Nrf2 enhances myocardial clearance of toxic ubiquitinated proteins

Journal of Molecular and Cellular Cardiology

Volumn 72, Issue , 2014, Pages 305-315

  Wang, Wenjuan ^a,b   Li, Siying ^a,b   Wang, Hui ^a,b   Li, Bin ^a,b   Shao, Lei ^a,b   Lai, Yimu ^b   Horvath, Gary ^c   Wang, Qian ^c   Yamamoto, Masayuki ^d   Janicki, Joseph S ^b   Wang, Xing Li ^a   Tang, Dongqi ^a,b   Cui, Taixing ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Autophagy; Cardiac dysfunction; Necrosis; Nrf2; Oxidative stress; Proteinopathy

Indexed keywords

RAPAMYCIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); THIOREDOXIN 1; TRANSCRIPTION FACTOR NRF2; NFE2L2 PROTEIN, MOUSE; UBIQUITIN; UBIQUITINATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ARCH; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CARDIOVASCULAR PARAMETERS; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; HEART DISEASE; HEART HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEMODYNAMIC STRESS; MALE; MOUSE; MYOCARDIAL CLEARANCE; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; UBIQUITINATION; UPREGULATION; AGONISTS; ANIMAL; CARDIOMEGALY; FIBROSIS; GENE EXPRESSION; GENETICS; HEART MUSCLE; HEART MUSCLE CELL; METABOLISM; PATHOLOGY; PROTEINOSIS; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CARDIOMEGALY; FIBROSIS; GENE EXPRESSION; MALE; MICE; MICE, TRANSGENIC; MYOCARDIUM; MYOCYTES, CARDIAC; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEOLYSIS; RATS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITINATED PROTEINS;

EID: 84901306680     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.04.006     Document Type: Article

References (54)

