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PMID: 20937869 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Bousette N, Chugh S, Fong V, Isserlin R, Kim KH, Volchuk A, Backx PH, Liu P, Kislinger T, MacLennan DH, Emili A, Gramolini AO

Abstract

Cardiac-specific overexpression of a constitutively active form of calcineurin A (CNA) leads directly to cardiac hypertrophy in the CNA mouse model. Because cardiac hypertrophy is a prominent characteristic of many cardiomyopathies, we deduced that delineating the proteomic profile of ventricular tissue from this model might identify novel, widely applicable therapeutic targets. Proteomic analysis was carried out by subjecting fractionated cardiac samples from CNA mice and their WT littermates to gel-free liquid chromatography linked to shotgun tandem mass spectrometry. We identified 1,918 proteins with high confidence, of which 290 were differentially expressed. Microarray analysis of the same tissue provided us with alterations in the ventricular transcriptome. Because bioinformatic analyses of both the proteome and transcriptome demonstrated the up-regulation of endoplasmic reticulum stress, we validated its occurrence in adult CNA hearts through a series of immunoblots and RT-PCR analyses. Endoplasmic reticulum stress often leads to increased apoptosis, but apoptosis was minimal in CNA hearts, suggesting that activated calcineurin might protect against apoptosis. Indeed, the viability of cultured neonatal mouse cardiomyocytes (NCMs) from CNA mice was higher than WT after serum starvation, an apoptotic trigger. Proteomic data identified α-crystallin B (Cryab) as a potential mediator of this protective effect and we showed that silencing of Cryab via lentivector-mediated transduction of shRNAs in NCMs led to a significant reduction in NCM viability and loss of protection against apoptosis. The identification of Cryab as a downstream effector of calcineurin-induced protection against apoptosis will permit elucidation of its role in cardiac apoptosis and its potential as a therapeutic target.

