Bulk Actin Dynamics Drive Phase Segregation in Zebrafish Oocytes

• Published in: Cell 2019-05, Vol.177 (6), p.1463-1479.e18
• Main Authors: Shamipour, Shayan, Kardos, Roland, Xue, Shi-Lei, Hof, Björn, Hannezo, Edouard, Heisenberg, Carl-Philipp
• Format: Article
• Language: English
• Subjects: actin comets; Actins - metabolism; Actins - physiology; actomyosin flows; Animals; Cell Cycle - physiology; Cell Polarity - physiology; Cytoplasm - metabolism; Egg Yolk - physiology; Oocytes - metabolism; ooplasmic streaming; phase segregation; Polymerization; zebrafish; Zebrafish - embryology; Zebrafish - metabolism; Zebrafish Proteins - metabolism; Zygote
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2019.04.030

Segregation of maternal determinants within the oocyte constitutes the first step in embryo patterning. In zebrafish oocytes, extensive ooplasmic streaming leads to the segregation of ooplasm from yolk granules along the animal-vegetal axis of the oocyte. Here, we show that this process does not rely on cortical actin reorganization, as previously thought, but instead on a cell-cycle-dependent bulk actin polymerization wave traveling from the animal to the vegetal pole of the oocyte. This wave functions in segregation by both pulling ooplasm animally and pushing yolk granules vegetally. Using biophysical experimentation and theory, we show that ooplasm pulling is mediated by bulk actin network flows exerting friction forces on the ooplasm, while yolk granule pushing is achieved by a mechanism closely resembling actin comet formation on yolk granules. Our study defines a novel role of cell-cycle-controlled bulk actin polymerization waves in oocyte polarization via ooplasmic segregation. [Display omitted] •Bulk actin polymerization waves move through the oocyte from animal to vegetal•An animal-to-vegetal actin gradient triggers animal-directed actin flows•Actin flows drag the ooplasm toward the animal pole via differential friction•Actin comets formed on yolk granules push them toward the vegetal pole Phase segregation of ooplasm and yolk granules in zebrafish oocytes relies on bulk actin polymerization waves, which pull the ooplasm toward the animal pole by bulk actin flows and push the yolk granules toward the vegetal pole through the formation of actin comets on the yolk granule surface.