Mechanical positional information guides the self-organized development of a polygonal network of creases in the skin of mammalian noses.

Autor: Dagenais P; Laboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, 1211 Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland., Jahanbakhsh E; Laboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, 1211 Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland., Capitan A; Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350 Jouy-en-Josas, France., Jammes H; BREED INRAE, UVSQ, Université Paris-Saclay, 78350 Jouy-en-Josas, France., Reynaud K; CNRS, IFCE, INRAE, Université de Tours, PRC, 37380 Nouzilly, France; École Nationale Vétérinaire d'Alfort, EnvA, 94700 Maisons-Alfort, France., De Juan Romero C; Instituto de Neurociencias, CSIC-UMH, 03540 San Juan de Alicante, Spain., Borrell V; Instituto de Neurociencias, CSIC-UMH, 03540 San Juan de Alicante, Spain., Milinkovitch MC; Laboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, 1211 Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland. Electronic address: michel.milinkovitch@unige.ch.
Jazyk: angličtina
Zdroj: Current biology : CB [Curr Biol] 2024 Nov 18; Vol. 34 (22), pp. 5197-5212.e4. Date of Electronic Publication: 2024 Oct 22.
DOI: 10.1016/j.cub.2024.09.055
Abstrakt: The glabrous skin of the rhinarium (naked nose) of many mammalian species exhibits a polygonal pattern of grooves that retain physiological fluid, thereby keeping their nose wet and, among other effects, facilitating the collection of chemosensory molecules. Here, we perform volumetric imaging of whole-mount rhinaria from sequences of embryonic and juvenile cows, dogs, and ferrets. We demonstrate that rhinarial polygonal domains are not placode-derived skin appendages but arise through a self-organized mechanical process consisting of the constrained growth and buckling of the epidermal basal layer, followed by the formation of sharp epidermal creases exactly facing an underlying network of stiff blood vessels. Our numerical simulations show that the mechanical stress generated by excessive epidermal growth concentrates at the positions of vessels that form rigid base points, causing the epidermal layers to move outward and shape domes-akin to arches rising against stiff pillars. Remarkably, this gives rise to a larger length scale (the distance between the vessels) in the surface folding pattern than would otherwise occur in the absence of vessels. These results hint at a concept of "mechanical positional information" by which material properties of anatomical elements can impose local constraints on an otherwise globally self-organized mechanical pattern. In addition, our analyses of the rhinarial patterns in cow clones highlight a substantial level of stochasticity in the pre-pattern of vessels, while our numerical simulations also recapitulate the disruption of the folding pattern in cows affected by a hereditary disorder that causes hyperextensibility of the skin.
Competing Interests: Declaration of interests The authors declare no competing interests.
(Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)
Databáze: MEDLINE