Induction of SENP1 in myocardium contributes to abnormities of mitochondria and cardiomyopathy

Journal of Molecular and Cellular Cardiology

Volumn 79, Issue , 2015, Pages 115-122

  Cai, Rong ^a   Gu, Jianmin ^b   Sun, Haipeng ^a   Liu, Xiaobing ^c   Mei, Wenhan ^a   Qi, Yitao ^d,e   Xue, Song ^b   Ren, Shuxun ^f   Rabinowitz, Joseph E ^g   Wang, Yibin ^f   Yeh, Edward T H ^d,e   Cheng, Jinke ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^d TEXAS HEART INSTITUTE   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium calcineurin NFAT3; Cardiac hypertrophy; MEF 2C; Mitochondria; PGC 1 ; Sentrin SUMO specific protease 1 (SENP1)

Indexed keywords

ADENOVIRUS VECTOR; CALCINEURIN; MESSENGER RNA; MYOCYTE ENHANCER FACTOR 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SMALL INTERFERING RNA; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR NFAT3; TRANSCRIPTION FACTOR NRF1; MEF2C PROTEIN, MOUSE; PPARGC1A PROTEIN, MOUSE; PROTEINASE; SENP1 PROTEIN, HUMAN; SENP1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFAT;

ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; BINDING SITE; BIOGENESIS; CARDIOMYOPATHY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ECHOCARDIOGRAPHY; ENERGY METABOLISM; GENE EXPRESSION; HEART DISEASE; HEART EJECTION FRACTION; HEART FAILURE; HEART MUSCLE; HUMAN; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SUMOYLATION; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CALCINEURIN; CARDIOMYOPATHIES; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; HEART FAILURE; HUMANS; MEF2 TRANSCRIPTION FACTORS; MICE; MITOCHONDRIA; MYOCARDIUM; NFATC TRANSCRIPTION FACTORS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84912051215     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.11.014     Document Type: Article

References (45)

