The COP9 signalosome is required for autophagy, proteasome-mediated proteolysis, and cardiomyocyte survival in adult mice

Circulation: Heart Failure

Volumn 6, Issue 5, 2013, Pages 1049-1057

  Su, Huabo ^a,b   Li, Jie ^a,b,f   Osinska, Hanna ^c   Li, Faqian ^d   Robbins, Jeffrey ^c   Liu, Jinbao ^a   Wei, Ning ^e   Wang, Xuejun ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c HEART INSTITUTE   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e YALE UNIVERSITY   (United States)

^f GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; COP9 signalosome; Heart; NEDD8; Proteasome endopeptidase complex

Indexed keywords

COP9 SIGNALOSOME; PROTEASOME; UBIQUITINATED PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; HEART MUSCLE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION;

AUTOPHAGY; COP9 SIGNALOSOME; HEART; NEDD8; PROTEASOME ENDOPEPTIDASE COMPLEX;

ANIMALS; AUTOPHAGY; CARDIOMYOPATHY, DILATED; CARRIER PROTEINS; CELL DEATH; CULLIN PROTEINS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; MYOCYTES, CARDIAC; NECROSIS; OXIDATION-REDUCTION; PEPTIDE HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SIGNAL TRANSDUCTION; UBIQUITINS;

EID: 84887423435     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000338     Document Type: Article

References (41)

