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

TY - JOUR

T1 - A mathematical model for mechanotransduction at the early steps of suture formation

AU - Khonsari, R. H.

AU - Olivier, J.

AU - Vigneaux, P.

AU - Sanchez, S.

AU - Tafforeau, P.

AU - Ahlberg, P. E.

AU - Di Rocco, F.

AU - Bresch, D.

AU - Corre, P.

AU - Ohazama, A.

AU - Sharpe, P. T.

AU - Calvez, V.

PY - 2013/5/22

Y1 - 2013/5/22

N2 - 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.

AB - 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.

KW - sutural bone growth

KW - mechanical instability

KW - partial differential equation

KW - synchrotron microtomography

KW - mechanotransduction

KW - CRANIAL SUTURES

KW - INTRAMEMBRANOUS BONE

KW - SKULL VAULT

KW - GROWTH

KW - MORPHOGENESIS

KW - MECHANICS

KW - STRAIN

KW - FGFR2

KW - FATE

KW - MICE

U2 - 10.1098/rspb.2012.2670

DO - 10.1098/rspb.2012.2670

M3 - Article

SN - 0962-8452

VL - 280

JO - Proceedings - Royal Society. Biological Sciences

JF - Proceedings - Royal Society. Biological Sciences

IS - 1759

M1 - 20122670

ER -