1. Jessup M., Brozena S. Heart failure. N Engl J Med 2003, 348:2007-2018.
2. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 2007, 356:1140-1151.
3. Galluzzi L., Kepp O., Trojel-Hansen C., Kroemer G. Mitochondrial control of cellular life, stress, and death. Circ Res 2012, 111:1198-1207.
4. Huss J.M., Kelly D.P. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Investig 2005, 115:547-555.
5. Bayeva M., Gheorghiade M., Ardehali H. Mitochondria as a therapeutic target in heart failure. J Am Coll Cardiol 2012, 61:599-610.
6. Murray A.J., Edwards L.M., Clarke K. Mitochondria and heart failure. Curr Opin Clin Nutr Metab Care 2007, 10:704-711.
7. Tuunanen H., Knuuti J. Metabolic remodelling in human heart failure. Cardiovasc Res 2011, 90:251-257.
8. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 2006, 116:615-622.
9. Russell L.K., Mansfield C.M., Lehman J.J., Kovacs A., Courtois M., Saffitz J.E., et al. Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res 2004, 94:525-533.
10. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
11. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005, 1:361-370.
12. Riehle C., Abel E.D. PGC-1 proteins and heart failure. Trends Cardiovasc Med 2012, 22:98-105.
13. Arany Z., He H., Lin J., Hoyer K., Handschin C., Toka O., et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab 2005, 1:259-271.
14. Arany Z., Novikov M., Chin S., Ma Y., Rosenzweig A., Spiegelman B.M. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci U S A 2006, 103:10086-10091.
15. Lai L., Leone T.C., Zechner C., Schaeffer P.J., Kelly S.M., Flanagan D.P., et al. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev 2008, 22:1948-1961.
16. Lehman J.J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D.M., Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 2000, 106:847-856.
17. Sebastiani M., Giordano C., Nediani C., Travaglini C., Borchi E., Zani M., et al. Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 2007, 50:1362-1369.
18. Hay R.T. SUMO: a history of modification. Mol Cell 2005, 18:1-12.
19. Gill G. Something about SUMO inhibits transcription. Curr Opin Genet Dev 2005, 15:536-541.
20. Rytinki M.M., Palvimo J.J. SUMOylation attenuates the function of PGC-1alpha. J Biol Chem 2009, 284:26184-26193.
21. Wang J., Schwartz R.J. Sumoylation and regulation of cardiac gene expression. Circ Res 2010, 107:19-29.
22. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 2007, 8:947-956.
23. Yeh E.T. SUMOylation and de-SUMOylation: wrestling with life's processes. J Biol Chem 2009, 284:8223-8227.
24. Hay R.T. SUMO-specific proteases: a twist in the tail. Trends Cell Biol 2007, 17:370-376.
25. Cheng J., Kang X., Zhang S., Yeh E.T. SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 2007, 131:584-595.
26. Kang X., Qi Y., Zuo Y., Wang Q., Zou Y., Schwartz R.J., et al. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol Cell 2010, 38:191-201.
27. Xu Y., Zuo Y., Zhang H., Kang X., Yue F., Yi Z., et al. Induction of SENP1 in endothelial cells contributes to hypoxia-driven VEGF expression and angiogenesis. J Biol Chem 2010, 285:36682-36688.
28. Jiang Z., Fan Q., Zhang Z., Zou Y., Cai R., Wang Q., et al. SENP1 deficiency promotes ER stress-induced apoptosis by increasing XBP1 SUMOylation. Cell Cycle 2012, 11:1118-1122.
29. Van Nguyen T., Angkasekwinai P., Dou H., Lin F.M., Lu L.S., Cheng J., et al. SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Mol Cell 2012, 45:210-221.
30. Cai R., Yu T., Huang C., Xia X., Liu X., Gu J., et al. SUMO-specific protease 1 regulates mitochondrial biogenesis through PGC-1alpha. J Biol Chem 2012, 287:44464-44470.
31. Ahuja P., Wanagat J., Wang Z., Wang Y., Liem D.A., Ping P., et al. Divergent mitochondrial biogenesis responses in human cardiomyopathy. Circulation 2013, 127:1957-1967.
32. Zincarelli C., Soltys S., Rengo G., Rabinowitz J.E. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008, 16:1073-1080.
33. Vega R.B., Huss J.M., Kelly D.P. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 2000, 20:1868-1876.
34. Rohas L.M., St-Pierre J., Uldry M., Jager S., Handschin C., Spiegelman B.M. A fundamental system of cellular energy homeostasis regulated by PGC-1alpha. Proc Natl Acad Sci U S A 2007, 104:7933-7938.
35. Czubryt M.P., McAnally J., Fishman G.I., Olson E.N. Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci U S A 2003, 100:1711-1716.
36. Handschin C., Rhee J., Lin J., Tarr P.T., Spiegelman B.M. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc Natl Acad Sci U S A 2003, 100:7111-7116.
37. Gregoire S., Yang X.J. Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol Cell Biol 2005, 25:2273-2287.
38. Kang J., Gocke C.B., Yu H. Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity. BMC Biochem 2006, 7:5.
39. Wilkins B.J., Dai Y.S., Bueno O.F., Parsons S.A., Xu J., Plank D.M., et al. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004, 94:110-118.
40. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 2003, 17:2205-2232.
41. Braz J.C., Bueno O.F., Liang Q., Wilkins B.J., Dai Y.S., Parsons S., et al. Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 2003, 111:1475-1486.
42. Liang Q., Bueno O.F., Wilkins B.J., Kuan C.Y., Xia Y., Molkentin J.D. c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. EMBO J 2003, 22:5079-5089.
43. Molkentin J.D. Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc Res 2004, 63:467-475.
44. Leone T.C., Lehman J.J., Finck B.N., Schaeffer P.J., Wende A.R., Boudina S., et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 2005, 3:e101.
45. Kho C., Lee A., Jeong D., Oh J.G., Chaanine A.H., Kizana E., et al. SUMO1-dependent modulation of SERCA2a in heart failure. Nature 2011, 477:601-605.