Spatial confinement of active microtubule networks induces large-scale rotational cytoplasmic flow
Spatial confinement of active microtubule networks induces large-scale rotational cytoplasmic flow
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DOI：
10.1073/pnas.1616001114
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发表时间：
2017-03
期刊：
影响因子：
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通讯作者：
Kazuya Suzuki;Makito Miyazaki;Jun Takagi;Takeshi Itabashi;S. Ishiwata
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文献类型：
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作者：
Kazuya Suzuki;Makito Miyazaki;Jun Takagi;Takeshi Itabashi;S. Ishiwata
意义在微观尺度上，运动单元的集体行为可以诱导定向流体流动在更大的长度尺度上比单个单元基于它们的流体动力学相互作用。在这里，我们发现，在细胞质中的微管束的电机驱动的可伸展行为诱导在细胞大小的有限空间的长度尺度和时间尺度上的旋转流，是10- 100倍以上的涡流出现在散装空间。这些规模的差异来自机械力产生的微管束伸长附近的物理边界和传输这种力的微管网络。这些发现表明，微管细胞骨架不仅利用流体动力学的相互作用，但也机械相互作用，以诱导大规模的细胞质流动。运动单元通过流体动力相互作用的集体行为在比单个单元更大的长度尺度上诱导定向流体流动。在细胞中，由极性细丝和分子马达组成的活性细胞骨架系统驱动流体流动，这一过程称为细胞质流动。马达驱动的微管束的伸长在纯化的系统中产生类似于顺时针的流动;然而，仍不清楚微管束是否以及如何诱导大规模的定向流动，如在细胞中观察到的细胞质流动。在这里，我们采用非洲爪蟾卵提取物作为细胞质的模型系统，发现微管束伸长诱导定向流的长度尺度和时间尺度依赖于几何约束的存在。在动力蛋白活性较低时，驱动蛋白使微管成束和滑动，组织可伸展的微管束。在散装提取物中，可伸展的束彼此连接，形成一个随机的网络，和涡流的长度规模可比束长度不断出现，并持续1分钟，在多个地方。当提取物被包裹在液滴中时，可伸展的束推动液滴边界。这种推力引发了随机取向的束网络的对称性破坏，导致束排列成旋转的涡流结构。该涡旋诱导的旋转细胞质流的长度和时间尺度比散装浸提液中出现的涡旋流长10- 100倍。我们的研究结果表明，微管系统不仅使用流体动力学相互作用，但也机械相互作用，以诱导大规模的时间稳定的细胞质流。
Significance At the microscopic scale, collective behaviors of motile units can induce directed fluid flow on a larger length scale than individual units based on their hydrodynamic interactions. Here, we found that the motor-driven extensile behaviors of microtubule bundles in the cytoplasm induce rotational flow in a cell-sized confined space on length scale and timescale that were 10- to 100-fold longer than the vortex flows emerging in the bulk space. These scale differences were derived from mechanical force generation by microtubule bundle elongation near the physical boundary and the transmission of this force over the microtubule network. These findings suggest that the microtubule cytoskeleton utilizes not only hydrodynamic interactions but also mechanical interactions to induce large-scale cytoplasmic flow. Collective behaviors of motile units through hydrodynamic interactions induce directed fluid flow on a larger length scale than individual units. In cells, active cytoskeletal systems composed of polar filaments and molecular motors drive fluid flow, a process known as cytoplasmic streaming. The motor-driven elongation of microtubule bundles generates turbulent-like flow in purified systems; however, it remains unclear whether and how microtubule bundles induce large-scale directed flow like the cytoplasmic streaming observed in cells. Here, we adopted Xenopus egg extracts as a model system of the cytoplasm and found that microtubule bundle elongation induces directed flow for which the length scale and timescale depend on the existence of geometrical constraints. At the lower activity of dynein, kinesins bundle and slide microtubules, organizing extensile microtubule bundles. In bulk extracts, the extensile bundles connected with each other and formed a random network, and vortex flows with a length scale comparable to the bundle length continually emerged and persisted for 1 min at multiple places. When the extracts were encapsulated in droplets, the extensile bundles pushed the droplet boundary. This pushing force initiated symmetry breaking of the randomly oriented bundle network, leading to bundles aligning into a rotating vortex structure. This vortex induced rotational cytoplasmic flows on the length scale and timescale that were 10- to 100-fold longer than the vortex flows emerging in bulk extracts. Our results suggest that microtubule systems use not only hydrodynamic interactions but also mechanical interactions to induce large-scale temporally stable cytoplasmic flow.