1. Mudd J.O., Kass D.A. Tackling heart failure in the twenty-first century. Nature 2008, 451:919-928.
2. Takimoto E., Kass D.A. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007, 49:241-248.
3. Li J., Ichikawa T., Janicki J.S., Cui T. Targeting the Nrf2 pathway against cardiovascular disease. Expert Opin Ther Targets 2009, 13:785-794.
4. Ichikawa T., Li J., Meyer C.J., Janicki J.S., Hannink M., Cui T. Dihydro-CDDO-trifluoroethyl amide (dh404), a novel Nrf2 activator, suppresses oxidative stress in cardiomyocytes. PLoS One 2009, 4:e8391.
5. Li J., Zhang C., Xing Y., Janicki J.S., Yamamoto M., Wang X.L., et al. Up-regulation of p27(kip1) contributes to Nrf2-mediated protection against angiotensin II-induced cardiac hypertrophy. Cardiovasc Res 2011, 90:315-324.
6. Tan Y., Ichikawa T., Li J., Si Q., Yang H., Chen X., et al. Diabetic downregulation of Nrf2 activity via ERK contributes to oxidative stress-induced insulin resistance in cardiac cells in vitro and in vivo. Diabetes 2011, 60:625-633.
7. Xing Y., Niu T., Wang W., Li J., Li S., Janicki J.S., et al. Triterpenoid dihydro-CDDO-trifluoroethyl amide protects against maladaptive cardiac remodeling and dysfunction in mice: a critical role of Nrf2. PLoS One 2012, 7:e44899.
8. Calvert J.W., Elston M., Nicholson C.K., Gundewar S., Jha S., Elrod J.W., et al. Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation 2010, 122:11-19.
9. Zhang Y., Sano M., Shinmura K., Tamaki K., Katsumata Y., Matsuhashi T., et al. 4-Hydroxy-2-nonenal protects against cardiac ischemia-reperfusion injury via the Nrf2-dependent pathway. J Mol Cell Cardiol 2010, 49:576-586.
10. Sussan T.E., Rangasamy T., Blake D.J., Malhotra D., El-Haddad H., Bedja D., et al. Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc Natl Acad Sci U S A 2009, 106:250-255.
11. Piao C.S., Gao S., Lee G.H., Kim do S., Park B.H., Chae S.W., et al. Sulforaphane protects ischemic injury of hearts through antioxidant pathway and mitochondrial K(ATP) channels. Pharmacol Res 2010, 61:342-348.
12. Li J., Ichikawa T., Jin Y., Hofseth L.J., Nagarkatti P., Nagarkatti M., et al. An essential role of Nrf2 in American ginseng-mediated anti-oxidative actions in cardiomyocytes. J Ethnopharmacol 2010, 130:222-230.
13. Rajasekaran N.S., Connell P., Christians E.S., Yan L.J., Taylor R.P., Orosz A., et al. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130:427-439.
14. Rajasekaran N.S., Varadharaj S., Khanderao G.D., Davidson C.J., Kannan S., Firpo M.A., et al. Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid Redox Signal 2011, 14:957-971.
15. Riley B.E., Kaiser S.E., Shaler T.A., Ng A.C., Hara T., Hipp M.S., et al. Ubiquitin accumulation in autophagy-deficient mice is dependent on the Nrf2-mediated stress response pathway: a potential role for protein aggregation in autophagic substrate selection. J Cell Biol 2010, 191:537-552.
16. Rao V.A., Klein S.R., Bonar S.J., Zielonka J., Mizuno N., Dickey J.S., et al. The antioxidant transcription factor Nrf2 negatively regulates autophagy and growth arrest induced by the anticancer redox agent mitoquinone. J Biol Chem 2010, 285:34447-34459.
17. Fujita K., Maeda D., Xiao Q., Srinivasula S.M. Nrf2-mediated induction of p62 controls Toll-like receptor-4-driven aggresome-like induced structure formation and autophagic degradation. Proc Natl Acad Sci U S A 2011, 108:1427-1432.
18. Mattart L., Calay D., Simon D., Roebroek L., Caesens-Koenig L., Van Steenbrugge M., et al. The peroxynitrite donor 3-morpholinosydnonimine activates Nrf2 and the UPR leading to a cytoprotective response in endothelial cells. Cell Signal 2012, 24:199-213.
19. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
20. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
21. Wong E., Cuervo A.M. Integration of clearance mechanisms: the proteasome and autophagy. Cold Spring Harb Perspect Biol 2010, 2:a006734.
22. Su H., Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 2010, 85:253-262.
23. 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, 106:463-478.
24. Gottlieb R.A., Mentzer R.M. Autophagy during cardiac stress: joys and frustrations of autophagy. Annu Rev Physiol 2010, 72:45-59.
25. Wang Z.V., Rothermel B.A., Hill J.A. Autophagy in hypertensive heart disease. J Biol Chem 2010, 285:8509-8514.
26. Subramaniam A., Jones W.K., Gulick J., Wert S., Neumann J., Robbins J. Tissue-specific regulation of the alpha-myosin heavy chain gene promoter in transgenic mice. J Biol Chem 1991, 266:24613-24620.
27. Menzies F.M., Hourez R., Imarisio S., Raspe M., Sadiq O., Chandraratna D., et al. Puromycin-sensitive aminopeptidase protects against aggregation-prone proteins via autophagy. Hum Mol Genet 2010, 19:4573-4586.
