Muscle atrophy‐related myotube‐derived exosomal microRNA in neuronal dysfunction: Targeting both coding and long noncoding RNAs

In mammals, microRNAs can be actively secreted from cells to blood. miR‐29b‐3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR‐29b‐3p was upregulated in normal and premature aging mouse muscle and plasm...

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Published inAging cell Vol. 19; no. 5; pp. e13107 - n/a
Main Authors Yang, Chia‐Pei, Yang, Wan‐Shan, Wong, Yu‐Hui, Wang, Kai‐Hsuan, Teng, Yuan‐Chi, Chang, Ming‐Hsuan, Liao, Ko‐Hsun, Nian, Fang‐Shin, Chao, Chuan‐Chuan, Tsai, Jin‐Wu, Hwang, Wei‐Lun, Lin, Ming‐Wei, Tzeng, Tsai‐Yu, Wang, Pei‐Ning, Campbell, Mel, Chen, Liang‐Kung, Tsai, Ting‐Fen, Chang, Pei‐Ching, Kung, Hsing‐Jien
Format Journal Article Web Resource
LanguageEnglish
Published England John Wiley & Sons, Inc 01.05.2020
Blackwell Publishing Ltd
John Wiley and Sons Inc
Subjects
Aging
Animals
Atrophy
Biomarkers
Cell Biology
Cell Differentiation
Cell interactions
Cell signaling
Cells, Cultured
Cellular Senescence
Communication
Exosomes
Exosomes/metabolism
Genetics & genetic processes
Génétique & processus génétiques
HIF-1α-AS2
Human subjects
Humans
Life sciences
lncRNAs
Mice
MicroRNAs
MicroRNAs/genetics
miR-29b-3p
MIRN29 microRNA, mouse
miRNA
muscle atrophy
Muscle Fibers, Skeletal
Muscle Fibers, Skeletal/metabolism
Muscular Atrophy
Muscular Atrophy/metabolism
Musculoskeletal system
Myogenesis
Myotubes
Neurons
Neurons/metabolism
Non-coding RNA
Original
Plasma
Proteins
RNA, Long Noncoding
RNA, Long Noncoding/genetics
RNA, Messenger
RNA, Messenger/genetics
Sarcopenia
Sciences du vivant
Skeletal muscle
lncRNAs
aging
muscle atrophy
miR-29b-3p
HIF-1α-AS2
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Abstract In mammals, microRNAs can be actively secreted from cells to blood. miR‐29b‐3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR‐29b‐3p was upregulated in normal and premature aging mouse muscle and plasma. miR‐29b‐3p was also upregulated in the blood of aging individuals, and circulating levels of miR‐29b‐3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR‐29b‐3p was observed in exosomes isolated from long‐term differentiated atrophic C2C12 cells. When C2C12‐derived miR‐29b‐3p‐containing exosomes were uptaken by neuronal SH‐SY5Y cells, increased miR‐29b‐3p levels in recipient cells were observed. Moreover, miR‐29b‐3p overexpression led to downregulation of neuronal‐related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α‐AS2 as a novel c‐FOS targeting lncRNA that is induced by miR‐29b‐3p through down‐modulation of c‐FOS and is required for miR‐29b‐3p‐mediated neuronal differentiation inhibition. Our results suggest that atrophy‐associated circulating miR‐29b‐3p may mediate distal communication between muscle cells and neurons. miR‐29b‐3p‐containing exosomes released from atrophied muscle can be transported via the circulation and transferred to neuronal cells. Increased miR‐29b‐3p levels in neuronal cells may lead to inhibition of neuronal differentiation.
AbstractList In mammals, microRNAs can be actively secreted from cells to blood. miR‐29b‐3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR‐29b‐3p was upregulated in normal and premature aging mouse muscle and plasma. miR‐29b‐3p was also upregulated in the blood of aging individuals, and circulating levels of miR‐29b‐3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR‐29b‐3p was observed in exosomes isolated from long‐term differentiated atrophic C2C12 cells. When C2C12‐derived miR‐29b‐3p‐containing exosomes were uptaken by neuronal SH‐SY5Y cells, increased miR‐29b‐3p levels in recipient cells were observed. Moreover, miR‐29b‐3p overexpression led to downregulation of neuronal‐related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α‐AS2 as a novel c‐FOS targeting lncRNA that is induced by miR‐29b‐3p through down‐modulation of c‐FOS and is required for miR‐29b‐3p‐mediated neuronal differentiation inhibition. Our results suggest that atrophy‐associated circulating miR‐29b‐3p may mediate distal communication between muscle cells and neurons.
