The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal

Abstract Pw1/Peg3 is an imprinted gene expressed from the paternally inherited allele. Several imprinted genes, including Pw1/Peg3, have been shown to regulate overall body size and play a role in adult stem cells. Pw1/Peg3 is expressed in muscle stem cells (satellite cells) as well as a progenitor...

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Autores principales:	Rosa Maria Correra, David Ollitrault, Mariana Valente, Alessia Mazzola, Bjorn T. Adalsteinsson, Anne C. Ferguson-Smith, Giovanna Marazzi, David A. Sassoon
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2018
Materias:	Satellite Cells Myofiber Number Skeletal Muscle Fiber Number Maternal Allele Mutant Muscle Medicine R Science Q
Acceso en línea:	https://doaj.org/article/586cd7a187fa4bc7bf928acf22771284
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spelling	oai:doaj.org-article:586cd7a187fa4bc7bf928acf227712842021-12-02T15:05:29ZThe imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal10.1038/s41598-018-32941-x2045-2322https://doaj.org/article/586cd7a187fa4bc7bf928acf227712842018-10-01T00:00:00Zhttps://doi.org/10.1038/s41598-018-32941-xhttps://doaj.org/toc/2045-2322Abstract Pw1/Peg3 is an imprinted gene expressed from the paternally inherited allele. Several imprinted genes, including Pw1/Peg3, have been shown to regulate overall body size and play a role in adult stem cells. Pw1/Peg3 is expressed in muscle stem cells (satellite cells) as well as a progenitor subset of muscle interstitial cells (PICs) in adult skeletal muscle. We therefore examined the impact of loss-of-function of Pw1/Peg3 during skeletal muscle growth and in muscle stem cell behavior. We found that constitutive loss of Pw1/Peg3 function leads to a reduced muscle mass and myofiber number. In newborn mice, the reduction in fiber number is increased in homozygous mutants as compared to the deletion of only the paternal Pw1/Peg3 allele, indicating that the maternal allele is developmentally functional. Constitutive and a satellite cell-specific deletion of Pw1/Peg3, revealed impaired muscle regeneration and a reduced capacity of satellite cells for self-renewal. RNA sequencing analyses revealed a deregulation of genes that control mitochondrial function. Consistent with these observations, Pw1/Peg3 mutant satellite cells displayed increased mitochondrial activity coupled with accelerated proliferation and differentiation. Our data show that Pw1/Peg3 regulates muscle fiber number determination during fetal development in a gene-dosage manner and regulates satellite cell metabolism in the adult.Rosa Maria CorreraDavid OllitraultMariana ValenteAlessia MazzolaBjorn T. AdalsteinssonAnne C. Ferguson-SmithGiovanna MarazziDavid A. SassoonNature PortfolioarticleSatellite CellsMyofiber NumberSkeletal Muscle Fiber NumberMaternal AlleleMutant MuscleMedicineRScienceQENScientific Reports, Vol 8, Iss 1, Pp 1-14 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Satellite Cells Myofiber Number Skeletal Muscle Fiber Number Maternal Allele Mutant Muscle Medicine R Science Q
spellingShingle	Satellite Cells Myofiber Number Skeletal Muscle Fiber Number Maternal Allele Mutant Muscle Medicine R Science Q Rosa Maria Correra David Ollitrault Mariana Valente Alessia Mazzola Bjorn T. Adalsteinsson Anne C. Ferguson-Smith Giovanna Marazzi David A. Sassoon The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
description	Abstract Pw1/Peg3 is an imprinted gene expressed from the paternally inherited allele. Several imprinted genes, including Pw1/Peg3, have been shown to regulate overall body size and play a role in adult stem cells. Pw1/Peg3 is expressed in muscle stem cells (satellite cells) as well as a progenitor subset of muscle interstitial cells (PICs) in adult skeletal muscle. We therefore examined the impact of loss-of-function of Pw1/Peg3 during skeletal muscle growth and in muscle stem cell behavior. We found that constitutive loss of Pw1/Peg3 function leads to a reduced muscle mass and myofiber number. In newborn mice, the reduction in fiber number is increased in homozygous mutants as compared to the deletion of only the paternal Pw1/Peg3 allele, indicating that the maternal allele is developmentally functional. Constitutive and a satellite cell-specific deletion of Pw1/Peg3, revealed impaired muscle regeneration and a reduced capacity of satellite cells for self-renewal. RNA sequencing analyses revealed a deregulation of genes that control mitochondrial function. Consistent with these observations, Pw1/Peg3 mutant satellite cells displayed increased mitochondrial activity coupled with accelerated proliferation and differentiation. Our data show that Pw1/Peg3 regulates muscle fiber number determination during fetal development in a gene-dosage manner and regulates satellite cell metabolism in the adult.
format	article
author	Rosa Maria Correra David Ollitrault Mariana Valente Alessia Mazzola Bjorn T. Adalsteinsson Anne C. Ferguson-Smith Giovanna Marazzi David A. Sassoon
author_facet	Rosa Maria Correra David Ollitrault Mariana Valente Alessia Mazzola Bjorn T. Adalsteinsson Anne C. Ferguson-Smith Giovanna Marazzi David A. Sassoon
author_sort	Rosa Maria Correra
title	The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
title_short	The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
title_full	The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
title_fullStr	The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
title_full_unstemmed	The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
title_sort	imprinted gene pw1/peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal
publisher	Nature Portfolio
publishDate	2018
url	https://doaj.org/article/586cd7a187fa4bc7bf928acf22771284
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The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal

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