Deciphering DSC2 arrhythmogenic cardiomyopathy electrical instability: From ion channels to ECG and tailored drug therapy.


Journal

Clinical and translational medicine
ISSN: 2001-1326
Titre abrégé: Clin Transl Med
Pays: United States
ID NLM: 101597971

Informations de publication

Date de publication:
03 2021
Historique:
revised: 22 01 2021
received: 02 12 2020
accepted: 25 01 2021
entrez: 30 3 2021
pubmed: 31 3 2021
medline: 11 1 2022
Statut: ppublish

Résumé

Severe ventricular rhythm disturbances are the hallmark of arrhythmogenic cardiomyopathy (ACM), and are often explained by structural conduction abnormalities. However, comprehensive investigations of ACM cell electrical instability are lacking. This study aimed to elucidate early electrical myogenic signature of ACM. We investigated a 41-year-old ACM patient with a missense mutation (c.394C>T) in the DSC2 gene, which encodes desmocollin 2. Pathogenicity of this variant was confirmed using a zebrafish DSC2 model system. Control and DSC2 patient-derived pluripotent stem cells were reprogrammed and differentiated into cardiomyocytes (hiPSC-CM) to examine the specific electromechanical phenotype and its modulation by antiarrhythmic drugs (AADs). Samples of the patient's heart and hiPSC-CM were examined to identify molecular and cellular alterations. A shortened action potential duration was associated with reduced Ca Thorough analysis of hiPSC-CM derived from the DSC2 patient revealed abnormal repolarization dynamics, prompting the discovery of a short QT interval in some ACM patients. Overall, these results confirm a myogenic origin of ACM electrical instability and provide a rationale for prescribing class 1 and 3 AADs in ACM patients with increased ventricular repolarization reserve.

Sections du résumé

BACKGROUND
Severe ventricular rhythm disturbances are the hallmark of arrhythmogenic cardiomyopathy (ACM), and are often explained by structural conduction abnormalities. However, comprehensive investigations of ACM cell electrical instability are lacking. This study aimed to elucidate early electrical myogenic signature of ACM.
METHODS
We investigated a 41-year-old ACM patient with a missense mutation (c.394C>T) in the DSC2 gene, which encodes desmocollin 2. Pathogenicity of this variant was confirmed using a zebrafish DSC2 model system. Control and DSC2 patient-derived pluripotent stem cells were reprogrammed and differentiated into cardiomyocytes (hiPSC-CM) to examine the specific electromechanical phenotype and its modulation by antiarrhythmic drugs (AADs). Samples of the patient's heart and hiPSC-CM were examined to identify molecular and cellular alterations.
RESULTS
A shortened action potential duration was associated with reduced Ca
CONCLUSIONS
Thorough analysis of hiPSC-CM derived from the DSC2 patient revealed abnormal repolarization dynamics, prompting the discovery of a short QT interval in some ACM patients. Overall, these results confirm a myogenic origin of ACM electrical instability and provide a rationale for prescribing class 1 and 3 AADs in ACM patients with increased ventricular repolarization reserve.

Identifiants

pubmed: 33784018
doi: 10.1002/ctm2.319
pmc: PMC7908047
doi:

Substances chimiques

Anti-Arrhythmia Agents 0
DSC2 protein, human 0
Desmocollins 0
Ion Channels 0

Types de publication

Case Reports Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e319

Informations de copyright

© 2021 The Authors. Clinical and Translational Medicine published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.