In mammals, microRNAs can be actively secreted from cells to blood. miR‐29b‐3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR‐29b‐3p was upregulated in normal and premature aging mouse muscle and plasma. miR‐29b‐3p was also upregulated in the blood of aging individuals, and circulating levels of miR‐29b‐3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR‐29b‐3p was observed in exosomes isolated from long‐term differentiated atrophic C2C12 cells. When C2C12‐derived miR‐29b‐3p‐containing exosomes were uptaken by neuronal SH‐SY5Y cells, increased miR‐29b‐3p levels in recipient cells were observed. Moreover, miR‐29b‐3p overexpression led to downregulation of neuronal‐related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α‐AS2 as a novel c‐FOS targeting lncRNA that is induced by miR‐29b‐3p through down‐modulation of c‐FOS and is required for miR‐29b‐3p‐mediated neuronal differentiation inhibition. Our results suggest that atrophy‐associated circulating miR‐29b‐3p may mediate distal communication between muscle cells and neurons. miR‐29b‐3p‐containing exosomes released from atrophied muscle can be transported via the circulation and transferred to neuronal cells. Increased miR‐29b‐3p levels in neuronal cells may lead to inhibition of neuronal differentiation.
In mammals, microRNAs can be actively secreted from cells to blood. miR-29b-3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR-29b-3p was upregulated in normal and premature aging mouse muscle and plasma. miR-29b-3p was also upregulated in the blood of aging individuals, and circulating levels of miR-29b-3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR-29b-3p was observed in exosomes isolated from long-term differentiated atrophic C2C12 cells. When C2C12-derived miR-29b-3p-containing exosomes were uptaken by neuronal SH-SY5Y cells, increased miR-29b-3p levels in recipient cells were observed. Moreover, miR-29b-3p overexpression led to downregulation of neuronal-related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α-AS2 as a novel c-FOS targeting lncRNA that is induced by miR-29b-3p through down-modulation of c-FOS and is required for miR-29b-3p-mediated neuronal differentiation inhibition. Our results suggest that atrophy-associated circulating miR-29b-3p may mediate distal communication between muscle cells and neurons.
In mammals, microRNAs can be actively secreted from cells to blood. miR-29b-3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR-29b-3p was upregulated in normal and premature aging mouse muscle and plasma. miR-29b-3p was also upregulated in the blood of aging individuals, and circulating levels of miR-29b-3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR-29b-3p was observed in exosomes isolated from long-term differentiated atrophic C2C12 cells. When C2C12-derived miR-29b-3p-containing exosomes were uptaken by neuronal SH-SY5Y cells, increased miR-29b-3p levels in recipient cells were observed. Moreover, miR-29b-3p overexpression led to downregulation of neuronal-related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α-AS2 as a novel c-FOS targeting lncRNA that is induced by miR-29b-3p through down-modulation of c-FOS and is required for miR-29b-3p-mediated neuronal differentiation inhibition. Our results suggest that atrophy-associated circulating miR-29b-3p may mediate distal communication between muscle cells and neurons.In mammals, microRNAs can be actively secreted from cells to blood. miR-29b-3p has been shown to play a pivotal role in muscle atrophy, but its role in intercellular communication is largely unknown. Here, we showed that miR-29b-3p was upregulated in normal and premature aging mouse muscle and plasma. miR-29b-3p was also upregulated in the blood of aging individuals, and circulating levels of miR-29b-3p were negatively correlated with relative appendicular skeletal muscle. Consistently, miR-29b-3p was observed in exosomes isolated from long-term differentiated atrophic C2C12 cells. When C2C12-derived miR-29b-3p-containing exosomes were uptaken by neuronal SH-SY5Y cells, increased miR-29b-3p levels in recipient cells were observed. Moreover, miR-29b-3p overexpression led to downregulation of neuronal-related genes and inhibition of neuronal differentiation. Interestingly, we identified HIF1α-AS2 as a novel c-FOS targeting lncRNA that is induced by miR-29b-3p through down-modulation of c-FOS and is required for miR-29b-3p-mediated neuronal differentiation inhibition. Our results suggest that atrophy-associated circulating miR-29b-3p may mediate distal communication between muscle cells and neurons.
