Molecular characterization of the intact mouse muscle spindle using a multi-omics approach

  1. Bavat Bornstein  Is a corresponding author
  2. Lia Heinemann-Yerushalmi
  3. Sharon Krief
  4. Ruth Adler
  5. Bareket Dassa
  6. Dena Leshkowitz
  7. Minchul Kim
  8. Guy Bewick
  9. Robert W Banks
  10. Elazar Zelzer  Is a corresponding author
  1. Weizmann Institute of Science, Israel
  2. Max Delbrueck Center for Molecular Medicine, Germany
  3. University of Aberdeen, United Kingdom
  4. Durham University, United Kingdom

Abstract

The proprioceptive system is essential for the control of coordinated movement, posture and skeletal integrity. The sense of proprioception is produced in the brain using peripheral sensory input from receptors such as the muscle spindle, which detects changes in the length of skeletal muscles. Despite its importance, the molecular composition of the muscle spindle is largely unknown. In this study, we generated comprehensive transcriptomic and proteomic datasets of the entire muscle spindle isolated from the murine deep masseter muscle. We then associated differentially expressed genes with the various tissues composing the spindle using bioinformatic analysis. Immunostaining verified these predictions, thus establishing new markers for the different spindle tissues. Utilizing these markers, we identified the differentiation stages the spindle capsule cells undergo during development. Together, these findings provide comprehensive molecular characterization of the intact spindle as well as new tools to study its development and function in health and disease.

Data availability

Sequencing data have been deposited in GEO under accession number GSE208147.The raw data of proteomic profiling were deposited in the ProteomeXchange via the Proteomic Identification Database (PRIDE partner repository)

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Bavat Bornstein

    Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    bavat.bornstein@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
  2. Lia Heinemann-Yerushalmi

    Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Sharon Krief

    Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Ruth Adler

    Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Bareket Dassa

    Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Dena Leshkowitz

    Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Minchul Kim

    Developmental Biology/Signal Transduction, Max Delbrueck Center for Molecular Medicine, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Guy Bewick

    Institute of Medical Sciences, University of Aberdeen, Durham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Robert W Banks

    Department of Biosciences, Durham University, Durham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1614-6488
  10. Elazar Zelzer

    Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    eli.zelzer@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1584-6602

Funding

The David and Fela Shapell Family Center for Genetic Disorders Research

  • Elazar Zelzer

The Julie and Eric Borman Family Research Funds

  • Elazar Zelzer

The Nella and Leon Benoziyo Center for Neurological Diseases

  • Elazar Zelzer

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

Reviewing Editor

  1. Benjamin L Prosser, University of Pennsylvania Perelman School of Medicine, United States

Ethics

Animal experimentation: All experiments involving mice were approved by the Institutional Animal Care and Use Committee (IACUC) of the Weizmann Institute (#02180222-2).

Version history

  1. Received: July 13, 2022
  2. Preprint posted: July 14, 2022 (view preprint)
  3. Accepted: February 3, 2023
  4. Accepted Manuscript published: February 6, 2023 (version 1)
  5. Version of Record published: February 15, 2023 (version 2)

Copyright

© 2023, Bornstein 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. Bavat Bornstein
  2. Lia Heinemann-Yerushalmi
  3. Sharon Krief
  4. Ruth Adler
  5. Bareket Dassa
  6. Dena Leshkowitz
  7. Minchul Kim
  8. Guy Bewick
  9. Robert W Banks
  10. Elazar Zelzer
(2023)
Molecular characterization of the intact mouse muscle spindle using a multi-omics approach
eLife 12:e81843.
https://doi.org/10.7554/eLife.81843

Share this article

https://doi.org/10.7554/eLife.81843

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