Institute of Science and Technology Austria, Klosterneuburg, Austria.
Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.
PLoS Biol. 2023 Jun 8;21(6):e3002146. doi: 10.1371/journal.pbio.3002146. eCollection 2023 Jun.
Dynamic reorganization of the cytoplasm is key to many core cellular processes, such as cell division, cell migration, and cell polarization. Cytoskeletal rearrangements are thought to constitute the main drivers of cytoplasmic flows and reorganization. In contrast, remarkably little is known about how dynamic changes in size and shape of cell organelles affect cytoplasmic organization. Here, we show that within the maturing zebrafish oocyte, the surface localization of exocytosis-competent cortical granules (Cgs) upon germinal vesicle breakdown (GVBD) is achieved by the combined activities of yolk granule (Yg) fusion and microtubule aster formation and translocation. We find that Cgs are moved towards the oocyte surface through radially outward cytoplasmic flows induced by Ygs fusing and compacting towards the oocyte center in response to GVBD. We further show that vesicles decorated with the small Rab GTPase Rab11, a master regulator of vesicular trafficking and exocytosis, accumulate together with Cgs at the oocyte surface. This accumulation is achieved by Rab11-positive vesicles being transported by acentrosomal microtubule asters, the formation of which is induced by the release of CyclinB/Cdk1 upon GVBD, and which display a net movement towards the oocyte surface by preferentially binding to the oocyte actin cortex. We finally demonstrate that the decoration of Cgs by Rab11 at the oocyte surface is needed for Cg exocytosis and subsequent chorion elevation, a process central in egg activation. Collectively, these findings unravel a yet unrecognized role of organelle fusion, functioning together with cytoskeletal rearrangements, in orchestrating cytoplasmic organization during oocyte maturation.
细胞质的动态重排是许多核心细胞过程的关键，例如细胞分裂、细胞迁移和细胞极化。细胞骨架的重排被认为是细胞质流动和重排的主要驱动因素。相比之下，关于细胞器大小和形状的动态变化如何影响细胞质组织，人们知之甚少。在这里，我们发现在成熟的斑马鱼卵母细胞中，皮质颗粒（Cgs）的表面定位是通过卵黄颗粒（Yg）融合和微管星形成和移位的联合作用来实现的。我们发现，Cgs 通过 Ygs 融合并向卵母细胞中心压缩引起的径向向外细胞质流动，被推向卵母细胞表面，以响应 GVBD。我们进一步表明，用小 Rab GTPase Rab11 装饰的小泡与 Cgs 一起积聚在卵母细胞表面，Rab11 是囊泡运输和胞吐作用的主要调节因子。这种积累是通过无中心体微管星形成来实现的，微管星形成是由 GVBD 释放 CyclinB/Cdk1 诱导的，并且由于优先与卵母细胞肌动蛋白皮层结合，这些微管星具有向卵母细胞表面的净运动。我们最后证明，Rab11 对卵母细胞表面 Cgs 的装饰对于 Cg 胞吐作用和随后的卵壳隆起是必需的，这是卵激活过程中的一个核心过程。总之，这些发现揭示了细胞器融合与细胞骨架重排一起在卵母细胞成熟过程中协调细胞质组织的作用。
