Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues

  1. Erin E Terry
  2. Xiping Zhang
  3. Christy Hoffmann
  4. Laura D Hughes
  5. Scott A Lewis
  6. Jiajia Li
  7. Matthew J Wallace
  8. Lance Riley
  9. Collin M Douglas
  10. Miguel A Gutierrez-Montreal
  11. Nicholas F Lahens
  12. Ming C Gong
  13. Francisco Andrade
  14. Karyn A Esser
  15. Michael E Hughes  Is a corresponding author
  1. Washington University School of Medicine, United States
  2. University of Florida, United States
  3. The Scripps Research Institute, United States
  4. University of Pennsylvania, United States
  5. University of Kentucky, United States

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.

Data availability

RNA Sequencing data have been deposited in GEO under accession code GSE100505. Analyzed data are available on http://muscledb.org.

The following data sets were generated

Article and author information

Author details

  1. Erin E Terry

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1334-4238
  2. Xiping Zhang

    Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Christy Hoffmann

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura D Hughes

    Department of Integrative, Structural and Computational Biology, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Scott A Lewis

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jiajia Li

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Matthew J Wallace

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Lance Riley

    Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Collin M Douglas

    Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Miguel A Gutierrez-Montreal

    Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Nicholas F Lahens

    Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3965-5624
  12. Ming C Gong

    Department of Physiology, School of Medicine, University of Kentucky, Lexington, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Francisco Andrade

    Department of Physiology, School of Medicine, University of Kentucky, Lexington, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Karyn A Esser

    Department of Physiology and Functional Genomics, 2.Department of Physiology and Functional Genomics, University of Florida, Gainsville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5791-1441
  15. Michael E Hughes

    Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, St. Louis, United States
    For correspondence
    michael.hughes@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8828-3732

Funding

National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR069266)

  • Karyn A Esser
  • Michael E Hughes

National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR066082)

  • Karyn A Esser

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal procedures were conducted in compliance with the guidelines of the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC) and were approved by the Institutional Animal Care and Use Committee at University of Kentucky (IACUC assurance number: A-3336-01).

Reviewing Editor

  1. Andrew Brack, University of California, San Francisco, United States

Publication history

  1. Received: December 22, 2017
  2. Accepted: May 15, 2018
  3. Accepted Manuscript published: May 29, 2018 (version 1)
  4. Version of Record published: June 19, 2018 (version 2)

Copyright

© 2018, Terry et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Erin E Terry
  2. Xiping Zhang
  3. Christy Hoffmann
  4. Laura D Hughes
  5. Scott A Lewis
  6. Jiajia Li
  7. Matthew J Wallace
  8. Lance Riley
  9. Collin M Douglas
  10. Miguel A Gutierrez-Montreal
  11. Nicholas F Lahens
  12. Ming C Gong
  13. Francisco Andrade
  14. Karyn A Esser
  15. Michael E Hughes
(2018)
Transcriptional profiling reveals extraordinary diversity among skeletal muscle tissues
eLife 7:e34613.
https://doi.org/10.7554/eLife.34613
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