Constitutively active calcineurin induces cardiac endoplasmic reticulum stress and protects against apoptosis that is mediated by α-crystallin-B

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 43, 2010, Pages 18481-18486

  Bousette, Nicolas ^a,b   Chugh, Shaan ^a,b   Fong, Vincent ^a,b   Isserlin, Ruth ^a,b   Kim, Kyoung Han ^a   Volchuk, Allen ^c   Backx, Peter H ^a,b   Liu, Peter ^d   Kislinger, Thomas ^d   MacLennan, David H ^a,b   Emili, Andrew ^a,b   Gramolini, Anthony O ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; CALCINEURIN; PROTEOME; SHORT HAIRPIN RNA; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HEART; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; UPREGULATION;

ALPHA-CRYSTALLIN B CHAIN; ANIMALS; APOPTOSIS; CALCINEURIN; CARDIOMEGALY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; MICE; MICE, TRANSGENIC; MYOCARDIUM; PROTEIN ARRAY ANALYSIS; PROTEOMICS; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL;

MUS;

EID: 78649866399     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1013555107     Document Type: Article

References (48)

1. Kung H-C, Hoyert DL, Xu J, Murphy SL (2008) Deaths: Final data for 2005. Natl Vital Stat Rep 56(10):1-120.
2. Rosamond W, et al.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2008) Heart disease and stroke statistics - 2008 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 117:e25-e146.
3. MacLennan DH, Kranias EG (2003) Phospholamban: A crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4:566-577.
4. Gramolini AO, et al. (2008) Comparative proteomics profiling of a phospholamban mutant mouse model of dilated cardiomyopathy reveals progressive intracellular stress responses. Mol Cell Proteomics 7:519-533.
5. Molkentin JD, et al. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228. (Pubitemid 28180855)
6. Haq S, et al. (2001) Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure. Circulation 103:670-677.
7. Semeniuk LM, et al. (2003) Time-dependent systolic and diastolic function in mice overexpressing calcineurin. Am J Physiol Heart Circ Physiol 284:H425-H430.
8. Chu G, et al. (2002) Enhanced myocyte contractility and Ca2+ handling in a calcineurin transgenic model of heart failure. Cardiovasc Res 54:105-116.
9. Dong D, et al. (2003) Overexpression of calcineurin in mouse causes sudden cardiac death associated with decreased density of K+ channels. Cardiovasc Res 57:320-332.
10. Gramolini AO, Kislinger T, Liu P, MacLennan DH, Emili A (2007) Analyzing the cardiac muscle proteome by liquid chromatography-mass spectrometry-based expression proteomics. Methods Mol Biol 357:15-31.
11. Bousette N, et al. (2009) Large-scale characterization and analysis of the murine cardiac proteome. J Proteome Res 8:1887-1901.
12. Peng W, et al. (2010) Cardioprotection by CaMKII-deltaB is mediated by phosphorylation of heat shock factor 1 and subsequent expression of inducible heat shock protein 70. Circ Res 106:102-110.
13. Small EM, Frost RJ, Olson EN (2010) MicroRNAs add a new dimension to cardiovascular disease. Circulation 121:1022-1032.
14. Dong DL, et al. (2010) Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: A novel mechanism for progressive cardiac hypertrophy. Hypertension 55:946-952.
15. van Rooij E, et al. (2006) A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci USA 103:18255-18260.
16. Takemura G, et al. (1991) Expression and distribution of atrial natriuretic peptide in human hypertrophic ventricle of hypertensive hearts and hearts with hypertrophic cardiomyopathy. Circulation 83:181-190.
17. Schunkert H, et al. (1990) Increased rat cardiac angiotensin converting enzyme activity and mRNA expression in pressure overload left ventricular hypertrophy. Effects on coronary resistance, contractility, and relaxation. J Clin Invest 86:1913-1920.
18. Reiser PJ, Portman MA, Ning XH, Schomisch Moravec C (2001) Human cardiac myosin heavy chain isoforms in fetal and failing adult atria and ventricles. Am J Physiol Heart Circ Physiol 280:H1814-H1820.
19. McGrath MJ, et al. (2006) Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly. J Biol Chem 281:7666-7683.
20. Lim DS, Roberts R, Marian AJ (2001) Expression profiling of cardiac genes in human hypertrophic cardiomyopathy: Insight into the pathogenesis of phenotypes. J Am Coll Cardiol 38:1175-1180.
