Early satellite cell communication creates a permissive environment for long-term muscle growth

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

doi:10.1016/j.isci.2021.102372

Early satellite cell communication creates a permissive environment for long-term muscle growth

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

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

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.

Original language	English
Article number	102372
Journal	iScience
Volume	24
Issue number	4
DOIs	https://doi.org/10.1016/j.isci.2021.102372
State	Published - Apr 23 2021

Bibliographical note

Publisher Copyright:
© 2021 The Authors

Funding

The authors wish to thank Jennifer Strange of the University of Kentucky Flow Cytometry Core and Dr. Doug Harrison of the University of Kentucky Biology Department/Genetics and Genomics Imaging Center for their technical expertise with fluorescent activated cell sorting and single-cell RNA sequencing, respectively. Partial computational support was provided by the University of Kentucky High Performance Computing complex. The authors thank Dr. Ferdinand von Walden for providing mice for this study, Dr. Yuan Wen for his technical expertise, and Dr. Eric Wang for providing resources. This work was supported by funding from the NIH National Institutes of Arthritis and Musculoskeletal and Skin Diseases (AR060701 to C.A.P. and J.J.M. and AR071753 to K.A.M), National Institute on Aging (AG049086 to C.A.P. and J.J.M. and AG063994 to K.A.M), National Institute of Diabetes and Digestive and Kidney Diseases (DK119619 to C.A.P. and J.J.M), and National Institute of General Medical Sciences (GM130349 to J.J.S.), K.A.M. C.S.F. C.A.P. and J.J.M. designed experiments. K.A.M. B.D.P. D.W.V.P. L.T.D. I.J.V. B.D.P. C.M.D. C.R.B. C.S.F. X.F. and C.I.R. performed experiments. K.A.M. B.D.P. R.A.P. D.W.V.P. I.J.V. B.D.P. C.R.B. X.F. C.I.R. and J.J.S. analyzed data. G.E.Z. and E.E.D.-V. provided resources. K.A.M wrote the manuscript and prepared the figures. C.A.P. and J.J.M. provided funding support and supervised the study. C.A.P. J.J.M. and R.A.P. assisted with data interpretation and manuscript writing. All authors edited and approved the final manuscript. The authors have no conflicts to declare. The authors wish to thank Jennifer Strange of the University of Kentucky Flow Cytometry Core and Dr. Doug Harrison of the University of Kentucky Biology Department/Genetics and Genomics Imaging Center for their technical expertise with fluorescent activated cell sorting and single-cell RNA sequencing, respectively. Partial computational support was provided by the University of Kentucky High Performance Computing complex. The authors thank Dr. Ferdinand von Walden for providing mice for this study, Dr. Yuan Wen for his technical expertise, and Dr. Eric Wang for providing resources. This work was supported by funding from the NIH National Institutes of Arthritis and Musculoskeletal and Skin Diseases ( AR060701 to C.A.P. and J.J.M. and AR071753 to K.A.M), National Institute on Aging ( AG049086 to C.A.P. and J.J.M. and AG063994 to K.A.M), National Institute of Diabetes and Digestive and Kidney Diseases ( DK119619 to C.A.P. and J.J.M), and National Institute of General Medical Sciences ( GM130349 to J.J.S.)

Funders	Funder number
University of Kentucky Biology Department/Genetics
National Institute on Aging	AG049086, AG063994
National Institute of General Medical Sciences	GM130349
National Institute of Diabetes and Digestive and Kidney Diseases	DK119619
National Institute of Arthritis and Musculoskeletal and Skin Diseases	AR060701, AR071753
University of Kentucky

Keywords

Cell Biology
Functional Aspects of Cell Biology

ASJC Scopus subject areas

General

Access to Document

10.1016/j.isci.2021.102372

Cite this

Murach, K. A., Peck, B. D., Policastro, R. A., Vechetti, I. J., Van Pelt, D. W., Dungan, C. M., Denes, L. T., Fu, X., Brightwell, C. R., Zentner, G. E., Dupont-Versteegden, E. E., Richards, C. I., Smith, J. J., Fry, C. S., McCarthy, J. J., & Peterson, C. A. (2021). Early satellite cell communication creates a permissive environment for long-term muscle growth. iScience, 24(4), Article 102372. https://doi.org/10.1016/j.isci.2021.102372

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abstract = "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.",

keywords = "Cell Biology, Functional Aspects of Cell Biology",

author = "Murach, {Kevin A.} and Peck, {Bailey D.} and Policastro, {Robert A.} and Vechetti, {Ivan J.} and {Van Pelt}, {Douglas W.} and Dungan, {Cory M.} and Denes, {Lance T.} and Xu Fu and Brightwell, {Camille R.} and Zentner, {Gabriel E.} and Dupont-Versteegden, {Esther E.} and Richards, {Christopher I.} and Smith, {Jeramiah J.} and Fry, {Christopher S.} and McCarthy, {John J.} and Peterson, {Charlotte A.}",

note = "Publisher Copyright: {\textcopyright} 2021 The Authors",

year = "2021",

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doi = "10.1016/j.isci.2021.102372",

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Murach, KA, Peck, BD, Policastro, RA, Vechetti, IJ, Van Pelt, DW, Dungan, CM, Denes, LT, Fu, X, Brightwell, CR, Zentner, GE, Dupont-Versteegden, EE , Richards, CI , Smith, JJ , Fry, CS , McCarthy, JJ & Peterson, CA 2021, 'Early satellite cell communication creates a permissive environment for long-term muscle growth', iScience, vol. 24, no. 4, 102372. https://doi.org/10.1016/j.isci.2021.102372

TY - JOUR

T1 - Early satellite cell communication creates a permissive environment for long-term muscle growth

AU - Murach, Kevin A.

AU - Peck, Bailey D.

AU - Policastro, Robert A.

AU - Vechetti, Ivan J.

AU - Van Pelt, Douglas W.

AU - Dungan, Cory M.

AU - Denes, Lance T.

AU - Fu, Xu

AU - Brightwell, Camille R.

AU - Zentner, Gabriel E.

AU - Dupont-Versteegden, Esther E.

AU - Richards, Christopher I.

AU - Smith, Jeramiah J.

AU - Fry, Christopher S.

AU - McCarthy, John J.

AU - Peterson, Charlotte A.

PY - 2021/4/23

Y1 - 2021/4/23

N2 - 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.

AB - 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.

KW - Cell Biology

KW - Functional Aspects of Cell Biology

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ER -

Early satellite cell communication creates a permissive environment for long-term muscle growth

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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