Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton

Mechanical loading is critical for collagen network maintenance and remodelling in adult skeletal tissues, but the role of loading in collagen network formation during development is poorly understood. We test the hypothesis that mechanical loading is necessary for the onset and maturation of spatia...

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Published in:Royal Society Open Science
Main Authors: Saima Ahmed, Andrew V. Rogers, Niamh C. Nowlan
Format: Article
Language:English
Published: The Royal Society 2023-10-01
Subjects:
Online Access:https://royalsocietypublishing.org/doi/10.1098/rsos.231023
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author Saima Ahmed
Andrew V. Rogers
Niamh C. Nowlan
author_facet Saima Ahmed
Andrew V. Rogers
Niamh C. Nowlan
author_sort Saima Ahmed
collection DOAJ
container_title Royal Society Open Science
description Mechanical loading is critical for collagen network maintenance and remodelling in adult skeletal tissues, but the role of loading in collagen network formation during development is poorly understood. We test the hypothesis that mechanical loading is necessary for the onset and maturation of spatial localization and structure of collagens in prenatal cartilage and bone, using in vivo and in vitro mouse models of altered loading. The majority of collagens studied was aberrant in structure or localization, or both, when skeletal muscle was absent in vivo. Using in vitro bioreactor culture system, we demonstrate that mechanical loading directly modulates the spatial localization and structure of collagens II and X. Furthermore, we show that mechanical loading in vitro rescues aspects of the development of collagens II and X from the effects of fetal immobility. In conclusion, our findings show that mechanical loading is a critical determinant of collagen network establishment during prenatal skeletal development.
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spelling doaj-art-e5ac3475e0a544f69a3239087ec4e7de2025-08-19T22:14:15ZengThe Royal SocietyRoyal Society Open Science2054-57032023-10-01101010.1098/rsos.231023Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeletonSaima Ahmed0Andrew V. Rogers1Niamh C. Nowlan2Department of Bioengineering, Imperial College London, London, UKElectron Microscopy Unit, Royal Brompton Hospital, London, UKDepartment of Bioengineering, Imperial College London, London, UKMechanical loading is critical for collagen network maintenance and remodelling in adult skeletal tissues, but the role of loading in collagen network formation during development is poorly understood. We test the hypothesis that mechanical loading is necessary for the onset and maturation of spatial localization and structure of collagens in prenatal cartilage and bone, using in vivo and in vitro mouse models of altered loading. The majority of collagens studied was aberrant in structure or localization, or both, when skeletal muscle was absent in vivo. Using in vitro bioreactor culture system, we demonstrate that mechanical loading directly modulates the spatial localization and structure of collagens II and X. Furthermore, we show that mechanical loading in vitro rescues aspects of the development of collagens II and X from the effects of fetal immobility. In conclusion, our findings show that mechanical loading is a critical determinant of collagen network establishment during prenatal skeletal development.https://royalsocietypublishing.org/doi/10.1098/rsos.231023collagen Icollagen IIcollagen VIcollagen Xcollagen XIbioreactor
spellingShingle Saima Ahmed
Andrew V. Rogers
Niamh C. Nowlan
Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
collagen I
collagen II
collagen VI
collagen X
collagen XI
bioreactor
title Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
title_full Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
title_fullStr Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
title_full_unstemmed Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
title_short Mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
title_sort mechanical loading due to muscle movement regulates establishment of the collagen network in the developing murine skeleton
topic collagen I
collagen II
collagen VI
collagen X
collagen XI
bioreactor
url https://royalsocietypublishing.org/doi/10.1098/rsos.231023
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AT andrewvrogers mechanicalloadingduetomusclemovementregulatesestablishmentofthecollagennetworkinthedevelopingmurineskeleton
AT niamhcnowlan mechanicalloadingduetomusclemovementregulatesestablishmentofthecollagennetworkinthedevelopingmurineskeleton