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PMID: 21742996 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Catecholaminergic-induced arrhythmias in failing cardiomyocytes associated with human HRCS96A variant overexpression.

American journal of physiology. Heart and circulatory physiology ·Vol. 301 ·No. 4 ·2011-10-00 ·Pages H1588-95

Han P, Cai W, Wang Y, Lam CK, Arvanitis DA, Singh VP, Chen S, Zhang H, Zhang R, Cheng H, Kranias EG

Abstract

The histidine-rich calcium binding protein (HRC) Ser96Ala polymorphism was shown to correlate with ventricular arrhythmias and sudden death only in dilated cardiomyopathy patients but not in healthy human carriers. In the present study, we assessed the molecular and cellular mechanisms underlying human arrhythmias by adenoviral expression of the human wild-type (HRC(WT)) or mutant HRC (HRC(S96A)) in adult rat ventricular cardiomyocytes. Total HRC protein was increased by ∼50% in both HRC(WT)- and HRC(S96A)-infected cells. The HRC(S96A) mutant exacerbated the inhibitory effects of HRC(WT) on the amplitude of Ca(2+) transients, prolongation of Ca(2+) decay time, and caffeine-induced sarcoplasmic reticulum Ca(2+) release. Consistent with these findings, HRC(S96A) reduced maximal sarcoplasmic reticulum calcium uptake rate to a higher extent than HRC(WT). Furthermore, the frequency of spontaneous Ca(2+) sparks, which was reduced by HRC(WT), was increased by mutant HRC(S96A) under resting conditions although there were no spontaneous Ca(2+) waves under stress conditions. However, expression of the HRC(S96A) genetic variant in cardiomyocytes from a rat model of postmyocardial infarction heart failure induced dramatic disturbances of rhythmic Ca(2+) transients. These findings indicate that the HRC Ser96Ala variant increases the propensity of arrhythmogenic Ca(2+) waves in the stressed failing heart, suggesting a link between this genetic variant and life-threatening ventricular arrhythmias in human carriers.

