Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles

Skeletal muscle growth and maintenance depend on two tightly regulated processes, myogenesis and muscle regeneration. Both processes involve a series of crucial regulatory molecules including muscle-specific microRNAs, known as myomiRs. We recently showed that four myomiRs, miR-1, miR-133a, miR-133b...

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Autores principales: Chrystalla Mytidou, Andrie Koutsoulidou, Margarita Zachariou, Marianna Prokopi, Konstantinos Kapnisis, George M. Spyrou, Andreas Anayiotos, Leonidas A. Phylactou
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:86f3128605ab452590a0feba08a9e1c52021-11-18T09:20:07ZAge-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles1664-042X10.3389/fphys.2021.708278https://doaj.org/article/86f3128605ab452590a0feba08a9e1c52021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fphys.2021.708278/fullhttps://doaj.org/toc/1664-042XSkeletal muscle growth and maintenance depend on two tightly regulated processes, myogenesis and muscle regeneration. Both processes involve a series of crucial regulatory molecules including muscle-specific microRNAs, known as myomiRs. We recently showed that four myomiRs, miR-1, miR-133a, miR-133b, and miR-206, are encapsulated within muscle-derived exosomes and participate in local skeletal muscle communication. Although these four myomiRs have been extensively studied for their function in muscles, no information exists regarding their endogenous and exosomal levels across age. Here we aimed to identify any age-related changes in the endogenous and muscle-derived exosomal myomiR levels during acute skeletal muscle growth. The four endogenous and muscle-derived myomiRs were investigated in five skeletal muscles (extensor digitorum longus, soleus, tibialis anterior, gastrocnemius, and quadriceps) of 2-week–1-year-old wild-type male mice. The expression of miR-1, miR-133a, and miR-133b was found to increase rapidly until adolescence in all skeletal muscles, whereas during adulthood it remained relatively stable. By contrast, endogenous miR-206 levels were observed to decrease with age in all muscles, except for soleus. Differential expression of the four myomiRs is also inversely reflected on the production of two protein targets; serum response factor and connexin 43. Muscle-derived exosomal miR-1, miR-133a, and miR-133b levels were found to increase until the early adolescence, before reaching a plateau phase. Soleus was found to be the only skeletal muscle to release exosomes enriched in miR-206. In this study, we showed for the first time an in-depth longitudinal analysis of the endogenous and exosomal levels of the four myomiRs during skeletal muscle development. We showed that the endogenous expression and extracellular secretion of the four myomiRs are associated to the function and size of skeletal muscles as the mice age. Overall, our findings provide new insights for the myomiRs’ significant role in the first year of life in mice.Chrystalla MytidouChrystalla MytidouAndrie KoutsoulidouAndrie KoutsoulidouMargarita ZachariouMargarita ZachariouMarianna ProkopiMarianna ProkopiKonstantinos KapnisisGeorge M. SpyrouGeorge M. SpyrouAndreas AnayiotosLeonidas A. PhylactouLeonidas A. PhylactouFrontiers Media S.A.articleskeletal musclemuscle endogenousmuscle-derived exosomesagemyomiRsdifferential expressionPhysiologyQP1-981ENFrontiers in Physiology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic skeletal muscle
muscle endogenous
muscle-derived exosomes
age
myomiRs
differential expression
Physiology
QP1-981
spellingShingle skeletal muscle
muscle endogenous
muscle-derived exosomes
age
myomiRs
differential expression
Physiology
QP1-981
Chrystalla Mytidou
Chrystalla Mytidou
Andrie Koutsoulidou
Andrie Koutsoulidou
Margarita Zachariou
Margarita Zachariou
Marianna Prokopi
Marianna Prokopi
Konstantinos Kapnisis
George M. Spyrou
George M. Spyrou
Andreas Anayiotos
Leonidas A. Phylactou
Leonidas A. Phylactou
Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
description Skeletal muscle growth and maintenance depend on two tightly regulated processes, myogenesis and muscle regeneration. Both processes involve a series of crucial regulatory molecules including muscle-specific microRNAs, known as myomiRs. We recently showed that four myomiRs, miR-1, miR-133a, miR-133b, and miR-206, are encapsulated within muscle-derived exosomes and participate in local skeletal muscle communication. Although these four myomiRs have been extensively studied for their function in muscles, no information exists regarding their endogenous and exosomal levels across age. Here we aimed to identify any age-related changes in the endogenous and muscle-derived exosomal myomiR levels during acute skeletal muscle growth. The four endogenous and muscle-derived myomiRs were investigated in five skeletal muscles (extensor digitorum longus, soleus, tibialis anterior, gastrocnemius, and quadriceps) of 2-week–1-year-old wild-type male mice. The expression of miR-1, miR-133a, and miR-133b was found to increase rapidly until adolescence in all skeletal muscles, whereas during adulthood it remained relatively stable. By contrast, endogenous miR-206 levels were observed to decrease with age in all muscles, except for soleus. Differential expression of the four myomiRs is also inversely reflected on the production of two protein targets; serum response factor and connexin 43. Muscle-derived exosomal miR-1, miR-133a, and miR-133b levels were found to increase until the early adolescence, before reaching a plateau phase. Soleus was found to be the only skeletal muscle to release exosomes enriched in miR-206. In this study, we showed for the first time an in-depth longitudinal analysis of the endogenous and exosomal levels of the four myomiRs during skeletal muscle development. We showed that the endogenous expression and extracellular secretion of the four myomiRs are associated to the function and size of skeletal muscles as the mice age. Overall, our findings provide new insights for the myomiRs’ significant role in the first year of life in mice.
format article
author Chrystalla Mytidou
Chrystalla Mytidou
Andrie Koutsoulidou
Andrie Koutsoulidou
Margarita Zachariou
Margarita Zachariou
Marianna Prokopi
Marianna Prokopi
Konstantinos Kapnisis
George M. Spyrou
George M. Spyrou
Andreas Anayiotos
Leonidas A. Phylactou
Leonidas A. Phylactou
author_facet Chrystalla Mytidou
Chrystalla Mytidou
Andrie Koutsoulidou
Andrie Koutsoulidou
Margarita Zachariou
Margarita Zachariou
Marianna Prokopi
Marianna Prokopi
Konstantinos Kapnisis
George M. Spyrou
George M. Spyrou
Andreas Anayiotos
Leonidas A. Phylactou
Leonidas A. Phylactou
author_sort Chrystalla Mytidou
title Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
title_short Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
title_full Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
title_fullStr Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
title_full_unstemmed Age-Related Exosomal and Endogenous Expression Patterns of miR-1, miR-133a, miR-133b, and miR-206 in Skeletal Muscles
title_sort age-related exosomal and endogenous expression patterns of mir-1, mir-133a, mir-133b, and mir-206 in skeletal muscles
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/86f3128605ab452590a0feba08a9e1c5
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