Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model
The extracellular-matrix (ECM) is a complex interconnected three-dimensional network that provides structural support for the cells and tissues and defines organ architecture as key for their healthy functioning. However, the intimate mechanisms by which ECM acquire their three-dimensional architect...
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| Format: | Article |
| Language: | English |
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The Royal Society
2024-01-01
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| Series: | Royal Society Open Science |
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| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsos.231456 |
| _version_ | 1797265920911998976 |
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| author | Pauline Chassonnery Jenny Paupert Anne Lorsignol Childérick Séverac Marielle Ousset Pierre Degond Louis Casteilla Diane Peurichard |
| author_facet | Pauline Chassonnery Jenny Paupert Anne Lorsignol Childérick Séverac Marielle Ousset Pierre Degond Louis Casteilla Diane Peurichard |
| author_sort | Pauline Chassonnery |
| collection | DOAJ |
| description | The extracellular-matrix (ECM) is a complex interconnected three-dimensional network that provides structural support for the cells and tissues and defines organ architecture as key for their healthy functioning. However, the intimate mechanisms by which ECM acquire their three-dimensional architecture are still largely unknown. In this paper, we study this question by means of a simple three-dimensional individual based model of interacting fibres able to spontaneously crosslink or unlink to each other and align at the crosslinks. We show that such systems are able to spontaneously generate different types of architectures. We provide a thorough analysis of the emerging structures by an exhaustive parametric analysis and the use of appropriate visualization tools and quantifiers in three dimensions. The most striking result is that the emergence of ordered structures can be fully explained by a single emerging variable: the number of links per fibre in the network. If validated on real tissues, this simple variable could become an important putative target to control and predict the structuring of biological tissues, to suggest possible new therapeutic strategies to restore tissue functions after disruption, and to help in the development of collagen-based scaffolds for tissue engineering. Moreover, the model reveals that the emergence of architecture is a spatially homogeneous process following a unique evolutionary path, and highlights the essential role of dynamical crosslinking in tissue structuring. |
| first_indexed | 2024-03-08T09:31:38Z |
| format | Article |
| id | doaj.art-1cf3a5c45e8e41ac87bbabc64ef5202b |
| institution | Directory Open Access Journal |
| issn | 2054-5703 |
| language | English |
| last_indexed | 2024-04-25T00:52:28Z |
| publishDate | 2024-01-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Royal Society Open Science |
| spelling | doaj.art-1cf3a5c45e8e41ac87bbabc64ef5202b2024-03-11T15:19:35ZengThe Royal SocietyRoyal Society Open Science2054-57032024-01-0111110.1098/rsos.231456Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network modelPauline Chassonnery0Jenny Paupert1Anne Lorsignol2Childérick Séverac3Marielle Ousset4Pierre Degond5Louis Casteilla6Diane Peurichard7RESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceRESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceRESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceRESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceRESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceInstitut de Mathématiques de Toulouse, UMR5219, Université de Toulouse, CNRS, UPS, 31062 Toulouse Cedex 9, FranceRESTORE, Université de Toulouse, Inserm U1031, EFS, INP-ENVT, UPS, CNRS ERL5311, Toulouse, FranceInria Paris, team MAMBA, Sorbonne Université, CNRS, Université de Paris, Laboratoire Jacques-Louis Lions UMR7598, 75005 Paris, FranceThe extracellular-matrix (ECM) is a complex interconnected three-dimensional network that provides structural support for the cells and tissues and defines organ architecture as key for their healthy functioning. However, the intimate mechanisms by which ECM acquire their three-dimensional architecture are still largely unknown. In this paper, we study this question by means of a simple three-dimensional individual based model of interacting fibres able to spontaneously crosslink or unlink to each other and align at the crosslinks. We show that such systems are able to spontaneously generate different types of architectures. We provide a thorough analysis of the emerging structures by an exhaustive parametric analysis and the use of appropriate visualization tools and quantifiers in three dimensions. The most striking result is that the emergence of ordered structures can be fully explained by a single emerging variable: the number of links per fibre in the network. If validated on real tissues, this simple variable could become an important putative target to control and predict the structuring of biological tissues, to suggest possible new therapeutic strategies to restore tissue functions after disruption, and to help in the development of collagen-based scaffolds for tissue engineering. Moreover, the model reveals that the emergence of architecture is a spatially homogeneous process following a unique evolutionary path, and highlights the essential role of dynamical crosslinking in tissue structuring.https://royalsocietypublishing.org/doi/10.1098/rsos.231456interaction networksthree-dimensional mathematical modellingself-organizationextracellular matrixdynamical crosslinkingarchitecture emergence |
| spellingShingle | Pauline Chassonnery Jenny Paupert Anne Lorsignol Childérick Séverac Marielle Ousset Pierre Degond Louis Casteilla Diane Peurichard Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model Royal Society Open Science interaction networks three-dimensional mathematical modelling self-organization extracellular matrix dynamical crosslinking architecture emergence |
| title | Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model |
| title_full | Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model |
| title_fullStr | Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model |
| title_full_unstemmed | Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model |
| title_short | Fibre crosslinking drives the emergence of order in a three-dimensional dynamical network model |
| title_sort | fibre crosslinking drives the emergence of order in a three dimensional dynamical network model |
| topic | interaction networks three-dimensional mathematical modelling self-organization extracellular matrix dynamical crosslinking architecture emergence |
| url | https://royalsocietypublishing.org/doi/10.1098/rsos.231456 |
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