Department of Physics and Astronomy, Tufts University, Medford, Massachusetts, United States of America.
Department of Biomedical Engineering, Tufts University, Medford, Massachusetts, United States of America.
PLoS One. 2021 Sep 23;16(9):e0257659. doi: 10.1371/journal.pone.0257659. eCollection 2021.
The formation of neuron networks is a complex phenomenon of fundamental importance for understanding the development of the nervous system, and for creating novel bioinspired materials for tissue engineering and neuronal repair. The basic process underlying the network formation is axonal growth, a process involving the extension of axons from the cell body towards target neurons. Axonal growth is guided by environmental stimuli that include intercellular interactions, biochemical cues, and the mechanical and geometrical features of the growth substrate. The dynamics of the growing axon and its biomechanical interactions with the growing substrate remains poorly understood. In this paper, we develop a model of axonal motility which incorporates mechanical interactions between the axon and the growth substrate. We combine experimental data with theoretical analysis to measure the parameters that describe axonal growth on surfaces with micropatterned periodic geometrical features: diffusion (cell motility) coefficients, speed and angular distributions, and axon bending rigidities. Experiments performed on neurons treated Taxol (inhibitor of microtubule dynamics) and Blebbistatin (disruptor of actin filaments) show that the dynamics of the cytoskeleton plays a critical role in the axon steering mechanism. Our results demonstrate that axons follow geometrical patterns through a contact-guidance mechanism, in which high-curvature geometrical features impart high traction forces to the growth cone. These results have important implications for our fundamental understanding of axonal growth as well as for bioengineering novel substrates that promote neuronal growth and nerve repair.
神经元网络的形成是理解神经系统发育的一个非常重要的基本现象,也是为组织工程和神经元修复创造新型仿生材料的关键。网络形成的基本过程是轴突生长,这是一个涉及轴突从细胞体向靶神经元延伸的过程。轴突生长受到环境刺激的引导,包括细胞间的相互作用、生化线索以及生长基质的机械和几何特征。生长轴突的动力学及其与生长基质的生物力学相互作用仍知之甚少。在本文中,我们开发了一个包含轴突和生长基质之间机械相互作用的轴突运动模型。我们将实验数据与理论分析相结合,以测量描述在具有微图案周期性几何特征的表面上轴突生长的参数:扩散(细胞运动)系数、速度和角度分布以及轴突弯曲刚度。在经紫杉醇(微管动力学抑制剂)和 blebbistatin(肌动蛋白丝破坏剂)处理的神经元上进行的实验表明,细胞骨架的动力学在轴突转向机制中起着关键作用。我们的结果表明,轴突通过接触制导机制遵循几何图案,其中高曲率几何特征向生长锥施加高牵引力。这些结果对我们深入了解轴突生长以及生物工程促进神经元生长和神经修复的新型基质具有重要意义。