physiol. 2009;297(6):H2054- H2058.