Barakat Joseph M, Modica Kevin J, Lu Le, Anujarerat Stephanie, Choi Kyu Hwan, Takatori Sho C
Department of Chemical Engineering, University of California, Santa Barbara, Santa Barbara, California 93106, United States.
ACS Appl Nano Mater. 2024 May 8;7(10):12142-12152. doi: 10.1021/acsanm.4c02020. eCollection 2024 May 24.
Surface-bound molecular motors can drive the collective motion of cytoskeletal filaments in the form of nematic bands and polar flocks in reconstituted gliding assays. Although these "swarming transitions" are an emergent property of active filament collisions, they can be controlled and guided by tuning the surface chemistry or topography of the substrate. To date, the impact of surface topography on collective motion in active nematics is only partially understood, with most experimental studies focusing on the escape of a single filament from etched channels. Since the late 1990s, significant progress has been made to utilize the nonequilibrium properties of active filaments and create a range of functional nanodevices relevant to biosensing and parallel computation; however, the complexity of these swarming transitions presents a challenge when attempting to increase filament surface concentrations. In this work, we etch shallow, linear trenches into glass substrates to induce the formation of swarming nematic bands and investigate the mechanisms by which surface topography regulates the two-dimensional (2D) collective motion of driven filamentous actin (F-actin). We demonstrate that nematic swarms only appear at intermediate trench spacings and vanish if the trenches are made too narrow, wide, or tortuous. To rationalize these results, we simulate the F-actin as self-propelled, semiflexible chains subject to a soft, spatially modulated potential that encodes the energetic cost of bending a filament along the edge of a trench. In our model, we hypothesize that an individual filament experiences a penalty when its projected end-to-end distance is smaller than the trench spacing ("bending and turning"). However, chains that span the channel width glide above the trenches in a force- and torque-free manner ("crowd-surfing"). Our simulations demonstrate that collections of filaments form nematic bands only at intermediate trench spacings, consistent with our experimental findings.
在重构的滑动实验中，表面结合的分子马达能够驱动细胞骨架丝以向列带和极性群的形式进行集体运动。尽管这些“聚集转变”是活性丝碰撞的一种涌现特性，但可以通过调整底物的表面化学性质或形貌来对其进行控制和引导。迄今为止，表面形貌对活性向列相集体运动的影响仅得到部分理解，大多数实验研究集中在单根丝从蚀刻通道中逸出的情况。自20世纪90年代末以来，在利用活性丝的非平衡特性以及创建一系列与生物传感和并行计算相关的功能性纳米器件方面已经取得了重大进展；然而，当试图提高丝的表面浓度时，这些聚集转变的复杂性带来了挑战。在这项工作中，我们在玻璃基板上蚀刻浅的线性沟槽，以诱导向列带的形成，并研究表面形貌调节驱动丝状肌动蛋白（F-肌动蛋白）二维（2D）集体运动的机制。我们证明，向列群仅在中间沟槽间距处出现，如果沟槽做得太窄、太宽或太曲折则会消失。为了合理解释这些结果，我们将F-肌动蛋白模拟为自推进的半柔性链，其受到一种软的、空间调制的势场作用，该势场编码了沿沟槽边缘弯曲丝的能量成本。在我们的模型中，我们假设当单根丝的投影端到端距离小于沟槽间距时（“弯曲和转向”），它会受到惩罚。然而，跨越通道宽度的链以无外力和无扭矩的方式在沟槽上方滑动（“人群冲浪”）。我们的模拟表明，丝的集合仅在中间沟槽间距处形成向列带，这与我们的实验结果一致。
