Microstructural differences in the osteochondral unit of terrestrial and aquatic mammals

  1. Irina AD Mancini
  2. Riccardo Levato
  3. Marlena M Ksiezarczyk
  4. Miguel Dias Castilho
  5. Michael Chen
  6. Mattie HP van Rijen
  7. Lonneke L IJsseldijk
  8. Marja Kik
  9. René van Weeren
  10. Jos Malda  Is a corresponding author
  1. Utrecht University, Netherlands
  2. University Medical Center Utrecht, Netherlands
  3. Eindhoven University of Technology, Netherlands
  4. University of Adelaide, Netherlands

Abstract

During evolution, animals have returned from land to water, adapting with morphological modifications to life in an aquatic environment. We compared the osteochondral units of the humeral head of marine and terrestrial mammals across species spanning a wide range of body weights, focusing on microstructural organization and biomechanical performance. Aquatic mammals feature cartilage with essentially random collagen fiber configuration, lacking the depth-dependent, arcade-like organization characteristic of terrestrial mammalian species. They have a less stiff articular cartilage at equilibrium with a significantly lower peak modulus, and at the osteochondral interface do not have a calcified cartilage layer, displaying only a thin, highly porous subchondral bone plate. This totally different constitution of the osteochondral unit in aquatic mammals reflects that accommodation of loading is the primordial function of the osteochondral unit. Recognizing the crucial importance of the microarchitecture-function relationship is pivotal for understanding articular biology and, hence, for the development of durable functional regenerative approaches for treatment of joint damage, which are thus far lacking.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figure 1.

Article and author information

Author details

  1. Irina AD Mancini

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Riccardo Levato

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Marlena M Ksiezarczyk

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Miguel Dias Castilho

    Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael Chen

    5Department of Mathematical Sciences, University of Adelaide, Adelaide, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Mattie HP van Rijen

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Lonneke L IJsseldijk

    Department of Biomolecular Health Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7288-9118
  8. Marja Kik

    Department of Biomolecular Health Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. René van Weeren

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6654-1817
  10. Jos Malda

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    For correspondence
    j.malda@umcutrecht.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9241-7676

Funding

European Commission (3099622 (FP7))

  • Irina AD Mancini
  • René van Weeren
  • Jos Malda

Dutch Arthritis Society (LLP12 and LLP22)

  • Riccardo Levato
  • Miguel Dias Castilho
  • René van Weeren
  • Jos Malda

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

Copyright

© 2023, Mancini 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.

Metrics

  • 676
    views
  • 158
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Irina AD Mancini
  2. Riccardo Levato
  3. Marlena M Ksiezarczyk
  4. Miguel Dias Castilho
  5. Michael Chen
  6. Mattie HP van Rijen
  7. Lonneke L IJsseldijk
  8. Marja Kik
  9. René van Weeren
  10. Jos Malda
(2023)
Microstructural differences in the osteochondral unit of terrestrial and aquatic mammals
eLife 12:e80936.
https://doi.org/10.7554/eLife.80936

Share this article

https://doi.org/10.7554/eLife.80936

Further reading

    1. Developmental Biology
    Wei Yan
    Editorial

    The articles in this special issue highlight the diversity and complexity of research into reproductive health, including the need for a better understanding of the fundamental biology of reproduction and for new treatments for a range of reproductive disorders.

    1. Developmental Biology
    Anastasiia Lozovska, Ana Casaca ... Moises Mallo
    Research Article

    During the trunk to tail transition the mammalian embryo builds the outlets for the intestinal and urogenital tracts, lays down the primordia for the hindlimb and external genitalia, and switches from the epiblast/primitive streak (PS) to the tail bud as the driver of axial extension. Genetic and molecular data indicate that Tgfbr1 is a key regulator of the trunk to tail transition. Tgfbr1 has been shown to control the switch of the neuromesodermal competent cells from the epiblast to the chordoneural hinge to generate the tail bud. We now show that in mouse embryos Tgfbr1 signaling also controls the remodeling of the lateral plate mesoderm (LPM) and of the embryonic endoderm associated with the trunk to tail transition. In the absence of Tgfbr1, the two LPM layers do not converge at the end of the trunk, extending instead as separate layers until the caudal embryonic extremity, and failing to activate markers of primordia for the hindlimb and external genitalia. The vascular remodeling involving the dorsal aorta and the umbilical artery leading to the connection between embryonic and extraembryonic circulation was also affected in the Tgfbr1 mutant embryos. Similar alterations in the LPM and vascular system were also observed in Isl1 null mutants, indicating that this factor acts in the regulatory cascade downstream of Tgfbr1 in LPM-derived tissues. In addition, in the absence of Tgfbr1 the embryonic endoderm fails to expand to form the endodermal cloaca and to extend posteriorly to generate the tail gut. We present evidence suggesting that the remodeling activity of Tgfbr1 in the LPM and endoderm results from the control of the posterior PS fate after its regression during the trunk to tail transition. Our data, together with previously reported observations, place Tgfbr1 at the top of the regulatory processes controlling the trunk to tail transition.