Laboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, 1211 Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350 Jouy-en-Josas, France.
Curr Biol. 2024 Nov 18;34(22):5197-5212.e4. doi: 10.1016/j.cub.2024.09.055. Epub 2024 Oct 22.
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.
许多哺乳动物的鼻甲骨(裸露的鼻子)无毛皮肤呈现出多边形的凹槽图案,这些凹槽保留了生理液体,从而保持鼻子湿润,并且在其他方面促进了化学感觉分子的收集。在这里,我们对来自牛、狗和雪貂的胚胎和幼年个体的全鼻甲骨进行了体积成像。我们证明,鼻甲骨的多边形区域不是基板衍生的皮肤附属物,而是通过一个由表皮基底层的受限生长和屈曲组成的自组织机械过程产生的,随后形成了正好面对下方刚性血管网络的尖锐表皮褶皱。我们的数值模拟表明,由表皮过度生长产生的机械应力集中在形成刚性基点的血管位置,导致表皮层向外移动并形成穹顶——类似于对抗刚性支柱的拱形。值得注意的是,这在不存在血管的情况下会导致表面折叠模式中的更大长度尺度(血管之间的距离)。这些结果暗示了一种“机械位置信息”的概念,即解剖元素的材料特性可以对全局自组织机械模式施加局部约束。此外,我们对牛克隆体鼻甲骨模式的分析突出了血管前模式中存在相当大的随机性,而我们的数值模拟也再现了在一种遗传性疾病影响下,皮肤过度伸展的牛的折叠模式的破坏,这种疾病导致皮肤过度伸展。