Muscle Regeneration with Intermuscular Adipose Tissue (IMAT) Accumulation Is Modulated by Mechanical Constraints

Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study was designed to investigate whether hypoactivity would influence IMAT accumulation in regenerating mouse skeletal muscle using the glycerol m...

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Veröffentlicht in:	PloS one Jg. 10; H. 12; S. e0144230
Hauptverfasser:	Pagano, Allan F., Demangel, Rémi, Brioche, Thomas, Jublanc, Elodie, Bertrand-Gaday, Christelle, Candau, Robin, Dechesne, Claude A., Dani, Christian, Bonnieu, Anne, Py, Guillaume, Chopard, Angèle
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 02.12.2015 Public Library of Science (PLoS)
Schlagworte:	Accumulation Adipocytes Adipocytes - metabolism Adipocytes - physiology Adipogenesis Adipogenesis - physiology Adipose tissue Adipose Tissue - metabolism Adipose Tissue - physiology Analysis Animals Apoptosis Bioaccumulation Body fat Body weight CCAAT-Enhancer-Binding Proteins - metabolism Cell surface Experiments Fibrosis Gene expression Genes Glycerol Hindlimb Suspension - physiology Injection Laboratory animals Life Sciences Markers Mechanical unloading Mice Microgravity mRNA Muscle function Muscle, Skeletal - metabolism Muscle, Skeletal - physiology Muscles Muscular dystrophy Musculoskeletal system Physiology PPAR gamma - metabolism Recruitment Regeneration Regeneration - physiology RNA RNA, Messenger - metabolism Rodents Skeletal muscle Soleus muscle Stem cells Studies Surface markers Trauma Unloading muscle regénération musculaire
ISSN:	1932-6203, 1932-6203
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Abstract	Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study was designed to investigate whether hypoactivity would influence IMAT accumulation in regenerating mouse skeletal muscle using the glycerol model of muscle regeneration. The animals were immediately hindlimb unloaded for 21 days after glycerol injection into the tibialis anterior (TA) muscle. Muscle fiber and adipocyte cross-sectional area (CSA) and IMAT accumulation were determined by histomorphometric analysis. Adipogenesis during regenerative processes was examined using RT-qPCR and Western blot quantification. Twenty-one days of hindlimb unloading resulted in decreases of 38% and 50.6% in the muscle weight/body weight ratio and CSA, respectively, in soleus muscle. Glycerol injection into TA induced IMAT accumulation, reaching 3% of control normal-loading muscle area. This IMAT accumulation was largely inhibited in unloading conditions (0.09%) and concomitant with a marked reduction in perilipin and FABP4 protein content, two key markers of mature adipocytes. Induction of PPARγ and C/EBPα mRNA, two markers of adipogenesis, was also decreased. Furthermore, the protein expression of PDGFRα, a cell surface marker of fibro/adipogenic progenitors, was much lower in regenerating TA from the unloaded group. Exposure of regenerating muscle to hypoactivity severely reduces IMAT development and accumulation. These results provide new insight into the mechanisms regulating IMAT development in skeletal muscle and highlight the importance of taking into account the level of mechanical constraint imposed on skeletal muscle during the regeneration processes.
