Sodium current abnormalities and deregulation of Wnt/β-catenin signaling in iPSC-derived cardiomyocytes generated from patient with arrhythmogenic cardiomyopathy harboring compound genetic variants in plakophilin 2 gene.


Journal

Biochimica et biophysica acta. Molecular basis of disease
ISSN: 1879-260X
Titre abrégé: Biochim Biophys Acta Mol Basis Dis
Pays: Netherlands
ID NLM: 101731730

Informations de publication

Date de publication:
01 11 2020
Historique:
received: 20 11 2019
revised: 29 06 2020
accepted: 01 08 2020
pubmed: 10 8 2020
medline: 15 12 2020
entrez: 10 8 2020
Statut: ppublish

Résumé

Mutations in desmosomal genes linked to arrhythmogenic cardiomyopathy are commonly associated with Wnt/β-catenin signaling abnormalities and reduction of the sodium current density. Inhibitors of GSK3B were reported to restore sodium current and improve heart function in various arrhythmogenic cardiomyopathy models, but mechanisms underlying this effect remain unclear. We hypothesized that there is a crosstalk between desmosomal proteins, signaling pathways, and cardiac sodium channels. To reveal molecular mechanisms of arrhythmogenic cardiomyopathy, we established human iPSC-based model of this pathology. iPSC-derived cardiomyocytes from patient carrying two genetic variants in PKP2 gene demonstrated that PKP2 haploinsufficiency due to frameshift variant, in combination with the missense variant expressed from the second allele, was associated with decreased Wnt/β-catenin activity and reduced sodium current. Different approaches were tested to restore impaired cardiomyocytes functions, including wild type PKP2 transduction, GSK3B inhibition and Wnt/β-catenin signaling modulation. Inhibition of GSK3B led to the restoration of both Wnt/β-catenin signaling activity and sodium current density in patient-specific cardiomyocytes while GSK3B activation led to the reduction of sodium current density. Moreover, we found that upon inhibition GSK3B sodium current was restored through Wnt/β-catenin-independent mechanism. We propose that alterations in GSK3B-Wnt/β-catenin signaling pathways lead to regulation of sodium current implying its role in molecular pathogenesis of arrhythmogenic cardiomyopathy.

Sections du résumé

BACKGROUND
Mutations in desmosomal genes linked to arrhythmogenic cardiomyopathy are commonly associated with Wnt/β-catenin signaling abnormalities and reduction of the sodium current density. Inhibitors of GSK3B were reported to restore sodium current and improve heart function in various arrhythmogenic cardiomyopathy models, but mechanisms underlying this effect remain unclear. We hypothesized that there is a crosstalk between desmosomal proteins, signaling pathways, and cardiac sodium channels.
METHODS AND RESULTS
To reveal molecular mechanisms of arrhythmogenic cardiomyopathy, we established human iPSC-based model of this pathology. iPSC-derived cardiomyocytes from patient carrying two genetic variants in PKP2 gene demonstrated that PKP2 haploinsufficiency due to frameshift variant, in combination with the missense variant expressed from the second allele, was associated with decreased Wnt/β-catenin activity and reduced sodium current. Different approaches were tested to restore impaired cardiomyocytes functions, including wild type PKP2 transduction, GSK3B inhibition and Wnt/β-catenin signaling modulation. Inhibition of GSK3B led to the restoration of both Wnt/β-catenin signaling activity and sodium current density in patient-specific cardiomyocytes while GSK3B activation led to the reduction of sodium current density. Moreover, we found that upon inhibition GSK3B sodium current was restored through Wnt/β-catenin-independent mechanism.
CONCLUSION
We propose that alterations in GSK3B-Wnt/β-catenin signaling pathways lead to regulation of sodium current implying its role in molecular pathogenesis of arrhythmogenic cardiomyopathy.

Identifiants

pubmed: 32768677
pii: S0925-4439(20)30263-5
doi: 10.1016/j.bbadis.2020.165915
pii:
doi:

Substances chimiques

Plakophilins 0
Sodium 9NEZ333N27
GSK3B protein, human EC 2.7.11.1
Glycogen Synthase Kinase 3 beta EC 2.7.11.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

165915

Informations de copyright

Copyright © 2020 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Aleksandr Khudiakov (A)

Almazov National Medical Research Centre, Saint-Petersburg, Russia. Electronic address: khudyakov_aa@almazovcentre.ru.

Anastasia Zaytseva (A)

Almazov National Medical Research Centre, Saint-Petersburg, Russia; Sechenov Institute of Evolutionary Physiology and Biochemistry RAS, Saint-Petersburg, Russia.

Kseniya Perepelina (K)

Almazov National Medical Research Centre, Saint-Petersburg, Russia; Saint Petersburg State University, Saint-Petersburg, Russia.

Natalia Smolina (N)

Almazov National Medical Research Centre, Saint-Petersburg, Russia; Department of Women's and Children's Health, Center for Molecular Medicine, Karolinska Institute, Stockholm, Sweden.

Tatiana Pervunina (T)

Almazov National Medical Research Centre, Saint-Petersburg, Russia.

Elena Vasichkina (E)

Almazov National Medical Research Centre, Saint-Petersburg, Russia.

Alexey Karpushev (A)

Almazov National Medical Research Centre, Saint-Petersburg, Russia.

Alexey Tomilin (A)

Institute of Cytology RAS, Saint-Petersburg, Russia.

Anna Malashicheva (A)

Almazov National Medical Research Centre, Saint-Petersburg, Russia; Saint Petersburg State University, Saint-Petersburg, Russia; Institute of Cytology RAS, Saint-Petersburg, Russia.

Anna Kostareva (A)

Almazov National Medical Research Centre, Saint-Petersburg, Russia; Department of Women's and Children's Health, Center for Molecular Medicine, Karolinska Institute, Stockholm, Sweden.

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Classifications MeSH