Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues

Erin E. Terry; Xiping Zhang; Christy Hoffmann; Laura D. Hughes; Scott A. Lewis; Jiajia Li; Matthew J. Wallace; Lance A. Riley; Collin M. Douglas; Miguel A. Gutierrez-Monreal; Nicholas F. Lahens; Ming C. Gong; Francisco Andrade; Karyn A. Esser; Michael E. Hughes

doi:10.7554/eLife.34613

Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues

Erin E. Terry, Xiping Zhang, Christy Hoffmann, Laura D. Hughes, Scott A. Lewis, Jiajia Li, Matthew J. Wallace, Lance A. Riley, Collin M. Douglas, Miguel A. Gutierrez-Monreal, Nicholas F. Lahens, Ming C. Gong, Francisco Andrade, Karyn A. Esser, Michael E. Hughes

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

74 Scopus citations

Abstract

Skeletal muscle comprises a family of diverse tissues with highly specialized functions. Many acquired diseases, including HIV and COPD, affect specific muscles while sparing others. Even monogenic muscular dystrophies selectively affect certain muscle groups. These observations suggest that factors intrinsic to muscle tissues influence their resistance to disease. Nevertheless, most studies have not addressed transcriptional diversity among skeletal muscles. Here we use RNAseq to profile mRNA expression in skeletal, smooth, and cardiac muscle tissues from mice and rats. Our data set, MuscleDB, reveals extensive transcriptional diversity, with greater than 50% of transcripts differentially expressed among skeletal muscle tissues. We detect mRNA expression of hundreds of putative myokines that may underlie the endocrine functions of skeletal muscle. We identify candidate genes that may drive tissue specialization, including Smarca4, Vegfa, and Myostatin. By demonstrating the intrinsic diversity of skeletal muscles, these data provide a resource for studying the mechanisms of tissue specialization.

Original language	English
Article number	e34613
Journal	eLife
Volume	7
DOIs	https://doi.org/10.7554/eLife.34613
State	Published - May 29 2018

Bibliographical note

Funding Information:
We thank Jeanne Geskes, Robert Lyons, and the University of Michigan DNA sequencing core facility for assistance with next-generation sequencing. We thank Ron Anafi, (UPenn), Jeff Haspel (Washington University Department of Medicine), John Hogenesch (Cincinnati Children’s Hospital), Patty Parker (UMSL), Bob Ricklefs (UMSL), and members of the Hughes and Esser laboratories for helpful discussion and technical support throughout this project. We thank Dr. Michael Chicoine (Washington University Department of Neurosurgery) for inestimable contributions without which this paper would never have been written. Work in the Gong lab is supported by NIH award HL106843. Work in the Esser lab is supported by NIH award R01AR066082. Work in the Hughes Lab is supported by NIH award R21AR069266 and start-up funds from the Department of Medicine at Washington University in St. Louis. We thank the Genome Technology Access Center in the Department of Genetics at Washington University School of Medicine for help with genomic analysis. The Center is partially supported by NCI Cancer Center Support Grant #P30 CA91842 to the Siteman Cancer Center and by ICTS/CTSA Grant# UL1 TR000448 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH), and NIH Roadmap for Medical Research. This publication is solely the responsibility of the authors and does not necessarily represent the official view of NCRR or NIH.

Publisher Copyright:
© Terry et al.

ASJC Scopus subject areas

Neuroscience (all)
Immunology and Microbiology (all)
Biochemistry, Genetics and Molecular Biology (all)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.7554/eLife.34613

Cite this

Terry, E. E., Zhang, X., Hoffmann, C., Hughes, L. D., Lewis, S. A., Li, J., Wallace, M. J., Riley, L. A., Douglas, C. M., Gutierrez-Monreal, M. A., Lahens, N. F., Gong, M. C., Andrade, F., Esser, K. A., & Hughes, M. E. (2018). Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues. eLife, 7, Article e34613. https://doi.org/10.7554/eLife.34613

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abstract = "Skeletal muscle comprises a family of diverse tissues with highly specialized functions. Many acquired diseases, including HIV and COPD, affect specific muscles while sparing others. Even monogenic muscular dystrophies selectively affect certain muscle groups. These observations suggest that factors intrinsic to muscle tissues influence their resistance to disease. Nevertheless, most studies have not addressed transcriptional diversity among skeletal muscles. Here we use RNAseq to profile mRNA expression in skeletal, smooth, and cardiac muscle tissues from mice and rats. Our data set, MuscleDB, reveals extensive transcriptional diversity, with greater than 50% of transcripts differentially expressed among skeletal muscle tissues. We detect mRNA expression of hundreds of putative myokines that may underlie the endocrine functions of skeletal muscle. We identify candidate genes that may drive tissue specialization, including Smarca4, Vegfa, and Myostatin. By demonstrating the intrinsic diversity of skeletal muscles, these data provide a resource for studying the mechanisms of tissue specialization.",

author = "Terry, {Erin E.} and Xiping Zhang and Christy Hoffmann and Hughes, {Laura D.} and Lewis, {Scott A.} and Jiajia Li and Wallace, {Matthew J.} and Riley, {Lance A.} and Douglas, {Collin M.} and Gutierrez-Monreal, {Miguel A.} and Lahens, {Nicholas F.} and Gong, {Ming C.} and Francisco Andrade and Esser, {Karyn A.} and Hughes, {Michael E.}",

note = "Funding Information: We thank Jeanne Geskes, Robert Lyons, and the University of Michigan DNA sequencing core facility for assistance with next-generation sequencing. We thank Ron Anafi, (UPenn), Jeff Haspel (Washington University Department of Medicine), John Hogenesch (Cincinnati Children{\textquoteright}s Hospital), Patty Parker (UMSL), Bob Ricklefs (UMSL), and members of the Hughes and Esser laboratories for helpful discussion and technical support throughout this project. We thank Dr. Michael Chicoine (Washington University Department of Neurosurgery) for inestimable contributions without which this paper would never have been written. Work in the Gong lab is supported by NIH award HL106843. Work in the Esser lab is supported by NIH award R01AR066082. Work in the Hughes Lab is supported by NIH award R21AR069266 and start-up funds from the Department of Medicine at Washington University in St. Louis. We thank the Genome Technology Access Center in the Department of Genetics at Washington University School of Medicine for help with genomic analysis. The Center is partially supported by NCI Cancer Center Support Grant #P30 CA91842 to the Siteman Cancer Center and by ICTS/CTSA Grant# UL1 TR000448 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH), and NIH Roadmap for Medical Research. This publication is solely the responsibility of the authors and does not necessarily represent the official view of NCRR or NIH. Publisher Copyright: {\textcopyright} Terry et al.",

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AU - Li, Jiajia

AU - Wallace, Matthew J.

AU - Riley, Lance A.

AU - Douglas, Collin M.

AU - Gutierrez-Monreal, Miguel A.

AU - Lahens, Nicholas F.

AU - Gong, Ming C.

AU - Andrade, Francisco

AU - Esser, Karyn A.

AU - Hughes, Michael E.

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Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues

Abstract

Bibliographical note

ASJC Scopus subject areas

UN SDGs

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