Spatial confinement of active microtubule networks induces large-scale rotational cytoplasmic flow

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 11; pp. 2922 - 2927
• Main Authors: Suzuki, Kazuya, Miyazaki, Makito, Takagi, Jun, Itabashi, Takeshi, Ishiwata, Shin’ichi
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 14.03.2017
• Subjects: Biological Sciences; Cells; Cytoplasm; Cytoskeleton; Frogs; self-organization; symmetry breaking; active matter; cytoskeleton; directed flow
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1616001114

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.