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Postnatal mechanical loading drives adaptation of tissues primarily through modulation of the non-collagenous matrix

  1. Danae E Zamboulis  Is a corresponding author
  2. Chavaunne T Thorpe
  3. Yalda Ashraf Kharaz
  4. Helen L Birch
  5. Hazel R C Screen
  6. Peter D Clegg
  1. University of Liverpool, United Kingdom
  2. Royal Veterinary College, United Kingdom
  3. University College London, United Kingdom
  4. Queen Mary University of London, United Kingdom
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Cite this article as: eLife 2020;9:e58075 doi: 10.7554/eLife.58075

Abstract

Mature connective tissues demonstrate highly specialised properties, remarkably adapted to meet their functional requirements. Tissue adaptation to environmental cues can occur throughout life and poor adaptation commonly results in injury. However, the temporal nature and drivers of functional adaptation remain undefined. Here, we explore functional adaptation and specialisation of mechanically loaded tissues using tendon; a simple aligned biological composite, in which the collagen (fascicle) and surrounding predominantly non-collagenous matrix (interfascicular matrix) can be interrogated independently. Using an equine model of late development, we report the first phase-specific analysis of biomechanical, structural and compositional changes seen in functional adaptation, demonstrating adaptation occurs postnatally, following mechanical loading, and is almost exclusively localised to the non-collagenous interfascicular matrix. These novel data redefine adaptation in connective tissue, highlighting the fundamental importance of non-collagenous matrix and suggesting that regenerative medicine strategies should change focus from the fibrous to the non-collagenous matrix of tissue.

Article and author information

Author details

  1. Danae E Zamboulis

    Institute of Ageing and Chronic Disease, Musculoskeletal Biology I, University of Liverpool, Liverpool, United Kingdom
    For correspondence
    danaez@liverpool.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2839-7620
  2. Chavaunne T Thorpe

    Comparative Biomedical Sciences, Royal Veterinary College, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7051-3504
  3. Yalda Ashraf Kharaz

    Institute of Ageing and Chronic Disease, Musculoskeletal Biology I, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Helen L Birch

    Department of Orthopaedics and Musculoskeletal Science, University College London, Stanmore, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Hazel R C Screen

    School of Engineering and Materials Science, Institute of Bioengineering, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter D Clegg

    Institute of Ageing and Chronic Disease, Musculoskeletal Biology I, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

Horserace Betting Levy Board (PRJ/776)

  • Danae E Zamboulis
  • Helen L Birch
  • Hazel R C Screen
  • Peter D Clegg

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

Ethics

Animal experimentation: Samples were collected from horses euthanised for reasons unrelated to this project at a commercial abattoir or equine practices following owner consent under ethical approval for use of the cadaveric material granted by the Veterinary Research Ethics Committee, School of Veterinary Science, University of Liverpool (VREC352).

Reviewing Editor

  1. Subburaman Mohan, Loma Linda University, United States

Publication history

  1. Received: April 20, 2020
  2. Accepted: October 12, 2020
  3. Accepted Manuscript published: October 16, 2020 (version 1)
  4. Version of Record published: October 28, 2020 (version 2)

Copyright

© 2020, Zamboulis 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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