Author Nian, Fang‐Shin
Yang, Chia‐Pei
Tsai, Jin‐Wu
Wang, Pei‐Ning
Chen, Liang‐Kung
Liao, Ko‐Hsun
Campbell, Mel
Wong, Yu‐Hui
Chang, Ming‐Hsuan
Teng, Yuan‐Chi
Yang, Wan‐Shan
Hwang, Wei‐Lun
Kung, Hsing‐Jien
Tzeng, Tsai‐Yu
Lin, Ming‐Wei
Tsai, Ting‐Fen
Wang, Kai‐Hsuan
Chao, Chuan‐Chuan
Chang, Pei‐Ching
AuthorAffiliation 10 Institute of Public Health National Yang‐Ming University Taipei Taiwan
11 Cancer Progression Research Center National Yang‐Ming University Taipei Taiwan
5 Department of Life Sciences Institute of Genome Sciences National Yang‐Ming University Taipei Taiwan
14 UC Davis Comprehensive Cancer Center University of California Davis CA USA
15 Department of Geriatric Medicine School of Medicine National Yang Ming University Taipei Taiwan
7 Program in Molecular Medicine National Yang‐Ming University and Academia Sinica Taipei Taiwan
1 Institute of Microbiology and Immunology National Yang‐Ming University Taipei Taiwan
13 Aging and Health Research Center National Yang‐Ming University Taipei Taiwan
16 Center for Geriatrics and Gerontology Taipei Veterans General Hospital Taipei Taiwan
3 Institute of Molecular and Genomic Medicine National Health Research Institutes Zhunan Taiwan
9 Department of Biotechnology and Laboratory Science in Medicine National Yang‐Ming University Taipei Taiwan
8 The Ph.D. Program
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32233025$$D View this record in MEDLINE/PubMed
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2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Copyright_xml – notice: 2020 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd.
– notice: 2020 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.
– notice: 2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Issue 5
Keywords lncRNAs
aging
muscle atrophy
miR-29b-3p
HIF-1α-AS2
Language English
License Attribution
2020 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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content type line 14
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scopus-id:2-s2.0-85082619033
Chia‐Pei Yang, Wan‐Shan Yang and Yu‐Hui Wong equally contributed to this work.
ORCID 0000-0001-8665-5494
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Snippet In mammals, microRNAs can be actively secreted from cells to blood. miR‐29b‐3p has been shown to play a pivotal role in muscle atrophy, but its role in...
In mammals, microRNAs can be actively secreted from cells to blood. miR-29b-3p has been shown to play a pivotal role in muscle atrophy, but its role in...
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liege
proquest
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SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage e13107
SubjectTerms Aging
Animals
Atrophy
Biomarkers
Cell Biology
Cell Differentiation
Cell interactions
Cell signaling
Cells, Cultured
Cellular Senescence
Communication
Exosomes
Exosomes/metabolism
Genetics & genetic processes
Génétique & processus génétiques
HIF-1α-AS2
Human subjects
Humans
Life sciences
lncRNAs
Mice
MicroRNAs
MicroRNAs/genetics
miR-29b-3p
MIRN29 microRNA, mouse
miRNA
muscle atrophy
Muscle Fibers, Skeletal
Muscle Fibers, Skeletal/metabolism
Muscular Atrophy
Muscular Atrophy/metabolism
Musculoskeletal system
Myogenesis
Myotubes
Neurons
Neurons/metabolism
Non-coding RNA
Original
Plasma
Proteins
RNA, Long Noncoding
RNA, Long Noncoding/genetics
RNA, Messenger
RNA, Messenger/genetics
Sarcopenia
Sciences du vivant
Skeletal muscle
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Title Muscle atrophy‐related myotube‐derived exosomal microRNA in neuronal dysfunction: Targeting both coding and long noncoding RNAs
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Facel.13107
https://www.ncbi.nlm.nih.gov/pubmed/32233025
https://www.proquest.com/docview/2406993994
https://www.proquest.com/docview/2544349155
https://www.proquest.com/docview/2385270001
http://orbi.ulg.ac.be/handle/2268/330653
https://pubmed.ncbi.nlm.nih.gov/PMC7253071
Volume 19
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