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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. / Khudiakov, Aleksandr; Zaytseva, Anastasia; Perepelina, Kseniya; Smolina, Natalia; Pervunina, Tatiana; Vasichkina, Elena; Karpushev, Alexey; Tomilin, Alexey; Malashicheva, Anna; Kostareva, Anna.

In: Biochimica et Biophysica Acta - Molecular Basis of Disease, Vol. 1866, No. 11, 165915, 01.11.2020.

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@article{f6fa75e765674666b468fcef7708a3e7,
title = "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",
abstract = "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.",
keywords = "Arrhythmogenic cardiomyopathy, Glycogen synthase kinase 3 beta, Plakophilin 2, Sodium current, Wnt/β-catenin signaling, Mutation/genetics, Humans, Electrophysiology, Sodium/metabolism, Wnt Signaling Pathway/genetics, Plakophilins/genetics, Patch-Clamp Techniques, Glycogen Synthase Kinase 3 beta/genetics, HEK293 Cells, Induced Pluripotent Stem Cells/metabolism, Cardiomyopathies/genetics, CELLS, GLYCOGEN-SYNTHASE KINASE-3, Wnt/beta-catenin signaling, DIFFERENTIATION, INHIBITORS, MUTATIONS, RIGHT-VENTRICULAR CARDIOMYOPATHY",
author = "Aleksandr Khudiakov and Anastasia Zaytseva and Kseniya Perepelina and Natalia Smolina and Tatiana Pervunina and Elena Vasichkina and Alexey Karpushev and Alexey Tomilin and Anna Malashicheva and Anna Kostareva",
note = "Funding Information: This work was supported by Russian Science Foundation grants number 14-15-00745-П (iPSC-CMs signaling and electrophysiological experiments) and number 19-75-00070 (GSK3B experiments). Publisher Copyright: {\textcopyright} 2020 Elsevier B.V. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",
year = "2020",
month = nov,
day = "1",
doi = "10.1016/j.bbadis.2020.165915",
language = "English",
volume = "1866",
journal = "Biochimica et Biophysica Acta - Molecular Basis of Disease",
issn = "0925-4439",
publisher = "Elsevier",
number = "11",

}

RIS

TY - JOUR

T1 - 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

AU - Khudiakov, Aleksandr

AU - Zaytseva, Anastasia

AU - Perepelina, Kseniya

AU - Smolina, Natalia

AU - Pervunina, Tatiana

AU - Vasichkina, Elena

AU - Karpushev, Alexey

AU - Tomilin, Alexey

AU - Malashicheva, Anna

AU - Kostareva, Anna

N1 - Funding Information: This work was supported by Russian Science Foundation grants number 14-15-00745-П (iPSC-CMs signaling and electrophysiological experiments) and number 19-75-00070 (GSK3B experiments). Publisher Copyright: © 2020 Elsevier B.V. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/11/1

Y1 - 2020/11/1

N2 - 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.

AB - 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.

KW - Arrhythmogenic cardiomyopathy

KW - Glycogen synthase kinase 3 beta

KW - Plakophilin 2

KW - Sodium current

KW - Wnt/β-catenin signaling

KW - Mutation/genetics

KW - Humans

KW - Electrophysiology

KW - Sodium/metabolism

KW - Wnt Signaling Pathway/genetics

KW - Plakophilins/genetics

KW - Patch-Clamp Techniques

KW - Glycogen Synthase Kinase 3 beta/genetics

KW - HEK293 Cells

KW - Induced Pluripotent Stem Cells/metabolism

KW - Cardiomyopathies/genetics

KW - CELLS

KW - GLYCOGEN-SYNTHASE KINASE-3

KW - Wnt/beta-catenin signaling

KW - DIFFERENTIATION

KW - INHIBITORS

KW - MUTATIONS

KW - RIGHT-VENTRICULAR CARDIOMYOPATHY

UR - http://www.scopus.com/inward/record.url?scp=85089352325&partnerID=8YFLogxK

U2 - 10.1016/j.bbadis.2020.165915

DO - 10.1016/j.bbadis.2020.165915

M3 - Article

C2 - 32768677

AN - SCOPUS:85089352325

VL - 1866

JO - Biochimica et Biophysica Acta - Molecular Basis of Disease

JF - Biochimica et Biophysica Acta - Molecular Basis of Disease

SN - 0925-4439

IS - 11

M1 - 165915

ER -

ID: 71709481