Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit
Abstract By developing a 3D X‐ray modeling and spatially correlative imaging method for fibrous collagenous tissues, this study provides a comprehensive mapping of nanoscale deformation in the collagen fibril network across the intact bone‐cartilage unit (BCU), whose healthy functioning is critical...
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| Format: | Article |
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Wiley
2025-01-01
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| Series: | Advanced Science |
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| Online Access: | https://doi.org/10.1002/advs.202407649 |
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| author | Waqas Badar Sheetal R. Inamdar Peter Fratzl Tim Snow Nicholas J. Terrill Martin M. Knight Himadri S. Gupta |
| author_facet | Waqas Badar Sheetal R. Inamdar Peter Fratzl Tim Snow Nicholas J. Terrill Martin M. Knight Himadri S. Gupta |
| author_sort | Waqas Badar |
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| description | Abstract By developing a 3D X‐ray modeling and spatially correlative imaging method for fibrous collagenous tissues, this study provides a comprehensive mapping of nanoscale deformation in the collagen fibril network across the intact bone‐cartilage unit (BCU), whose healthy functioning is critical for joint function and preventing degeneration. Extracting the 3D fibril structure from 2D small‐angle X‐ray scattering before and during physiological compression reveals of dominant deformation modes, including crystallinity transitions, lateral fibril compression, and reorientation, which vary in a coupled, nonlinear, and correlated manner across the cartilage‐bone interface. A distinct intermolecular arrangement of collagen molecules, and enhanced molecular‐level disorder, is found in the cartilage (sliding) surface region. Just below, fibrils accommodate tissue strain by reorientation, which transitions molecular‐level kinking or loss of crystallinity in the deep zone. Crystalline fibrils laterally shrink far more (20×) than they contract, possibly by water loss from between tropocollagen molecules. With the calcified plate acting as an anchor for surrounding tissue, a qualitative switch occurs in fibrillar deformation between the articular cartilage and calcified regions. These findings significantly advance this understanding of the complex, nonlinear ultrastructural dynamics at this critical interface, and opens avenues for developing targeted diagnostic and therapeutic strategies for musculoskeletal disorders. |
| format | Article |
| id | doaj-art-8897bb61b1274b7d9280490f2114d783 |
| institution | Kabale University |
| issn | 2198-3844 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Wiley |
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| series | Advanced Science |
| spelling | doaj-art-8897bb61b1274b7d9280490f2114d7832025-01-09T11:44:45ZengWileyAdvanced Science2198-38442025-01-01121n/an/a10.1002/advs.202407649Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage UnitWaqas Badar0Sheetal R. Inamdar1Peter Fratzl2Tim Snow3Nicholas J. Terrill4Martin M. Knight5Himadri S. Gupta6Centre for Bioengineering and School of Engineering and Materials Science Queen Mary University of London London E1 4NS UKCentre for Bioengineering and School of Engineering and Materials Science Queen Mary University of London London E1 4NS UKMax Planck Institute of Colloids and Interfaces Research Campus Golm 14424 Potsdam GermanyDiamond Light Source Harwell Science Campus Harwell OX11 0DE UKDiamond Light Source Harwell Science Campus Harwell OX11 0DE UKCentre for Bioengineering and School of Engineering and Materials Science Queen Mary University of London London E1 4NS UKCentre for Bioengineering and School of Engineering and Materials Science Queen Mary University of London London E1 4NS UKAbstract By developing a 3D X‐ray modeling and spatially correlative imaging method for fibrous collagenous tissues, this study provides a comprehensive mapping of nanoscale deformation in the collagen fibril network across the intact bone‐cartilage unit (BCU), whose healthy functioning is critical for joint function and preventing degeneration. Extracting the 3D fibril structure from 2D small‐angle X‐ray scattering before and during physiological compression reveals of dominant deformation modes, including crystallinity transitions, lateral fibril compression, and reorientation, which vary in a coupled, nonlinear, and correlated manner across the cartilage‐bone interface. A distinct intermolecular arrangement of collagen molecules, and enhanced molecular‐level disorder, is found in the cartilage (sliding) surface region. Just below, fibrils accommodate tissue strain by reorientation, which transitions molecular‐level kinking or loss of crystallinity in the deep zone. Crystalline fibrils laterally shrink far more (20×) than they contract, possibly by water loss from between tropocollagen molecules. With the calcified plate acting as an anchor for surrounding tissue, a qualitative switch occurs in fibrillar deformation between the articular cartilage and calcified regions. These findings significantly advance this understanding of the complex, nonlinear ultrastructural dynamics at this critical interface, and opens avenues for developing targeted diagnostic and therapeutic strategies for musculoskeletal disorders.https://doi.org/10.1002/advs.2024076493D diffraction modellingbone‐cartilage interfacecollagen fibrilsnanoscale mechanicssmall‐angle x‐ray scattering |
| spellingShingle | Waqas Badar Sheetal R. Inamdar Peter Fratzl Tim Snow Nicholas J. Terrill Martin M. Knight Himadri S. Gupta Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit Advanced Science 3D diffraction modelling bone‐cartilage interface collagen fibrils nanoscale mechanics small‐angle x‐ray scattering |
| title | Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit |
| title_full | Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit |
| title_fullStr | Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit |
| title_full_unstemmed | Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit |
| title_short | Nonlinear Stress‐Induced Transformations in Collagen Fibrillar Organization, Disorder and Strain Mechanisms in the Bone‐Cartilage Unit |
| title_sort | nonlinear stress induced transformations in collagen fibrillar organization disorder and strain mechanisms in the bone cartilage unit |
| topic | 3D diffraction modelling bone‐cartilage interface collagen fibrils nanoscale mechanics small‐angle x‐ray scattering |
| url | https://doi.org/10.1002/advs.202407649 |
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