1. Schlossarek S, Carrier L. The ubiquitin-proteasome system in cardiomyopathies. Curr Opin Cardiol. 2011;26:190-195.
2. Gustafsson AB, Gottlieb RA. Recycle or die: the role of autophagy in cardioprotection. J Mol Cell Cardiol. 2008;44:654-661.
3. Wang X, Pattison JS, Su H. Posttranslational modification and quality control. Circ Res. 2013;112:367-381.
4. 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.
5. Wang X, Li J, Zheng H, Su H, Powell SR. Proteasome functional insufficiency in cardiac pathogenesis. Am J Physiol Heart Circ Physiol. 2011;301:H2207-H2219.
6. Day SM. The ubiquitin proteasome system in human cardiomyopathies and heart failure. Am J Physiol Heart Circ Physiol. 2013;304:H1283-H1293.
7. Xie M, Morales CR, Lavandero S, Hill JA. Tuning flux: autophagy as a target of heart disease therapy. Curr Opin Cardiol. 2011;26:216-222.
8. Zheng Q, Su H, Ranek MJ, Wang X. Autophagy and p62 in cardiac proteinopathy. Circ Res. 2011;109:296-308.
9. 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. 2011;121:3689-3700.
10. Tian Z, Zheng H, Li J, Li Y, Su H, Wang X. Genetically induced moderate inhibition of the proteasome in cardiomyocytes exacerbates myocardial ischemia-reperfusion injury in mice. Circ Res. 2012;111:532-542.
11. Sciarretta S, Zhai P, Shao D, Maejima Y, Robbins J, Volpe M, Condorelli G, Sadoshima J. Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation. 2012;125:1134-1146.
12. Wei N, Deng XW. COP9: a new genetic locus involved in light-regulated development and gene expression in arabidopsis. Plant Cell. 1992;4:1507-1518.
13. Wei N, Deng XW. The COP9 signalosome. Annu Rev Cell Dev Biol. 2003;19:261-286.
14. Kawakami T, Chiba T, Suzuki T, Iwai K, Yamanaka K, Minato N, Suzuki H, Shimbara N, Hidaka Y, Osaka F, Omata M, Tanaka K. NEDD8 recruits E2-ubiquitin to SCF E3 ligase. EMBO J. 2001;20:4003-4012.
15. Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, Zhou C, Wolf DA, Wei N, Shevchenko A, Deshaies RJ. Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science. 2001;292:1382-1385.
16. Kato JY, Yoneda-Kato N. Mammalian COP9 signalosome. Genes Cells. 2009;14:1209-1225.
17. Menon S, Chi H, Zhang H, Deng XW, Flavell RA, Wei N. COP9 signalosome subunit 8 is essential for peripheral T cell homeostasis and antigen receptor-induced entry into the cell cycle from quiescence. Nat Immunol. 2007;8:1236-1245.
18. Su H, Li J, Menon S, Liu J, Kumarapeli AR, Wei N, Wang X. 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;108:40-50.
19. Li F, Wang X, Capasso JM, Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol. 1996;28:1737-1746.
20. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S, Brownell JE, Burke KE, Cardin DP, Critchley S, Cullis CA, Doucette A, Garnsey JJ, Gaulin JL, Gershman RE, Lublinsky AR, McDonald A, Mizutani H, Narayanan U, Olhava EJ, Peluso S, Rezaei M, Sintchak MD, Talreja T, Thomas MP, Traore T, Vyskocil S, Weatherhead GS, Yu J, Zhang J, Dick LR, Claiborne CF, Rolfe M, Bolen JB, Langston SP. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature. 2009;458:732-736.
21. Lee YH, Judge AD, Seo D, Kitade M, Gómez-Quiroz LE, Ishikawa T, Andersen JB, Kim BK, Marquardt JU, Raggi C, Avital I, Conner EA, MacLachlan I, Factor VM, Thorgeirsson SS. Molecular targeting of CSN5 in human hepatocellular carcinoma: a mechanism of therapeutic response. Oncogene. 2011;30:4175-4184.
22. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD. Temporally regulated and tissuespecific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res. 2001;89:20-25.
23. Kumarapeli AR, Horak KM, Glasford JW, Li J, Chen Q, Liu J, Zheng H, Wang X. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J. 2005;19:2051-2053.
24. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15:1101-1111.
25. Wang X, Osinska H, Dorn GW 2nd, 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.
26. Kumarapeli AR, Su H, Huang W, Tang M, Zheng H, Horak KM, Li M, Wang X. Alpha B-crystallin suppresses pressure overload cardiac hypertrophy. Circ Res. 2008;103:1473-1482.
27. Watson IR, Irwin MS, Ohh M. NEDD8 pathways in cancer, Sine Quibus Non. Cancer Cell. 2011;19:168-176.
28. Zheng Q, Wang X. Autophagy and the ubiquitin-proteasome system in cardiac dysfunction. Panminerva Med. 2010;52:9-25.
29. Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell. 2009;33:517-527.
30. Kung G, Konstantinidis K, Kitsis RN. Programmed necrosis, not apoptosis, in the heart. Circ Res. 2011;108:1017-1036.
31. Su H, Li F, Ranek MJ, Wei N, Wang X. COP9 signalosome regulates autophagosome maturation. Circulation. 2011;124:2117-2128.
32. Lei D, Li F, Su H, Tian Z, Ye B, Wei N, Wang X. COP9 signalosome subunit 8 is required for postnatal hepatocyte survival and effective proliferation. Cell Death Differ. 2011;18:259-270.
33. Xirodimas DP. Novel substrates and functions for the ubiquitin-like molecule NEDD8. Biochem Soc Trans. 2008;36(Pt 5):802-806.
34. Wei N, Serino G, Deng XW. The COP9 signalosome: more than a protease. Trends Biochem Sci. 2008;33:592-600.
35. Li L, Deng XW. The COP9 signalosome: an alternative lid for the 26S proteasome? Trends Cell Biol. 2003;13:507-509.
36. Fernandez-Sanchez ME, Sechet E, Margottin-Goguet F, Rogge L, Bianchi E. The human COP9 signalosome protects ubiquitin-conjugating enzyme 3 (UBC3/Cdc34) from beta-transducin repeat-containing protein (betaTrCP)-mediated degradation. J Biol Chem. 2010;285:17390-17397.
37. Wang X, Terpstra EJ. Ubiquitin receptors and protein quality control. J Mol Cell Cardiol. 2013;55:73-84.
38. Nahlik K, Dumkow M, Bayram O, Helmstaedt K, Busch S, Valerius O, Gerke J, Hoppert M, Schwier E, Opitz L, Westermann M, Grond S, Feussner K, Goebel C, Kaever A, Meinicke P, Feussner I, Braus GH. The COP9 signalosome mediates transcriptional and metabolic response to hormones, oxidative stress protection and cell wall rearrangement during fungal development. Mol Microbiol. 2010;78:964-979.
39. 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.
40. Kostin S, Pool L, Elsässer A, Hein S, Drexler HC, Arnon E, Hayakawa Y, Zimmermann R, Bauer E, Klövekorn WP, Schaper J. Myocytes die by multiple mechanisms in failing human hearts. Circ Res. 2003;92:715-724.
41. Miyata S, Takemura G, Kawase Y, Li Y, Okada H, Maruyama R, Ushikoshi H, Esaki M, Kanamori H, Li L, Misao Y, Tezuka A, Toyo-Oka T, Minatoguchi S, Fujiwara T, Fujiwara H. Autophagic cardiomyocyte death in cardiomyopathic hamsters and its prevention by granulocyte colony-stimulating factor. Am J Pathol. 2006;168:386-397.