Early satellite cell communication creates a permissive environment for long-term muscle growth
Summary: Using in vivo muscle stem cell (satellite cell)-specific extracellular vesicle (EV) tracking, satellite cell depletion, in vitro cell culture, and single-cell RNA sequencing, we show satellite cells communicate with other cells in skeletal muscle during mechanical overload. Early satellite...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2021-04-01
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| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004221003400 |
| _version_ | 1818715780571725824 |
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| author | Kevin A. Murach Bailey D. Peck Robert A. Policastro Ivan J. Vechetti Douglas W. Van Pelt Cory M. Dungan Lance T. Denes Xu Fu Camille R. Brightwell Gabriel E. Zentner Esther E. Dupont-Versteegden Christopher I. Richards Jeramiah J. Smith Christopher S. Fry John J. McCarthy Charlotte A. Peterson |
| author_facet | Kevin A. Murach Bailey D. Peck Robert A. Policastro Ivan J. Vechetti Douglas W. Van Pelt Cory M. Dungan Lance T. Denes Xu Fu Camille R. Brightwell Gabriel E. Zentner Esther E. Dupont-Versteegden Christopher I. Richards Jeramiah J. Smith Christopher S. Fry John J. McCarthy Charlotte A. Peterson |
| author_sort | Kevin A. Murach |
| collection | DOAJ |
| description | Summary: Using in vivo muscle stem cell (satellite cell)-specific extracellular vesicle (EV) tracking, satellite cell depletion, in vitro cell culture, and single-cell RNA sequencing, we show satellite cells communicate with other cells in skeletal muscle during mechanical overload. Early satellite cell EV communication primes the muscle milieu for proper long-term extracellular matrix (ECM) deposition and is sufficient to support sustained hypertrophy in adult mice, even in the absence of fusion to muscle fibers. Satellite cells modulate chemokine gene expression across cell types within the first few days of loading, and EV delivery of miR-206 to fibrogenic cells represses Wisp1 expression required for appropriate ECM remodeling. Late-stage communication from myogenic cells during loading is widespread but may be targeted toward endothelial cells. Satellite cells coordinate adaptation by influencing the phenotype of recipient cells, which extends our understanding of their role in muscle adaptation beyond regeneration and myonuclear donation. |
| first_indexed | 2024-12-17T19:08:48Z |
| format | Article |
| id | doaj.art-bf5d536bcc1c44ae96a88fbbda14f370 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-12-17T19:08:48Z |
| publishDate | 2021-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-bf5d536bcc1c44ae96a88fbbda14f3702022-12-21T21:35:56ZengElsevieriScience2589-00422021-04-01244102372Early satellite cell communication creates a permissive environment for long-term muscle growthKevin A. Murach0Bailey D. Peck1Robert A. Policastro2Ivan J. Vechetti3Douglas W. Van Pelt4Cory M. Dungan5Lance T. Denes6Xu Fu7Camille R. Brightwell8Gabriel E. Zentner9Esther E. Dupont-Versteegden10Christopher I. Richards11Jeramiah J. Smith12Christopher S. Fry13John J. McCarthy14Charlotte A. Peterson15The Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USADepartment of Biology, College of Arts and Sciences, University of Indiana, Bloomington, IN 47405, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY 40536, USA; Department of Nutrition and Health Sciences, College of Education and Human Sciences, University of Nebraska, Lincoln, NE 68588, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USADepartment of Molecular Genetics and Microbiology, Center for Neurogenetics, University of Florida, Gainesville, FL 32611, USADepartment of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY 40536, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Athletic Training, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USADepartment of Biology, College of Arts and Sciences, University of Indiana, Bloomington, IN 47405, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USADepartment of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY 40536, USADepartment of Biology, College of Arts and Sciences, University of Kentucky, Lexington, KY 40506, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Athletic Training, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USAThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY 40536, USA; Corresponding authorThe Center for Muscle Biology, University of Kentucky, Lexington, KY 40536, USA; Department of Physical Therapy, College of Health Sciences, University of Kentucky, Lexington, KY 40536, USA; Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY 40536, USA; Corresponding authorSummary: Using in vivo muscle stem cell (satellite cell)-specific extracellular vesicle (EV) tracking, satellite cell depletion, in vitro cell culture, and single-cell RNA sequencing, we show satellite cells communicate with other cells in skeletal muscle during mechanical overload. Early satellite cell EV communication primes the muscle milieu for proper long-term extracellular matrix (ECM) deposition and is sufficient to support sustained hypertrophy in adult mice, even in the absence of fusion to muscle fibers. Satellite cells modulate chemokine gene expression across cell types within the first few days of loading, and EV delivery of miR-206 to fibrogenic cells represses Wisp1 expression required for appropriate ECM remodeling. Late-stage communication from myogenic cells during loading is widespread but may be targeted toward endothelial cells. Satellite cells coordinate adaptation by influencing the phenotype of recipient cells, which extends our understanding of their role in muscle adaptation beyond regeneration and myonuclear donation.http://www.sciencedirect.com/science/article/pii/S2589004221003400Cell BiologyFunctional Aspects of Cell Biology |
| spellingShingle | Kevin A. Murach Bailey D. Peck Robert A. Policastro Ivan J. Vechetti Douglas W. Van Pelt Cory M. Dungan Lance T. Denes Xu Fu Camille R. Brightwell Gabriel E. Zentner Esther E. Dupont-Versteegden Christopher I. Richards Jeramiah J. Smith Christopher S. Fry John J. McCarthy Charlotte A. Peterson Early satellite cell communication creates a permissive environment for long-term muscle growth iScience Cell Biology Functional Aspects of Cell Biology |
| title | Early satellite cell communication creates a permissive environment for long-term muscle growth |
| title_full | Early satellite cell communication creates a permissive environment for long-term muscle growth |
| title_fullStr | Early satellite cell communication creates a permissive environment for long-term muscle growth |
| title_full_unstemmed | Early satellite cell communication creates a permissive environment for long-term muscle growth |
| title_short | Early satellite cell communication creates a permissive environment for long-term muscle growth |
| title_sort | early satellite cell communication creates a permissive environment for long term muscle growth |
| topic | Cell Biology Functional Aspects of Cell Biology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004221003400 |
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