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

Abstract

Growth and patterning of craniofacial sutures is subjected to the effects ofmechanical 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 ourmodel,we use histology and synchrotron X-ray microtomography and reveal the fine structure of fibreswithin the sutural mesenchymeand their insertion into the bone. Furthermore, using amousemodel with impaired mechanotransduction,we showthat the architecture of sutures is disturbedwhen 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 showthat 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. © 2013 The Author(s) Published by the Royal Society. All rights reserved.