Schaeffer Julia, Weber Isabell P, Thompson Amelia J, Keynes Roger J, Franze Kristian
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.
Inserm, U1216, Grenoble Institut Neurosciences, Univ. Grenoble Alpes, Grenoble, France.
Front Cell Dev Biol. 2022 Jul 8;10:917589. doi: 10.3389/fcell.2022.917589. eCollection 2022.
During patterning of the peripheral nervous system, motor axons grow sequentially out of the neural tube in a segmented fashion to ensure functional integration of the motor roots between the surrounding cartilage and bones of the developing vertebrae. This segmented outgrowth is regulated by the intrinsic properties of each segment (somite) adjacent to the neural tube, and in particular by chemical repulsive guidance cues expressed in the posterior half. Yet, knockout models for such repulsive cues still display initial segmentation of outgrowing motor axons, suggesting the existence of additional, yet unknown regulatory mechanisms of axon growth segmentation. As neuronal growth is not only regulated by chemical but also by mechanical signals, we here characterized the mechanical environment of outgrowing motor axons. Using atomic force microscopy-based indentation measurements on chick embryo somite strips, we identified stiffness gradients in each segment, which precedes motor axon growth. Axon growth was restricted to the anterior, softer tissue, which showed lower cell body densities than the repulsive stiffer posterior parts at later stages. As tissue stiffness is known to regulate axon growth during development, our results suggest that motor axons also respond to periodic stiffness gradients imposed by the intrinsic mechanical properties of somites.
在周围神经系统的模式形成过程中,运动轴突以分段的方式依次从神经管中生长出来,以确保运动神经根在发育中的椎骨周围的软骨和骨骼之间实现功能整合。这种分段生长受神经管相邻的每个节段(体节)的内在特性调节,特别是后半部分表达的化学排斥性导向线索。然而,此类排斥性线索的基因敲除模型仍显示出正在生长的运动轴突的初始分段,这表明存在尚未知晓的轴突生长分段的额外调节机制。由于神经元生长不仅受化学信号调节,还受机械信号调节,我们在此对正在生长的运动轴突的机械环境进行了表征。通过对鸡胚体节条带进行基于原子力显微镜的压痕测量,我们在每个节段中识别出了在运动轴突生长之前的硬度梯度。轴突生长局限于前部较软的组织,该组织在后期的细胞体密度低于具有排斥性的较硬的后部组织。由于已知组织硬度在发育过程中调节轴突生长,我们的结果表明运动轴突也对体节的内在机械特性所施加的周期性硬度梯度作出反应。