AbstractList	Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study was designed to investigate whether hypoactivity would influence IMAT accumulation in regenerating mouse skeletal muscle using the glycerol model of muscle regeneration. The animals were immediately hindlimb unloaded for 21 days after glycerol injection into the tibialis anterior (TA) muscle. Muscle fiber and adipocyte cross-sectional area (CSA) and IMAT accumulation were determined by histomorphometric analysis. Adipogenesis during regenerative processes was examined using RT-qPCR and Western blot quantification. Twenty-one days of hindlimb unloading resulted in decreases of 38% and 50.6% in the muscle weight/body weight ratio and CSA, respectively, in soleus muscle. Glycerol injection into TA induced IMAT accumulation, reaching 3% of control normal-loading muscle area. This IMAT accumulation was largely inhibited in unloading conditions (0.09%) and concomitant with a marked reduction in perilipin and FABP4 protein content, two key markers of mature adipocytes. Induction of PPARγ and C/EBPα mRNA, two markers of adipogenesis, was also decreased. Furthermore, the protein expression of PDGFRα, a cell surface marker of fibro/adipogenic progenitors, was much lower in regenerating TA from the unloaded group. Exposure of regenerating muscle to hypoactivity severely reduces IMAT development and accumulation. These results provide new insight into the mechanisms regulating IMAT development in skeletal muscle and highlight the importance of taking into account the level of mechanical constraint imposed on skeletal muscle during the regeneration processes. Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study was designed to investigate whether hypoactivity would influence IMAT accumulation in regenerating mouse skeletal muscle using the glycerol model of muscle regeneration. The animals were immediately hindlimb unloaded for 21 days after glycerol injection into the tibialis anterior (TA) muscle. Muscle fiber and adipocyte cross-sectional area (CSA) and IMAT accumulation weredetermined by histomorphometric analysis. Adipogenesis during regenerative processes was examined using RT-qPCR and Western blot quantification. Twenty-one days of hindlimb unloading resulted in decreases of 38% and 50.6% in the muscle weight/body weight ratio and CSA, respectively, in soleus muscle. Glycerol injection into TA induced IMAT accumulation, reaching 3% of control normal-loading muscle area. This IMAT accumulationwas largely inhibited in unloading conditions (0.09%) and concomitant with a marked reduction in perilipin and FABP4 protein content, two key markers of mature adipocytes. Induction of PPARγ and C/EBPα mRNA, two markers of adipogenesis, was also decreased. Furthermore, the protein expression of PDGFRα, a cell surface marker of fibro/adipogenic progenitors, was much lower in regenerating TA from the unloaded group. Exposure ofregenerating muscle to hypoactivity severely reduces IMAT development and accumulation. These results provide new insight into the mechanisms regulating IMAT development in skeletal muscle and highlight the importance of taking into account the level of mechanical constraint imposed on skeletal muscle during the regeneration processes. Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study was designed to investigate whether hypoactivity would influence IMAT accumulation in regenerating mouse skeletal muscle using the glycerol model of muscle regeneration. The animals were immediately hindlimb unloaded for 21 days after glycerol injection into the tibialis anterior (TA) muscle. Muscle fiber and adipocyte cross-sectional area (CSA) and IMAT accumulation were determined by histomorphometric analysis. Adipogenesis during regenerative processes was examined using RT-qPCR and Western blot quantification. Twenty-one days of hindlimb unloading resulted in decreases of 38% and 50.6% in the muscle weight/body weight ratio and CSA, respectively, in soleus muscle. Glycerol injection into TA induced IMAT accumulation, reaching 3% of control normal-loading muscle area. This IMAT accumulation was largely inhibited in unloading conditions (0.09%) and concomitant with a marked reduction in perilipin and FABP4 protein content, two key markers of mature adipocytes. Induction of PPAR[gamma] and C/EBP[alpha] mRNA, two markers of adipogenesis, was also decreased. Furthermore, the protein expression of PDGFR[alpha], a cell surface marker of fibro/adipogenic progenitors, was much lower in regenerating TA from the unloaded group. Exposure of regenerating muscle to hypoactivity severely reduces IMAT development and accumulation. These results provide new insight into the mechanisms regulating IMAT development in skeletal muscle and highlight the importance of taking into account the level of mechanical constraint imposed on skeletal muscle during the regeneration processes.
