Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms

Background: Fabry disease (FD) results from pathogenic <i>GLA</i> variants, causing lysosomal α-galactosidase A (α-GalA) deficiency and sphingolipid ceramide trihexoside (Gb3 or THC) accumulation. Disease phenotype varies widely but cardiomyopathy is commonly life-limiting. As a multisys...

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Main Authors: Kathleen Nicholls, Andrea Wise, David Elliot, Menno ter Huurne, Maria Fuller, Sharon Ricardo
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:International Journal of Translational Medicine
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Online Access:https://www.mdpi.com/2673-8937/5/2/15
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author Kathleen Nicholls
Andrea Wise
David Elliot
Menno ter Huurne
Maria Fuller
Sharon Ricardo
author_facet Kathleen Nicholls
Andrea Wise
David Elliot
Menno ter Huurne
Maria Fuller
Sharon Ricardo
author_sort Kathleen Nicholls
collection DOAJ
description Background: Fabry disease (FD) results from pathogenic <i>GLA</i> variants, causing lysosomal α-galactosidase A (α-GalA) deficiency and sphingolipid ceramide trihexoside (Gb3 or THC) accumulation. Disease phenotype varies widely but cardiomyopathy is commonly life-limiting. As a multisystemic disorder, FD initiates at the cellular level; however, the mechanism/s underlying Gb3-induced cell dysfunction remains largely unknown. This study established an in vitro mutation-specific model of Fabry cardiomyopathy using human-induced pluripotent stem cell (iPSC)-derived cardiomyocytes to explore underlying cell pathology. Methods: Skin biopsies from consenting Fabry patients and normal control subjects were reprogrammed to iPSCs then differentiated into cardiomyocytes. The <i>GLA</i> mutations in Fabry cell lines were corrected using CRISP-Cas9. Phenotypic characteristics, α-Gal A activity, Gb3 accumulation, functional status, and lipid analysis were assessed. Cardiomyocytes derived from two patients with severe clinical phenotype and genotypes, <i>GLA</i><sup>c.851T>C</sup>, <i>GLA</i><sup>c.1193_1196del</sup>, and their respective corrected lines, <i>GLA</i><sup>corr c.851T>C</sup>, <i>GLA</i><sup>corr c.1193_1196del</sup>, were selected for further studies. Results: Cardiomyocytes derived from individuals with FD iPSCs exhibited stable expression of cardiomyocyte markers and spontaneous contraction, morphological features of FD, reduced α-Gal A activity, and accumulation of Gb3. Lipidomic profiling revealed differences in the Gb3 isoform profile between the control and FD patient iPSC-derived cardiomyocytes. Contraction strength was unchanged but relaxation after contraction was delayed, mimicking the diastolic dysfunction typical of Fabry cardiomyopathy. Conclusions: iPSC-derived cardiomyocytes provide a useful model to explore aspects of Fabry cardiomyopathy, including disruptions in sphingolipid pathways, proteomics, and multigene expression that together link genotype to phenotype. The platform potentially offers broad applicability across many genetic diseases and offers the prospect of testing and implementation of individualised therapies.
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spelling doaj-art-0a190b9f7fc24f3cad24d4756e9ab98c2025-08-20T03:24:39ZengMDPI AGInternational Journal of Translational Medicine2673-89372025-04-01521510.3390/ijtm5020015Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease MechanismsKathleen Nicholls0Andrea Wise1David Elliot2Menno ter Huurne3Maria Fuller4Sharon Ricardo5Department of Nephrology, Royal Melbourne Hospital and the University of Melbourne, Parkville, VIC 3050, AustraliaDepartment of Pharmacology, Monash University, Melbourne, VIC 3800, AustraliaNovo Nordisk Center for Stem Cell Medicine, Murdoch Children’s Research Institute, Royal Children’s Hospital, Parkville, VIC 3052, AustraliaNovo Nordisk Center for Stem Cell Medicine, Murdoch Children’s Research Institute, Royal Children’s Hospital, Parkville, VIC 3052, AustraliaGenetics and Molecular Pathology, South Australia Pathology at Women’s and Children’s Hospital and University of Adelaide, North Adelaide, SA 5006, AustraliaDepartment of Pharmacology, Monash University, Melbourne, VIC 3800, AustraliaBackground: Fabry disease (FD) results from pathogenic <i>GLA</i> variants, causing lysosomal α-galactosidase A (α-GalA) deficiency and sphingolipid ceramide trihexoside (Gb3 or THC) accumulation. Disease phenotype varies widely but cardiomyopathy is commonly life-limiting. As a multisystemic disorder, FD initiates at the cellular level; however, the mechanism/s underlying Gb3-induced cell dysfunction remains largely unknown. This study established an in vitro mutation-specific model of Fabry cardiomyopathy using human-induced pluripotent stem cell (iPSC)-derived cardiomyocytes to explore underlying cell pathology. Methods: Skin biopsies from consenting Fabry patients and normal control subjects were reprogrammed to iPSCs then differentiated into cardiomyocytes. The <i>GLA</i> mutations in Fabry cell lines were corrected using CRISP-Cas9. Phenotypic characteristics, α-Gal A activity, Gb3 accumulation, functional status, and lipid analysis were assessed. Cardiomyocytes derived from two patients with severe clinical phenotype and genotypes, <i>GLA</i><sup>c.851T>C</sup>, <i>GLA</i><sup>c.1193_1196del</sup>, and their respective corrected lines, <i>GLA</i><sup>corr c.851T>C</sup>, <i>GLA</i><sup>corr c.1193_1196del</sup>, were selected for further studies. Results: Cardiomyocytes derived from individuals with FD iPSCs exhibited stable expression of cardiomyocyte markers and spontaneous contraction, morphological features of FD, reduced α-Gal A activity, and accumulation of Gb3. Lipidomic profiling revealed differences in the Gb3 isoform profile between the control and FD patient iPSC-derived cardiomyocytes. Contraction strength was unchanged but relaxation after contraction was delayed, mimicking the diastolic dysfunction typical of Fabry cardiomyopathy. Conclusions: iPSC-derived cardiomyocytes provide a useful model to explore aspects of Fabry cardiomyopathy, including disruptions in sphingolipid pathways, proteomics, and multigene expression that together link genotype to phenotype. The platform potentially offers broad applicability across many genetic diseases and offers the prospect of testing and implementation of individualised therapies.https://www.mdpi.com/2673-8937/5/2/15Fabry disease<i>GLA</i> variantsinduced pluripotent stem cellscardiomyocytesα-Gal A deficiencyGb3 accumulation
spellingShingle Kathleen Nicholls
Andrea Wise
David Elliot
Menno ter Huurne
Maria Fuller
Sharon Ricardo
Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
International Journal of Translational Medicine
Fabry disease
<i>GLA</i> variants
induced pluripotent stem cells
cardiomyocytes
α-Gal A deficiency
Gb3 accumulation
title Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
title_full Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
title_fullStr Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
title_full_unstemmed Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
title_short Mutation-Specific Cardiomyocyte Lines from Patients with Fabry Disease: A Sustainable In Vitro Model to Investigate Structure, Function, and Disease Mechanisms
title_sort mutation specific cardiomyocyte lines from patients with fabry disease a sustainable in vitro model to investigate structure function and disease mechanisms
topic Fabry disease
<i>GLA</i> variants
induced pluripotent stem cells
cardiomyocytes
α-Gal A deficiency
Gb3 accumulation
url https://www.mdpi.com/2673-8937/5/2/15
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