Références

HeartRhythm Case Rep. 2018 Oct 10;5(1):25-30
pubmed: 30693201
Annu Rev Med. 2010;61:233-53
pubmed: 20059337
Eur Heart J. 2013 Apr;34(15):1122-33
pubmed: 22798562
Cell Cycle. 2010 Apr 1;9(7):1246-52
pubmed: 20305388
Nat Methods. 2014 Aug;11(8):855-60
pubmed: 24930130
Nat Rev Cardiol. 2011 Nov 29;9(4):223-33
pubmed: 22124316
Stem Cells Transl Med. 2014 Dec;3(12):1467-72
pubmed: 25355730
Circ Cardiovasc Genet. 2015 Jun;8(3):437-46
pubmed: 25820315
Arch Pathol Lab Med. 2000 Feb;124(2):287-90
pubmed: 10656741
Europace. 2000 Oct;2(4):277-85
pubmed: 11194593
Pacing Clin Electrophysiol. 2014 Jan;37(1):90-4
pubmed: 24102153
Circ Cardiovasc Genet. 2016 Aug;9(4):384-7
pubmed: 27531918
Hum Mol Genet. 2001 Feb 1;10(3):189-94
pubmed: 11159936
Annu Rev Med. 2019 Jan 27;70:1-18
pubmed: 30355260
Am J Med Genet C Semin Med Genet. 2013 Aug;163C(3):185-97
pubmed: 23824749
Nat Med. 2009 Apr;15(4):380-3
pubmed: 19330009
Nature. 2013 Feb 7;494(7435):105-10
pubmed: 23354045
Arrhythm Electrophysiol Rev. 2016 May;5(1):45-9
pubmed: 27403293
J Am Coll Cardiol. 2009 Aug 11;54(7):609-15
pubmed: 19660690
Nat Commun. 2017 Jul 24;8(1):106
pubmed: 28740174
Nat Rev Mol Cell Biol. 2004 Apr;5(4):271-81
pubmed: 15071552
Europace. 2010 Jun;12(6):861-8
pubmed: 20400443
Heart Lung Circ. 2019 Jan;28(1):164-177
pubmed: 30446243
Cardiovasc Res. 2013 May 1;98(2):286-96
pubmed: 23334259
Circulation. 1992 Jul;86(1):29-37
pubmed: 1617780
Nat Rev Cardiol. 2019 Sep;16(9):519-537
pubmed: 31028357
Eur Heart J. 2010 Apr;31(7):806-14
pubmed: 20172912
Can J Cardiol. 2015 Nov;31(11):1313-24
pubmed: 26199027
J Dermatol. 2004 Mar;31(3):171-87
pubmed: 15187337
Arrhythm Electrophysiol Rev. 2015 Aug;4(2):86-9
pubmed: 26835106
Nat Protoc. 2013 Jan;8(1):162-75
pubmed: 23257984
Cardiovasc Res. 2011 Apr 1;90(1):77-87
pubmed: 21062920
Cardiovasc Res. 2017 Jan;113(1):102-111
pubmed: 28069705
Circulation. 1982 Feb;65(2):384-98
pubmed: 7053899
Circ J. 2013;77(6):1534-42
pubmed: 23514727
J Pharmacol Toxicol Methods. 2014 Jan-Feb;69(1):30-8
pubmed: 24140389
Circ J. 2015;79(7):1402-8
pubmed: 25971409
J Am Coll Cardiol. 2016 May 10;67(18):2108-2115
pubmed: 27151341
Cell. 2007 Nov 30;131(5):861-72
pubmed: 18035408
Am J Hum Genet. 2006 Dec;79(6):1081-8
pubmed: 17186466
Europace. 2018 Jun 1;20(FI1):f46-f56
pubmed: 29566126
PLoS One. 2017 Mar 24;12(3):e0174019
pubmed: 28339476
Circ Res. 2010 Sep 17;107(6):700-14
pubmed: 20847325
Heart Rhythm. 2014 Nov;11(11):1999-2009
pubmed: 25041964
Nat Rev Mol Cell Biol. 2000 Dec;1(3):208-16
pubmed: 11252896
J Mol Cell Cardiol. 2010 Feb;48(2):293-301
pubmed: 19835880
J Clin Invest. 2006 Jul;116(7):2012-21
pubmed: 16823493
Circulation. 2014 Mar 11;129(10):1092-103
pubmed: 24352520
Circ Res. 2012 Oct 12;111(9):1125-36
pubmed: 22912385

Auteurs

Adrien Moreau (A)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.

Jean-Baptiste Reisqs (JB)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.
Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Helene Delanoe-Ayari (H)

Institut lumière matière, Claude Bernard University, Lyon 1, Villeurbanne, France.

Marion Pierre (M)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.

Alexandre Janin (A)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.
Service de Rythmologie, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Cardiogénétique moléculaire, Centre de biologie et pathologie Est, Bron, France.

Antoine Deliniere (A)

Service de Rythmologie, Hospices Civils de Lyon, Lyon, France.

Francis Bessière (F)

Service de Rythmologie, Hospices Civils de Lyon, Lyon, France.

Albano C Meli (AC)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.

Azzouz Charrabi (A)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.

Estele Lafont (E)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Camille Valla (C)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Delphine Bauer (D)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Elodie Morel (E)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Vincent Gache (V)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Gilles Millat (G)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.
Service de Rythmologie, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Cardiogénétique moléculaire, Centre de biologie et pathologie Est, Bron, France.

Xavier Nissan (X)

CECS, I-Stem, Corbeil-Essonnes, France.

Adele Faucherre (A)

IGF, CNRS, INSERM, Université de Montpellier, Montpellier, France.

Chris Jopling (C)

IGF, CNRS, INSERM, Université de Montpellier, Montpellier, France.

Sylvain Richard (S)

PhyMedExp, INSERM U1046, CNRS UMR9214, Université de Montpellier, Montpellier, France.

Alexandre Mejat (A)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.

Philippe Chevalier (P)

Neuromyogene Institut, Claude Bernard University, Lyon 1, Villeurbanne, France.
Service de Rythmologie, Hospices Civils de Lyon, Lyon, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH