Loading…

Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration

Myosin heavy chain-perinatal (MyHC-perinatal) is one of two development-specific myosin heavy chains expressed exclusively during skeletal muscle development and regeneration. The specific functions of MyHC-perinatal are unclear, although mutations are known to lead to contracture syndromes such as...

Full description

Saved in:
Bibliographic Details
Published in:The FEBS journal 2024-07, Vol.291 (13), p.2836-2848
Main Authors: Sharma, Akashi, Zehra, Aatifa, Mathew, Sam J
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites cdi_FETCH-LOGICAL-c274t-2f610f3cebb8aa02ec5be045b6d28f35269d2e0fb7c1a582eb5d1af9a8e9ba4f3
container_end_page 2848
container_issue 13
container_start_page 2836
container_title The FEBS journal
container_volume 291
creator Sharma, Akashi
Zehra, Aatifa
Mathew, Sam J
description Myosin heavy chain-perinatal (MyHC-perinatal) is one of two development-specific myosin heavy chains expressed exclusively during skeletal muscle development and regeneration. The specific functions of MyHC-perinatal are unclear, although mutations are known to lead to contracture syndromes such as Trismus-pseudocamptodactyly syndrome. Here, we characterize the functions of MyHC-perinatal during skeletal muscle differentiation and regeneration. Loss of MyHC-perinatal function leads to enhanced differentiation characterized by increased expression of myogenic regulatory factors and differentiation index as well as reduced reserve cell numbers in vitro. Proteomic analysis revealed that loss of MyHC-perinatal function results in a switch from oxidative to glycolytic metabolism in myofibers, suggesting a shift from slow type I to fast type IIb fiber type, also supported by reduced mitochondrial numbers. Paracrine signals mediate the effect of loss of MyHC-perinatal function on myogenic differentiation, possibly mediated by non-apoptotic caspase-3 signaling along with enhanced levels of the pro-survival apoptosis regulator Bcl2 and nuclear factor kappa-B (NF-κB). Knockdown of MyHC-perinatal during muscle regeneration in vivo results in increased expression of the differentiation marker myogenin (MyoG) and impaired differentiation, evidenced by smaller myofibers, elevated fibrosis and reduction in the number of satellite cells. Thus, we find that MyHC-perinatal is a crucial regulator of myogenic differentiation, myofiber oxidative phenotype and regeneration.
doi_str_mv 10.1111/febs.17085
format article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2927214339</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2927214339</sourcerecordid><originalsourceid>FETCH-LOGICAL-c274t-2f610f3cebb8aa02ec5be045b6d28f35269d2e0fb7c1a582eb5d1af9a8e9ba4f3</originalsourceid><addsrcrecordid>eNpdkUtLw0AUhQdRbK1u_AEScCNi6jwyyWQpxRdU3Ci4CzPJHTs1ncSZpJh_b9LWLrybe7h8HC7nIHRO8JT0c6tB-SlJsOAHaEySiIZRzMXhXkcfI3Ti_RJjxqM0PUYjJhgXmIkxKl-6yhsbLECuuyBfSGPDGpyxspFl4OCzLWUDPvBfUMJwWrU-LyEojNbgwDZGNqayN0H1Y4periGoF2CrpqshkLYYLMCC21Cn6EjL0sPZbk_Q-8P92-wpnL8-Ps_u5mFOk6gJqY4J1iwHpYSUmELOFeCIq7igQjNO47SggLVKciK5oKB4QaROpYBUyUizCbra-tau-m7BN9nK-BzKUlqoWp_RlCaURIylPXr5D11WrbP9dxnDSZ9WikXSU9dbKneV9w50Vjuzkq7LCM6GDrKhg2zTQQ9f7CxbtYJij_6Fzn4BHISFTA</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3074999087</pqid></control><display><type>article</type><title>Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration</title><source>Wiley-Blackwell Read &amp; Publish Collection</source><creator>Sharma, Akashi ; Zehra, Aatifa ; Mathew, Sam J</creator><creatorcontrib>Sharma, Akashi ; Zehra, Aatifa ; Mathew, Sam J</creatorcontrib><description>Myosin heavy chain-perinatal (MyHC-perinatal) is one of two development-specific myosin heavy chains expressed exclusively during skeletal muscle development and regeneration. The specific functions of MyHC-perinatal are unclear, although mutations are known to lead to contracture syndromes such as Trismus-pseudocamptodactyly syndrome. Here, we characterize the functions of MyHC-perinatal during skeletal muscle differentiation and regeneration. Loss of MyHC-perinatal function leads to enhanced differentiation characterized by increased expression of myogenic regulatory factors and differentiation index as well as reduced reserve cell numbers in vitro. Proteomic analysis revealed that loss of MyHC-perinatal function results in a switch from oxidative to glycolytic metabolism in myofibers, suggesting a shift from slow type I to fast type IIb fiber type, also supported by reduced mitochondrial numbers. Paracrine signals mediate the effect of loss of MyHC-perinatal function on myogenic differentiation, possibly mediated by non-apoptotic caspase-3 signaling along with enhanced levels of the pro-survival apoptosis regulator Bcl2 and nuclear factor kappa-B (NF-κB). Knockdown of MyHC-perinatal during muscle regeneration in vivo results in increased expression of the differentiation marker myogenin (MyoG) and impaired differentiation, evidenced by smaller myofibers, elevated fibrosis and reduction in the number of satellite cells. Thus, we find that MyHC-perinatal is a crucial regulator of myogenic differentiation, myofiber oxidative phenotype and regeneration.</description><identifier>ISSN: 1742-464X</identifier><identifier>ISSN: 1742-4658</identifier><identifier>EISSN: 1742-4658</identifier><identifier>DOI: 10.1111/febs.17085</identifier><identifier>PMID: 38358038</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Apoptosis ; Bcl-2 protein ; Caspase ; Caspase 3 - genetics ; Caspase 3 - metabolism ; Cell differentiation ; Cell Differentiation - genetics ; Cells (biology) ; Differentiation ; Fibrosis ; Glycolysis ; Mice ; Muscle Development - genetics ; Muscle regulatory factor ; Muscle, Skeletal - cytology ; Muscle, Skeletal - metabolism ; Muscles ; Musculoskeletal system ; Myogenin ; Myogenin - genetics ; Myogenin - metabolism ; Myosin ; Myosin Heavy Chains - genetics ; Myosin Heavy Chains - metabolism ; Oxidation-Reduction ; Oxidative metabolism ; Paracrine signalling ; Phenotype ; Phenotypes ; Proteomics ; Regeneration ; Regeneration - genetics ; Satellite cells ; Skeletal muscle</subject><ispartof>The FEBS journal, 2024-07, Vol.291 (13), p.2836-2848</ispartof><rights>2024 Federation of European Biochemical Societies.</rights><rights>Copyright © 2024 Federation of European Biochemical Societies</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c274t-2f610f3cebb8aa02ec5be045b6d28f35269d2e0fb7c1a582eb5d1af9a8e9ba4f3</cites><orcidid>0000-0001-7908-6094</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38358038$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sharma, Akashi</creatorcontrib><creatorcontrib>Zehra, Aatifa</creatorcontrib><creatorcontrib>Mathew, Sam J</creatorcontrib><title>Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration</title><title>The FEBS journal</title><addtitle>FEBS J</addtitle><description>Myosin heavy chain-perinatal (MyHC-perinatal) is one of two development-specific myosin heavy chains expressed exclusively during skeletal muscle development and regeneration. The specific functions of MyHC-perinatal are unclear, although mutations are known to lead to contracture syndromes such as Trismus-pseudocamptodactyly syndrome. Here, we characterize the functions of MyHC-perinatal during skeletal muscle differentiation and regeneration. Loss of MyHC-perinatal function leads to enhanced differentiation characterized by increased expression of myogenic regulatory factors and differentiation index as well as reduced reserve cell numbers in vitro. Proteomic analysis revealed that loss of MyHC-perinatal function results in a switch from oxidative to glycolytic metabolism in myofibers, suggesting a shift from slow type I to fast type IIb fiber type, also supported by reduced mitochondrial numbers. Paracrine signals mediate the effect of loss of MyHC-perinatal function on myogenic differentiation, possibly mediated by non-apoptotic caspase-3 signaling along with enhanced levels of the pro-survival apoptosis regulator Bcl2 and nuclear factor kappa-B (NF-κB). Knockdown of MyHC-perinatal during muscle regeneration in vivo results in increased expression of the differentiation marker myogenin (MyoG) and impaired differentiation, evidenced by smaller myofibers, elevated fibrosis and reduction in the number of satellite cells. Thus, we find that MyHC-perinatal is a crucial regulator of myogenic differentiation, myofiber oxidative phenotype and regeneration.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Bcl-2 protein</subject><subject>Caspase</subject><subject>Caspase 3 - genetics</subject><subject>Caspase 3 - metabolism</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - genetics</subject><subject>Cells (biology)</subject><subject>Differentiation</subject><subject>Fibrosis</subject><subject>Glycolysis</subject><subject>Mice</subject><subject>Muscle Development - genetics</subject><subject>Muscle regulatory factor</subject><subject>Muscle, Skeletal - cytology</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Muscles</subject><subject>Musculoskeletal system</subject><subject>Myogenin</subject><subject>Myogenin - genetics</subject><subject>Myogenin - metabolism</subject><subject>Myosin</subject><subject>Myosin Heavy Chains - genetics</subject><subject>Myosin Heavy Chains - metabolism</subject><subject>Oxidation-Reduction</subject><subject>Oxidative metabolism</subject><subject>Paracrine signalling</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Proteomics</subject><subject>Regeneration</subject><subject>Regeneration - genetics</subject><subject>Satellite cells</subject><subject>Skeletal muscle</subject><issn>1742-464X</issn><issn>1742-4658</issn><issn>1742-4658</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNpdkUtLw0AUhQdRbK1u_AEScCNi6jwyyWQpxRdU3Ci4CzPJHTs1ncSZpJh_b9LWLrybe7h8HC7nIHRO8JT0c6tB-SlJsOAHaEySiIZRzMXhXkcfI3Ti_RJjxqM0PUYjJhgXmIkxKl-6yhsbLECuuyBfSGPDGpyxspFl4OCzLWUDPvBfUMJwWrU-LyEojNbgwDZGNqayN0H1Y4periGoF2CrpqshkLYYLMCC21Cn6EjL0sPZbk_Q-8P92-wpnL8-Ps_u5mFOk6gJqY4J1iwHpYSUmELOFeCIq7igQjNO47SggLVKciK5oKB4QaROpYBUyUizCbra-tau-m7BN9nK-BzKUlqoWp_RlCaURIylPXr5D11WrbP9dxnDSZ9WikXSU9dbKneV9w50Vjuzkq7LCM6GDrKhg2zTQQ9f7CxbtYJij_6Fzn4BHISFTA</recordid><startdate>20240701</startdate><enddate>20240701</enddate><creator>Sharma, Akashi</creator><creator>Zehra, Aatifa</creator><creator>Mathew, Sam J</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7908-6094</orcidid></search><sort><creationdate>20240701</creationdate><title>Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration</title><author>Sharma, Akashi ; Zehra, Aatifa ; Mathew, Sam J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c274t-2f610f3cebb8aa02ec5be045b6d28f35269d2e0fb7c1a582eb5d1af9a8e9ba4f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Bcl-2 protein</topic><topic>Caspase</topic><topic>Caspase 3 - genetics</topic><topic>Caspase 3 - metabolism</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - genetics</topic><topic>Cells (biology)</topic><topic>Differentiation</topic><topic>Fibrosis</topic><topic>Glycolysis</topic><topic>Mice</topic><topic>Muscle Development - genetics</topic><topic>Muscle regulatory factor</topic><topic>Muscle, Skeletal - cytology</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Muscles</topic><topic>Musculoskeletal system</topic><topic>Myogenin</topic><topic>Myogenin - genetics</topic><topic>Myogenin - metabolism</topic><topic>Myosin</topic><topic>Myosin Heavy Chains - genetics</topic><topic>Myosin Heavy Chains - metabolism</topic><topic>Oxidation-Reduction</topic><topic>Oxidative metabolism</topic><topic>Paracrine signalling</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Proteomics</topic><topic>Regeneration</topic><topic>Regeneration - genetics</topic><topic>Satellite cells</topic><topic>Skeletal muscle</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sharma, Akashi</creatorcontrib><creatorcontrib>Zehra, Aatifa</creatorcontrib><creatorcontrib>Mathew, Sam J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The FEBS journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sharma, Akashi</au><au>Zehra, Aatifa</au><au>Mathew, Sam J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration</atitle><jtitle>The FEBS journal</jtitle><addtitle>FEBS J</addtitle><date>2024-07-01</date><risdate>2024</risdate><volume>291</volume><issue>13</issue><spage>2836</spage><epage>2848</epage><pages>2836-2848</pages><issn>1742-464X</issn><issn>1742-4658</issn><eissn>1742-4658</eissn><abstract>Myosin heavy chain-perinatal (MyHC-perinatal) is one of two development-specific myosin heavy chains expressed exclusively during skeletal muscle development and regeneration. The specific functions of MyHC-perinatal are unclear, although mutations are known to lead to contracture syndromes such as Trismus-pseudocamptodactyly syndrome. Here, we characterize the functions of MyHC-perinatal during skeletal muscle differentiation and regeneration. Loss of MyHC-perinatal function leads to enhanced differentiation characterized by increased expression of myogenic regulatory factors and differentiation index as well as reduced reserve cell numbers in vitro. Proteomic analysis revealed that loss of MyHC-perinatal function results in a switch from oxidative to glycolytic metabolism in myofibers, suggesting a shift from slow type I to fast type IIb fiber type, also supported by reduced mitochondrial numbers. Paracrine signals mediate the effect of loss of MyHC-perinatal function on myogenic differentiation, possibly mediated by non-apoptotic caspase-3 signaling along with enhanced levels of the pro-survival apoptosis regulator Bcl2 and nuclear factor kappa-B (NF-κB). Knockdown of MyHC-perinatal during muscle regeneration in vivo results in increased expression of the differentiation marker myogenin (MyoG) and impaired differentiation, evidenced by smaller myofibers, elevated fibrosis and reduction in the number of satellite cells. Thus, we find that MyHC-perinatal is a crucial regulator of myogenic differentiation, myofiber oxidative phenotype and regeneration.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>38358038</pmid><doi>10.1111/febs.17085</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-7908-6094</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 1742-464X
ispartof The FEBS journal, 2024-07, Vol.291 (13), p.2836-2848
issn 1742-464X
1742-4658
1742-4658
language eng
recordid cdi_proquest_miscellaneous_2927214339
source Wiley-Blackwell Read & Publish Collection
subjects Animals
Apoptosis
Bcl-2 protein
Caspase
Caspase 3 - genetics
Caspase 3 - metabolism
Cell differentiation
Cell Differentiation - genetics
Cells (biology)
Differentiation
Fibrosis
Glycolysis
Mice
Muscle Development - genetics
Muscle regulatory factor
Muscle, Skeletal - cytology
Muscle, Skeletal - metabolism
Muscles
Musculoskeletal system
Myogenin
Myogenin - genetics
Myogenin - metabolism
Myosin
Myosin Heavy Chains - genetics
Myosin Heavy Chains - metabolism
Oxidation-Reduction
Oxidative metabolism
Paracrine signalling
Phenotype
Phenotypes
Proteomics
Regeneration
Regeneration - genetics
Satellite cells
Skeletal muscle
title Myosin heavy chain-perinatal regulates skeletal muscle differentiation, oxidative phenotype and regeneration
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T23%3A45%3A18IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Myosin%20heavy%20chain-perinatal%20regulates%20skeletal%20muscle%20differentiation,%20oxidative%20phenotype%20and%20regeneration&rft.jtitle=The%20FEBS%20journal&rft.au=Sharma,%20Akashi&rft.date=2024-07-01&rft.volume=291&rft.issue=13&rft.spage=2836&rft.epage=2848&rft.pages=2836-2848&rft.issn=1742-464X&rft.eissn=1742-4658&rft_id=info:doi/10.1111/febs.17085&rft_dat=%3Cproquest_cross%3E2927214339%3C/proquest_cross%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c274t-2f610f3cebb8aa02ec5be045b6d28f35269d2e0fb7c1a582eb5d1af9a8e9ba4f3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3074999087&rft_id=info:pmid/38358038&rfr_iscdi=true