MeSH Terms
Animals Apoptosis/physiology Calcineurin/genetics,metabolism Cardiomegaly/genetics,metabolism,pathology Endoplasmic Reticulum/metabolism Gene Expression Gene Expression Profiling Gene Knockdown Techniques Mice Mice, Transgenic Myocardium/cytology,metabolism Protein Array Analysis Proteomics RNA, Small Interfering/genetics Stress, Physiological alpha-Crystallin B Chain/antagonists & inhibitors,genetics,metabolism
Chemicals
RNA, Small Interfering alpha-Crystallin B Chain Calcineurin
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Bousette Nicolas
Department of Physiology, University of Toronto, Toronto, ON, Canada M5G 1A8.
Chugh Shaan
Fong Vincent
Isserlin Ruth
Kim Kyoung-Han
Volchuk Allen
Backx Peter H
Liu Peter
Kislinger Thomas
MacLennan David H
Emili Andrew
Gramolini Anthony O
References (48)
48 references, click to expand
  1. Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly.
    J Biol Chem. 2006 Mar 17;281(11):7666-83 PMID: 16407297
  2. Analyzing the cardiac muscle proteome by liquid chromatography-mass spectrometry-based expression proteomics.
    Methods Mol Biol. 2007;357:15-31 PMID: 17172675
  3. 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. 1990 Dec;86(6):1913-20 PMID: 2174912
  4. Heart disease and stroke statistics--2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee.
    Circulation. 2008 Jan 29;117(4):e25-146 PMID: 18086926
  5. Common genomic response in different mouse models of beta-adrenergic-induced cardiomyopathy.
    Circulation. 2003 Dec 9;108(23):2926-33 PMID: 14623810
  6. MicroRNAs add a new dimension to cardiovascular disease.
    Circulation. 2010 Mar 2;121(8):1022-32 PMID: 20194875
  7. 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. 2004 Mar;286(3):H847-55 PMID: 14592939
  8. Energy metabolism in the hypertrophied heart.
    Heart Fail Rev. 2002 Apr;7(2):161-73 PMID: 11988640
  9. Comparative proteomics profiling of a phospholamban mutant mouse model of dilated cardiomyopathy reveals progressive intracellular stress responses.
    Mol Cell Proteomics. 2008 Mar;7(3):519-33 PMID: 18056057
  10. Phospholamban: a crucial regulator of cardiac contractility.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):566-77 PMID: 12838339
  11. 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. 1996 Jun 3;15(11):2695-706 PMID: 8654367
  12. Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis.
    Cell Death Differ. 2004 May;11(5):512-26 PMID: 14752512
  13. Expression and distribution of atrial natriuretic peptide in human hypertrophic ventricle of hypertensive hearts and hearts with hypertrophic cardiomyopathy.
    Circulation. 1991 Jan;83(1):181-90 PMID: 1824622
  14. Anti-apoptotic activity of Bcl-2 is enhanced by its interaction with RTN3.
    Cell Biol Int. 2007 Aug;31(8):825-30 PMID: 17379544
  15. Cross-talk between calcineurin/NFAT and Jak/STAT signalling induces cardioprotective alphaB-crystallin gene expression in response to hypertrophic stimuli.
    J Cell Mol Med. 2010 Jun;14(6B):1707-16 PMID: 19538478
  16. Heart block in mice overexpressing calcineurin but not NF-AT3.
    Cardiovasc Res. 2004 Dec 1;64(3):488-95 PMID: 15537502
  17. Reticulon 3 mediates Bcl-2 accumulation in mitochondria in response to endoplasmic reticulum stress.
    Apoptosis. 2007 Feb;12(2):319-28 PMID: 17191123
  18. LMCD1/Dyxin is a novel transcriptional cofactor that restricts GATA6 function by inhibiting DNA binding.
    Mol Cell Biol. 2005 Oct;25(20):8864-73 PMID: 16199866
  19. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure.
    Proc Natl Acad Sci U S A. 2006 Nov 28;103(48):18255-60 PMID: 17108080
  20. Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure.
    Circulation. 2001 Feb 6;103(5):670-7 PMID: 11156878
  21. Deaths: final data for 2005.
    Natl Vital Stat Rep. 2008 Apr 24;56(10):1-120 PMID: 18512336
  22. Human cardiac myosin heavy chain isoforms in fetal and failing adult atria and ventricles.
    Am J Physiol Heart Circ Physiol. 2001 Apr;280(4):H1814-20 PMID: 11247796
  23. Calcineurin regulates NFAT-dependent iNOS expression and protection of cardiomyocytes: co-operation with Src tyrosine kinase.
    Cardiovasc Res. 2006 Sep 1;71(4):672-83 PMID: 16828070
  24. Kinetics of the translocation and phosphorylation of alphaB-crystallin in mouse heart mitochondria during ex vivo ischemia.
    Am J Physiol Heart Circ Physiol. 2009 May;296(5):H1633-42 PMID: 19252088
  25. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen.
    Cell. 2006 Mar 24;124(6):1283-98 PMID: 16564017
  26. 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. 1997 Feb 18;95(4):988-96 PMID: 9054762
  27. Endoplasmic reticulum stress: cell life and death decisions.
    J Clin Invest. 2005 Oct;115(10):2656-64 PMID: 16200199
  28. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice.
    Circ Res. 2001 Jul 6;89(1):84-91 PMID: 11440982
  29. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts.
    Am J Physiol. 1994 Aug;267(2 Pt 2):H742-50 PMID: 8067430
  30. Cardioprotection by CaMKII-deltaB is mediated by phosphorylation of heat shock factor 1 and subsequent expression of inducible heat shock protein 70.
    Circ Res. 2010 Jan 8;106(1):102-10 PMID: 19910575
  31. Enhanced myocyte contractility and Ca2+ handling in a calcineurin transgenic model of heart failure.
    Cardiovasc Res. 2002 Apr;54(1):105-16 PMID: 12062367
  32. 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. 2001 May 11;276(19):16059-63 PMID: 11274139
  33. Overexpression of calcineurin in mouse causes sudden cardiac death associated with decreased density of K+ channels.
    Cardiovasc Res. 2003 Feb;57(2):320-32 PMID: 12566105
  34. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy.
    Nat Genet. 1998 Sep;20(1):92-5 PMID: 9731540
  35. Translocation of small heat shock proteins to the actin cytoskeleton upon proteasomal inhibition.
    J Mol Cell Cardiol. 2002 Feb;34(2):117-28 PMID: 11851352
  36. 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. 2001 Oct;108(1-2):105-19 PMID: 11578865
  37. Localization of phosphorylated alphaB-crystallin to heart mitochondria during ischemia-reperfusion.
    Am J Physiol Heart Circ Physiol. 2008 Jan;294(1):H337-44 PMID: 17993600
  38. Calcineurin Abeta gene targeting predisposes the myocardium to acute ischemia-induced apoptosis and dysfunction.
    Circ Res. 2004 Jan 9;94(1):91-9 PMID: 14615291
  39. Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: An apoptosis-independent model of dilated heart failure.
    Circ Res. 2000 Feb 18;86(3):255-63 PMID: 10679475
  40. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy.
    Cell. 1998 Apr 17;93(2):215-28 PMID: 9568714
  41. Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: a novel mechanism for progressive cardiac hypertrophy.
    Hypertension. 2010 Apr;55(4):946-52 PMID: 20177001
  42. Large-scale characterization and analysis of the murine cardiac proteome.
    J Proteome Res. 2009 Apr;8(4):1887-901 PMID: 19714876
  43. Time-dependent systolic and diastolic function in mice overexpressing calcineurin.
    Am J Physiol Heart Circ Physiol. 2003 Feb;284(2):H425-30 PMID: 12388248
  44. Expression profiling of cardiac genes in human hypertrophic cardiomyopathy: insight into the pathogenesis of phenotypes.
    J Am Coll Cardiol. 2001 Oct;38(4):1175-80 PMID: 11583900
  45. 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. 2009 Jul 8;279(2):185-92 PMID: 19250737
  46. 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 May 25;96(11):6137-42 PMID: 10339554
  47. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death.
    J Biol Chem. 1996 Jul 12;271(28):16510-4 PMID: 8663291
  48. Biochemical and mechanical dysfunction in a mouse model of desmin-related myopathy.
    Circ Res. 2009 Apr 24;104(8):1021-8 PMID: 19299643
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-10-26
Epub
2010-00-11
Pages
18481-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2972971
Subset
IM
Grants
CIHR · 84267-1 · Canada
CIHR · 87143-1 · Canada
CIHR · MT 125450 · Canada
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