A mathematical model for mechanotransduction at the early steps of suture formation

Author:

Khonsari R. H.12,Olivier J.3,Vigneaux P.4,Sanchez S.5,Tafforeau P.5,Ahlberg P. E.6,Di Rocco F.7,Bresch D.8,Corre P.2,Ohazama A.1,Sharpe P. T.1,Calvez V.4

Affiliation:

1. Department of Craniofacial Development and Stem Cell Research, Comprehensive Biomedical Research, Dental Institute, King's College London, London, UK

2. Service de Chirurgie maxillofaciale, Centre Hospitalier Universitaire, Nantes, France

3. Archimedes Center for Modeling, Analysis and Computation (ACMAC), Heraklion, Crete, Greece

4. Unité de Mathématiques Pures et Appliquées, École Normale Supérieure de Lyon, CNRS UMR, 5669 Lyon, France

5. European Synchrotron Radiation Facility (ESRF), Grenoble, France

6. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

7. Department of Pediatric Neurosurgery, Hôpital Necker-Enfants-Malades, Paris, France

8. Laboratoire de Mathématiques (LAMA), Université de Savoie, CNRS UMR, 5127 Chambéry, France

Abstract

Growth and patterning of craniofacial sutures is subjected to the effects of mechanical stress. Mechanotransduction processes occurring at the margins of the sutures are not precisely understood. Here, we propose a simple theoretical model based on the orientation of collagen fibres within the suture in response to local stress. We demonstrate that fibre alignment generates an instability leading to the emergence of interdigitations. We confirm the appearance of this instability both analytically and numerically. To support our model, we use histology and synchrotron X-ray microtomography and reveal the fine structure of fibres within the sutural mesenchyme and their insertion into the bone. Furthermore, using a mouse model with impaired mechanotransduction, we show that the architecture of sutures is disturbed when forces are not interpreted properly. Finally, by studying the structure of sutures in the mouse, the rat, an actinopterygian ( Polypterus bichir ) and a placoderm ( Compagopiscis croucheri ), we show that bone deposition patterns during dermal bone growth are conserved within jawed vertebrates. In total, these results support the role of mechanical constraints in the growth and patterning of craniofacial sutures, a process that was probably effective at the emergence of gnathostomes, and provide new directions for the understanding of normal and pathological suture fusion.

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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