28. Zhou Y.Y., Wang S.Q., Zhu W.Z., Chruscinski A., Kobilka B.K., Ziman B., et al. Culture and adenoviral infection of adult mouse cardiac myocytes: methods for cellular genetic physiology. Am J Physiol Heart Circ Physiol 2000, 279:H429-H436.
29. O'Connell T.D., Ishizaka S., Nakamura A., Swigart P.M., Rodrigo M.C., Simpson G.L., et al. The alpha(1A/C)- and alpha(1B)-adrenergic receptors are required for physiological cardiac hypertrophy in the double-knockout mouse. J Clin Invest 2003, 111:1783-1791.
30. Xia Y., Lee K., Li N., Corbett D., Mendoza L., Frangogiannis N.G. Characterization of the inflammatory and fibrotic response in a mouse model of cardiac pressure overload. Histochem Cell Biol 2009, 131:471-481.
31. Suryakumar G., Kasiganesan H., Balasubramanian S., Kuppuswamy D. Lack of beta3 integrin signaling contributes to calpain-mediated myocardial cell loss in pressure-overloaded myocardium. J Cardiovasc Pharmacol 2010, 55:567-573.
32. Chen Y., Guo H., Xu D., Xu X., Wang H., Hu X., et al. Left ventricular failure produces profound lung remodeling and pulmonary hypertension in mice: heart failure causes severe lung disease. Hypertension 2012, 59:1170-1178.
33. Tannous P., Zhu H., Nemchenko A., Berry J.M., Johnstone J.L., Shelton J.M., et al. Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation 2008, 117:3070-3078.
34. 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.
35. 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.
36. Klionsky D.J., Elazar Z., Seglen P.O., Rubinsztein D.C. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes?. Autophagy 2008, 4:849-850.
37. Iwai-Kanai E., Yuan H., Huang C., Sayen M.R., Perry-Garza C.N., Kim L., et al. A method to measure cardiac autophagic flux in vivo. Autophagy 2008, 4:322-329.
38. de Moissac D., Mustapha S., Greenberg A.H., Kirshenbaum L.A. Bcl-2 activates the transcription factor NFkappaB through the degradation of the cytoplasmic inhibitor IkappaBalpha. J Biol Chem 1998, 273:23946-23951.
39. + currents. Am J Physiol Cell Physiol 2003, 284:C1405-C1410.
40. Isodono K., Takahashi T., Imoto H., Nakanishi N., Ogata T., Asada S., et al. PARM-1 is an endoplasmic reticulum molecule involved in endoplasmic reticulum stress-induced apoptosis in rat cardiac myocytes. PLoS One 2010, 5:e9746.
41. Nickson P., Toth A., Erhardt P. PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress. Cardiovasc Res 2007, 73:48-56.
42. Kung G., Konstantinidis K., Kitsis R.N. Programmed necrosis, not apoptosis, in the heart. Circ Res 2011, 108:1017-1036.
43. Gold R., Schmied M., Giegerich G., Breitschopf H., Hartung H.P., Toyka K.V., et al. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest 1994, 71:219-225.
44. Ohno M., Takemura G., Ohno A., Misao J., Hayakawa Y., Minatoguchi S., et al. "Apoptotic" myocytes in infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with In situ nick end-labeling. Circulation 1998, 98:1422-1430.
45. Longnecker D.S., Shinozuka H., Farber E. Molecular pathology of in-vivo inhibition of protein synthesis. Electron microscopy of rat pancreatic acinar cells in puromycin-induced necrosis. Am J Pathol 1968, 52:891-915.
46. Szeto J., Kaniuk N.A., Canadien V., Nisman R., Mizushima N., Yoshimori T., et al. ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2006, 2:189-199.
47. Zhu H., Jia Z., Misra B.R., Zhang L., Cao Z., Yamamoto M., et al. Nuclear factor E2-related factor 2-dependent myocardiac cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol 2008, 8:71-85.
48. He X., Kan H., Cai L., Ma Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol 2009, 46:47-58.
49. Purdom-Dickinson S.E., Lin Y., Dedek M., Morrissy S., Johnson J., Chen Q.M. Induction of antioxidant and detoxification response by oxidants in cardiomyocytes: evidence from gene expression profiling and activation of Nrf2 transcription factor. J Mol Cell Cardiol 2007, 42:159-176.
50. Gurusamy N., Das D.K. Autophagy, redox signaling, and ventricular remodeling. Antioxid Redox Signal 2009, 11:1975-1988.
51. Yuan H., Perry C.N., Huang C., Iwai-Kanai E., Carreira R.S., Glembotski C.C., et al. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 2009, 296:H470-H479.
52. Younce C.W., Kolattukudy P.E. MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP. Biochem J 2010, 426:43-53.
53. Marambio P., Toro B., Sanhueza C., Troncoso R., Parra V., Verdejo H., et al. Glucose deprivation causes oxidative stress and stimulates aggresome formation and autophagy in cultured cardiac myocytes. Biochim Biophys Acta 1802, 2010:509-518.
54. Chapple S.J., Siow R.C., Mann G.E. Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging. Int J Biochem Cell Biol 2012, 44:1315-1320.