MeSH Terms
Adenoviridae/genetics Amino Acid Substitution Animals Arrhythmias, Cardiac/chemically induced,genetics Blotting, Western Calcium/metabolism,physiology Calcium Signaling/genetics,physiology Calcium-Binding Proteins/genetics Catecholamines DNA, Complementary/biosynthesis,genetics Electrocardiography Gene Expression HEK293 Cells Heart Failure/chemically induced,genetics Humans Immunoprecipitation Male Myocytes, Cardiac/drug effects Point Mutation/genetics,physiology Polymorphism, Genetic/genetics Rats Rats, Wistar Sarcoplasmic Reticulum Calcium-Transporting ATPases/genetics
Chemicals
Atp2a2 protein, rat Calcium-Binding Proteins Catecholamines DNA, Complementary HRC protein, rat Sarcoplasmic Reticulum Calcium-Transporting ATPases Calcium
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Han Peidong
Department of Pharmacology and Cell Biophysics, University of Cincinnati College of Medicine, Cincinnati, Ohio 45267-0575, USA.
Cai Wenfeng
Wang Yanru
Lam Chi Keung
Arvanitis Demetrios A
Singh Vivek P
Chen Shan
Zhang Huiliang
Zhang Rongli
Cheng Heping
Kranias Evangelia G
References (25)
25 references, click to expand
  1. Regulation of myocardial function by histidine-rich, calcium-binding protein.
    Am J Physiol Heart Circ Physiol. 2004 Oct;287(4):H1705-11 PMID: 15191886
  2. Sarcoplasmic reticulum calcium overloading in junctin deficiency enhances cardiac contractility but increases ventricular automaticity.
    Circulation. 2007 Jan 23;115(3):300-9 PMID: 17224479
  3. Abnormal interactions of calsequestrin with the ryanodine receptor calcium release channel complex linked to exercise-induced sudden cardiac death.
    Circ Res. 2006 May 12;98(9):1151-8 PMID: 16601229
  4. Upregulated Na/Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure.
    Basic Res Cardiol. 2002;97 Suppl 1:I36-42 PMID: 12479232
  5. Ablation of triadin causes loss of cardiac Ca2+ release units, impaired excitation-contraction coupling, and cardiac arrhythmias.
    Proc Natl Acad Sci U S A. 2009 May 5;106(18):7636-41 PMID: 19383796
  6. Calcium handling proteins in the failing human heart.
    Basic Res Cardiol. 1997;92 Suppl 1:87-93 PMID: 9202848
  7. Calcium sparks.
    Physiol Rev. 2008 Oct;88(4):1491-545 PMID: 18923188
  8. Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes.
    Circ Res. 2003 Sep 19;93(6):531-40 PMID: 12919952
  9. On the role of junctin in cardiac Ca2+ handling, contractility, and heart failure.
    Am J Physiol Heart Circ Physiol. 2007 Jul;293(1):H728-34 PMID: 17400717
  10. Intra-sarcoplasmic reticulum free [Ca2+] and buffering in arrhythmogenic failing rabbit heart.
    Circ Res. 2007 Oct 12;101(8):802-10 PMID: 17704210
  11. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation.
    Circ Res. 1994 Sep;75(3):401-9 PMID: 8062415
  12. Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase.
    Am J Physiol Heart Circ Physiol. 2007 Sep;293(3):H1581-9 PMID: 17526652
  13. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane.
    J Biol Chem. 1997 Sep 12;272(37):23389-97 PMID: 9287354
  14. Beneficial effects of chronic pharmacological manipulation of beta-adrenoreceptor subtype signaling in rodent dilated ischemic cardiomyopathy.
    Circulation. 2004 Aug 31;110(9):1083-90 PMID: 15313944
  15. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin.
    Circ Res. 2004 Mar 5;94(4):471-7 PMID: 14715535
  16. Carvedilol and its new analogs suppress arrhythmogenic store overload-induced Ca2+ release.
    Nat Med. 2011 Jul 10;17(8):1003-9 PMID: 21743453
  17. Calcium sparks and [Ca2+]i waves in cardiac myocytes.
    Am J Physiol. 1996 Jan;270(1 Pt 1):C148-59 PMID: 8772440
  18. The Ser96Ala variant in histidine-rich calcium-binding protein is associated with life-threatening ventricular arrhythmias in idiopathic dilated cardiomyopathy.
    Eur Heart J. 2008 Oct;29(20):2514-25 PMID: 18617481
  19. Ionic mechanism of delayed afterdepolarizations in ventricular cells isolated from human end-stage failing hearts.
    Circulation. 2001 Nov 27;104(22):2728-33 PMID: 11723027
  20. Expansion of acute myocardial infarction: an experimental study.
    Circulation. 1982 Jun;65(7):1446-50 PMID: 7074800
  21. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia.
    Circulation. 2001 Jan 16;103(2):196-200 PMID: 11208676
  22. Sudden cardiac death in dilated cardiomyopathy -- therapeutic options.
    Herz. 2002 Dec;27(8):750-9 PMID: 12574892
  23. Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes.
    Circ Res. 2005 Apr 1;96(6):651-8 PMID: 15731460
  24. Histidine-rich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function.
    J Mol Cell Cardiol. 2006 May;40(5):653-65 PMID: 16600288
  25. Interaction of HRC (histidine-rich Ca(2+)-binding protein) and triadin in the lumen of sarcoplasmic reticulum.
    J Biol Chem. 2001 Oct 26;276(43):39533-8 PMID: 11504710
Article Info
Journal
American journal of physiology. Heart and circulatory physiology
Abbr.
Am J Physiol Heart Circ Physiol
ISSN
1522-1539
Published
2011-10-00
Epub
2011-00-08
Pages
H1588-95
Language
English
Region
United States
NLM ID
100901228
PMCID
PMC3197373
Subset
IM
Grants
NHLBI NIH HHS · HL-26057 · United States
NHLBI NIH HHS · HL-64018 · United States
NHLBI NIH HHS · HL-77101 · United States
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