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The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart

Long noncoding RNAs (lncRNAs) are emerging as critical regulators of heart physiology and disease, although the studies unveiling their modes of action are still limited to few examples. We recently identified pCharme, a chromatin-associated lncRNA whose functional knockout in mice results in defect...

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Autores principales: Taliani, Valeria, Buonaiuto, Giulia, Desideri, Fabio, Setti, Adriano, Santini, Tiziana, Galfrè, Silvia, Schirone, Leonardo, Mariani, Davide, Frati, Giacomo, Valenti, Valentina, Sciarretta, Sebastiano, Perlas, Emerald, Nicoletti, Carmine, Musarò, Antonio, Ballarino, Monica
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10023161/
https://www.ncbi.nlm.nih.gov/pubmed/36877136
http://dx.doi.org/10.7554/eLife.81360
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author Taliani, Valeria
Buonaiuto, Giulia
Desideri, Fabio
Setti, Adriano
Santini, Tiziana
Galfrè, Silvia
Schirone, Leonardo
Mariani, Davide
Frati, Giacomo
Valenti, Valentina
Sciarretta, Sebastiano
Perlas, Emerald
Nicoletti, Carmine
Musarò, Antonio
Ballarino, Monica
author_facet Taliani, Valeria
Buonaiuto, Giulia
Desideri, Fabio
Setti, Adriano
Santini, Tiziana
Galfrè, Silvia
Schirone, Leonardo
Mariani, Davide
Frati, Giacomo
Valenti, Valentina
Sciarretta, Sebastiano
Perlas, Emerald
Nicoletti, Carmine
Musarò, Antonio
Ballarino, Monica
author_sort Taliani, Valeria
collection PubMed
description Long noncoding RNAs (lncRNAs) are emerging as critical regulators of heart physiology and disease, although the studies unveiling their modes of action are still limited to few examples. We recently identified pCharme, a chromatin-associated lncRNA whose functional knockout in mice results in defective myogenesis and morphological remodeling of the cardiac muscle. Here, we combined Cap-Analysis of Gene Expression (CAGE), single-cell (sc)RNA sequencing, and whole-mount in situ hybridization analyses to study pCharme cardiac expression. Since the early steps of cardiomyogenesis, we found the lncRNA being specifically restricted to cardiomyocytes, where it assists the formation of specific nuclear condensates containing MATR3, as well as important RNAs for cardiac development. In line with the functional significance of these activities, pCharme ablation in mice results in a delayed maturation of cardiomyocytes, which ultimately leads to morphological alterations of the ventricular myocardium. Since congenital anomalies in myocardium are clinically relevant in humans and predispose patients to major complications, the identification of novel genes controlling cardiac morphology becomes crucial. Our study offers unique insights into a novel lncRNA-mediated regulatory mechanism promoting cardiomyocyte maturation and bears relevance to Charme locus for future theranostic applications.
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spelling pubmed-100231612023-03-18 The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart Taliani, Valeria Buonaiuto, Giulia Desideri, Fabio Setti, Adriano Santini, Tiziana Galfrè, Silvia Schirone, Leonardo Mariani, Davide Frati, Giacomo Valenti, Valentina Sciarretta, Sebastiano Perlas, Emerald Nicoletti, Carmine Musarò, Antonio Ballarino, Monica eLife Chromosomes and Gene Expression Long noncoding RNAs (lncRNAs) are emerging as critical regulators of heart physiology and disease, although the studies unveiling their modes of action are still limited to few examples. We recently identified pCharme, a chromatin-associated lncRNA whose functional knockout in mice results in defective myogenesis and morphological remodeling of the cardiac muscle. Here, we combined Cap-Analysis of Gene Expression (CAGE), single-cell (sc)RNA sequencing, and whole-mount in situ hybridization analyses to study pCharme cardiac expression. Since the early steps of cardiomyogenesis, we found the lncRNA being specifically restricted to cardiomyocytes, where it assists the formation of specific nuclear condensates containing MATR3, as well as important RNAs for cardiac development. In line with the functional significance of these activities, pCharme ablation in mice results in a delayed maturation of cardiomyocytes, which ultimately leads to morphological alterations of the ventricular myocardium. Since congenital anomalies in myocardium are clinically relevant in humans and predispose patients to major complications, the identification of novel genes controlling cardiac morphology becomes crucial. Our study offers unique insights into a novel lncRNA-mediated regulatory mechanism promoting cardiomyocyte maturation and bears relevance to Charme locus for future theranostic applications. eLife Sciences Publications, Ltd 2023-03-06 /pmc/articles/PMC10023161/ /pubmed/36877136 http://dx.doi.org/10.7554/eLife.81360 Text en © 2023, Taliani, Buonaiuto et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Chromosomes and Gene Expression
Taliani, Valeria
Buonaiuto, Giulia
Desideri, Fabio
Setti, Adriano
Santini, Tiziana
Galfrè, Silvia
Schirone, Leonardo
Mariani, Davide
Frati, Giacomo
Valenti, Valentina
Sciarretta, Sebastiano
Perlas, Emerald
Nicoletti, Carmine
Musarò, Antonio
Ballarino, Monica
The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title_full The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title_fullStr The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title_full_unstemmed The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title_short The long noncoding RNA Charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
title_sort long noncoding rna charme supervises cardiomyocyte maturation by controlling cell differentiation programs in the developing heart
topic Chromosomes and Gene Expression
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10023161/
https://www.ncbi.nlm.nih.gov/pubmed/36877136
http://dx.doi.org/10.7554/eLife.81360
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