Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)

Background Hypertrophic cardiomyopathy is an autosomal dominant cardiac disease. The mechanisms that determine its variable expressivity are poorly understood. Epigenetics could play a crucial role in bridging the gap between genotype and phenotype by orchestrating the interplay between the environm...

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Main Authors: Alfonso Peñarroya, Rebeca Lorca, José Julián Rodríguez Reguero, Juan Gómez, Pablo Avanzas, Juan Ramon Tejedor, Agustín F. Fernandez, Mario F. Fraga
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
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Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.124.035777
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author Alfonso Peñarroya
Rebeca Lorca
José Julián Rodríguez Reguero
Juan Gómez
Pablo Avanzas
Juan Ramon Tejedor
Agustín F. Fernandez
Mario F. Fraga
author_facet Alfonso Peñarroya
Rebeca Lorca
José Julián Rodríguez Reguero
Juan Gómez
Pablo Avanzas
Juan Ramon Tejedor
Agustín F. Fernandez
Mario F. Fraga
author_sort Alfonso Peñarroya
collection DOAJ
description Background Hypertrophic cardiomyopathy is an autosomal dominant cardiac disease. The mechanisms that determine its variable expressivity are poorly understood. Epigenetics could play a crucial role in bridging the gap between genotype and phenotype by orchestrating the interplay between the environment and the genome regulation. In this study we aimed to establish a possible correlation between the peripheral blood DNA methylation patterns and left ventricular hypertrophy severity in patients with hypertrophic cardiomyopathy, evaluating the potential impact of lifestyle variables and providing a biological context to the observed changes. Methods and Results Methylation data were obtained from peripheral blood samples (Infinium MethylationEPIC BeadChip arrays). We employed multiple pair‐matched models to extract genomic positions whose methylation correlates with the degree of left ventricular hypertrophy in 3 monozygotic twin pairs carrying the same founder pathogenic variant (MYBPC3 p.Gly263Ter). This model enables the isolation of the environmental influence, beyond age, on DNA methylation changes by removing the genetic background. Our results revealed a more anxious personality among more severely affected individuals. We identified 56 differentially methylated positions that exhibited moderate, proportional changes in methylation associated with left ventricular hypertrophy. These differentially methylated positions were enriched in regions regulated by repressor histone marks and tended to cluster at genes involved in left ventricular hypertrophy development, such as HOXA5, TRPC3, UCN3, or PLSCR2, suggesting that changes in peripheral blood may reflect myocardial alterations. Conclusions We present a unique pair‐matched model, based on 3 monozygotic twin pairs carrying the same founder pathogenic variant and different phenotypes. This study provides further evidence of the pivotal role of epigenetics in hypertrophic cardiomyopathy variable expressivity.
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spelling doaj-art-46e63391c45c41ae8d0a7886775cb27e2025-08-20T01:54:22ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802024-11-01132110.1161/JAHA.124.035777Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)Alfonso Peñarroya0Rebeca Lorca1José Julián Rodríguez Reguero2Juan Gómez3Pablo Avanzas4Juan Ramon Tejedor5Agustín F. Fernandez6Mario F. Fraga7Nanomaterials and Nanotechnology Research Center (CINN) Spanish National Research Council (CSIC) El Entrego Asturias SpainHealth Research Institute of the Principality of Asturias (ISPA) Oviedo Asturias SpainHealth Research Institute of the Principality of Asturias (ISPA) Oviedo Asturias SpainHealth Research Institute of the Principality of Asturias (ISPA) Oviedo Asturias SpainHealth Research Institute of the Principality of Asturias (ISPA) Oviedo Asturias SpainNanomaterials and Nanotechnology Research Center (CINN) Spanish National Research Council (CSIC) El Entrego Asturias SpainNanomaterials and Nanotechnology Research Center (CINN) Spanish National Research Council (CSIC) El Entrego Asturias SpainNanomaterials and Nanotechnology Research Center (CINN) Spanish National Research Council (CSIC) El Entrego Asturias SpainBackground Hypertrophic cardiomyopathy is an autosomal dominant cardiac disease. The mechanisms that determine its variable expressivity are poorly understood. Epigenetics could play a crucial role in bridging the gap between genotype and phenotype by orchestrating the interplay between the environment and the genome regulation. In this study we aimed to establish a possible correlation between the peripheral blood DNA methylation patterns and left ventricular hypertrophy severity in patients with hypertrophic cardiomyopathy, evaluating the potential impact of lifestyle variables and providing a biological context to the observed changes. Methods and Results Methylation data were obtained from peripheral blood samples (Infinium MethylationEPIC BeadChip arrays). We employed multiple pair‐matched models to extract genomic positions whose methylation correlates with the degree of left ventricular hypertrophy in 3 monozygotic twin pairs carrying the same founder pathogenic variant (MYBPC3 p.Gly263Ter). This model enables the isolation of the environmental influence, beyond age, on DNA methylation changes by removing the genetic background. Our results revealed a more anxious personality among more severely affected individuals. We identified 56 differentially methylated positions that exhibited moderate, proportional changes in methylation associated with left ventricular hypertrophy. These differentially methylated positions were enriched in regions regulated by repressor histone marks and tended to cluster at genes involved in left ventricular hypertrophy development, such as HOXA5, TRPC3, UCN3, or PLSCR2, suggesting that changes in peripheral blood may reflect myocardial alterations. Conclusions We present a unique pair‐matched model, based on 3 monozygotic twin pairs carrying the same founder pathogenic variant and different phenotypes. This study provides further evidence of the pivotal role of epigenetics in hypertrophic cardiomyopathy variable expressivity.https://www.ahajournals.org/doi/10.1161/JAHA.124.035777DNA methylationepigeneticsHCMmonozygotic twinsMYBPC3 pathogenic variantphenotypic expressivity
spellingShingle Alfonso Peñarroya
Rebeca Lorca
José Julián Rodríguez Reguero
Juan Gómez
Pablo Avanzas
Juan Ramon Tejedor
Agustín F. Fernandez
Mario F. Fraga
Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
DNA methylation
epigenetics
HCM
monozygotic twins
MYBPC3 pathogenic variant
phenotypic expressivity
title Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
title_full Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
title_fullStr Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
title_full_unstemmed Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
title_short Epigenetic Study of Cohort of Monozygotic Twins With Hypertrophic Cardiomyopathy Due to MYBPC3 (Cardiac Myosin‐Binding Protein C)
title_sort epigenetic study of cohort of monozygotic twins with hypertrophic cardiomyopathy due to mybpc3 cardiac myosin binding protein c
topic DNA methylation
epigenetics
HCM
monozygotic twins
MYBPC3 pathogenic variant
phenotypic expressivity
url https://www.ahajournals.org/doi/10.1161/JAHA.124.035777
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