Audience	Academic
Author	Dechesne, Claude A. Pagano, Allan F. Brioche, Thomas Dani, Christian Chopard, Angèle Candau, Robin Bertrand-Gaday, Christelle Py, Guillaume Demangel, Rémi Jublanc, Elodie Bonnieu, Anne
AuthorAffiliation	2 Université Nice-Sophia Antipolis, iBV, CNRS UMR7277, INSERM U1091, 06107, Nice, France West Virginia University School of Medicine, UNITED STATES 1 Université de Montpellier, INRA, UMR866 Dynamique Musculaire et Métabolisme, F-34060, Montpellier, France
AuthorAffiliation_xml	– name: 2 Université Nice-Sophia Antipolis, iBV, CNRS UMR7277, INSERM U1091, 06107, Nice, France – name: 1 Université de Montpellier, INRA, UMR866 Dynamique Musculaire et Métabolisme, F-34060, Montpellier, France – name: West Virginia University School of Medicine, UNITED STATES
Author_xml	– sequence: 1 givenname: Allan F. surname: Pagano fullname: Pagano, Allan F. – sequence: 2 givenname: Rémi surname: Demangel fullname: Demangel, Rémi – sequence: 3 givenname: Thomas surname: Brioche fullname: Brioche, Thomas – sequence: 4 givenname: Elodie surname: Jublanc fullname: Jublanc, Elodie – sequence: 5 givenname: Christelle surname: Bertrand-Gaday fullname: Bertrand-Gaday, Christelle – sequence: 6 givenname: Robin surname: Candau fullname: Candau, Robin – sequence: 7 givenname: Claude A. surname: Dechesne fullname: Dechesne, Claude A. – sequence: 8 givenname: Christian surname: Dani fullname: Dani, Christian – sequence: 9 givenname: Anne surname: Bonnieu fullname: Bonnieu, Anne – sequence: 10 givenname: Guillaume surname: Py fullname: Py, Guillaume – sequence: 11 givenname: Angèle surname: Chopard fullname: Chopard, Angèle
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: AFP RD AC TB GP CD CAD. Performed the experiments: AFP RD GP TB. Analyzed the data: AFP RD GP AC AB. Contributed reagents/materials/analysis tools: AFP RD AC GP EJ CBG. Wrote the paper: AFP GP AC. Manuscript revision and feedback: AFP AC GP CD CAD RC AB. Competing Interests: The authors have declared that no competing interests exist. These authors also contributed equally to this work.
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Snippet	Sports trauma are able to induce muscle injury with fibrosis and accumulation of intermuscular adipose tissue (IMAT), which affect muscle function. This study...
SourceID	plos doaj pubmedcentral hal proquest gale pubmed crossref
SourceType	Open Website Open Access Repository Aggregation Database Index Database Enrichment Source
StartPage	e0144230
SubjectTerms	Accumulation Adipocytes Adipocytes - metabolism Adipocytes - physiology Adipogenesis Adipogenesis - physiology Adipose tissue Adipose Tissue - metabolism Adipose Tissue - physiology Analysis Animals Apoptosis Bioaccumulation Body fat Body weight CCAAT-Enhancer-Binding Proteins - metabolism Cell surface Experiments Fibrosis Gene expression Genes Glycerol Hindlimb Suspension - physiology Injection Laboratory animals Life Sciences Markers Mechanical unloading Mice Microgravity mRNA Muscle function Muscle, Skeletal - metabolism Muscle, Skeletal - physiology Muscles Muscular dystrophy Musculoskeletal system Physiology PPAR gamma - metabolism Recruitment Regeneration Regeneration - physiology RNA RNA, Messenger - metabolism Rodents Skeletal muscle Soleus muscle Stem cells Studies Surface markers Trauma Unloading
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Title	Muscle Regeneration with Intermuscular Adipose Tissue (IMAT) Accumulation Is Modulated by Mechanical Constraints
URI	https://www.ncbi.nlm.nih.gov/pubmed/26629696 https://www.proquest.com/docview/1738753110 https://www.proquest.com/docview/1744662659 https://hal.science/hal-01837620 https://pubmed.ncbi.nlm.nih.gov/PMC4668059 https://doaj.org/article/bc0159d62f944d5dbd81fed18e8c3dca http://dx.doi.org/10.1371/journal.pone.0144230
Volume	10
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