21. Gaussin V, et al. (2003) Common genomic response in different mouse models of beta-adrenergic-induced cardiomyopathy. Circulation 108:2926-2933.
22. Peters NS, Coromilas J, Severs NJ, Wit AL (1997) Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 95:988-996.
23. Gillis AM, et al. (2004) Heart block in mice overexpressing calcineurin but not NF-AT3. Cardiovasc Res 64:488-495.
24. Davis DL, et al. (2001) A GATA-6 gene heart-region-specific enhancer provides a novel means to mark and probe a discrete component of the mouse cardiac conduction system. Mech Dev 108:105-119.
25. Rath N, Wang Z, Lu MM, Morrisey EE (2005) LMCD1/Dyxin is a novel transcriptional cofactor that restricts GATA6 function by inhibiting DNA binding. Mol Cell Biol 25:8864-8873. (Pubitemid 41429078)
26. Allard MF, Schönekess BO, Henning SL, English DR, Lopaschuk GD (1994) Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol 267:H742-H750.
27. Sambandam N, Lopaschuk GD, Brownsey RW, Allard MF (2002) Energy metabolism in the hypertrophied heart. Heart Fail Rev 7:161-173.
28. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: Cell life and death decisions. J Clin Invest 115:2656-2664.
29. De Windt LJ, et al. (2000) Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: An apoptosis-independent model of dilated heart failure. Circ Res 86:255-263.
30. Bueno OF, et al. (2004) Calcineurin Abeta gene targeting predisposes the myocardium to acute ischemia-induced apoptosis and dysfunction. Circ Res 94:91-99.
31. Obasanjo-Blackshire K, et al. (2006) Calcineurin regulates NFAT-dependent iNOS expression and protection of cardiomyocytes: Co-operation with Src tyrosine kinase. Cardiovasc Res 71:672-683.
32. Lee JT, Lee TJ, Kim CH, Kim NS, Kwon TK (2009) Over-expression of Reticulon 3 (RTN3) enhances TRAIL-mediated apoptosis via up-regulation of death receptor 5 (DR5) and down-regulation of c-FLIP. Cancer Lett 279:185-192.
33. Zhu L, Xiang R, Dong W, Liu Y, Qi Y (2007) Anti-apoptotic activity of Bcl-2 is enhanced by its interaction with RTN3. Cell Biol Int 31:825-830.
34. Wan Q, et al. (2007) Reticulon 3 mediates Bcl-2 accumulation in mitochondria in response to endoplasmic reticulum stress. Apoptosis 12:319-328.
35. Mehlen P, Kretz-Remy C, Préville X, Arrigo AP (1996) Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15:2695-2706.
36. Mehlen P, Schulze-Osthoff K, Arrigo AP (1996) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271:16510-16514.
37. Kamradt MC, Chen F, Cryns VL (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 276:16059-16063.
38. Manukyan I, Galatioto J, Mascareno E, Bhaduri S, Siddiqui MA (2009) Cross-talk between calcineurin/NFAT and Jak/STAT signalling induces cardioprotective alphaB-crystallin gene expression in response to hypertrophic stimuli. J Cell Mol Med 14:1707-1716.
39. Morrison LE, Whittaker RJ, Klepper RE, Wawrousek EF, Glembotski CC (2004) Roles for alphaB-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion- induced damage in a KO mouse model. Am J Physiol Heart Circ Physiol 286:H847-H855.
40. Jin JK, et al. (2008) Localization of phosphorylated alphaB-crystallin to heart mitochondria during ischemia-reperfusion. Am J Physiol Heart Circ Physiol 294:H337-H344.
41. Whittaker R, et al. (2009) Kinetics of the translocation and phosphorylation of alphaB-crystallin in mouse heart mitochondria during ex vivo ischemia. Am J Physiol Heart Circ Physiol 296:H1633-H1642.
42. Mao YW, Liu JP, Xiang H, Li DW (2004) Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 11:512-526.
43. Verschuure P, et al. (2002) Translocation of small heat shock proteins to the actin cytoskeleton upon proteasomal inhibition. J Mol Cell Cardiol 34:117-128.
44. Vicart P, et al. (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20:92-95.
45. Bova MP, et al. (1999) 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 USA 96:6137-6142.
46. Wang X, et al. (2001) Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ Res 89:84-91.
47. Maloyan A, et al. (2009) Biochemical and mechanical dysfunction in a mouse model of desmin-related myopathy. Circ Res 104:1021-1028.
48. Moffat J, et al. (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124:1283-1298.