Mouse germline cysts contain a fusome-like structure that mediates oocyte development

Mouse female primordial germ cells (PGCs) undergo five synchronous, incomplete mitotic divisions and send each resulting germline cyst into meiosis to fragment and produce 4–6 oocytes and 24–26 supportive nurse cells. However, no system of polarity has been found to specify mammalian oocytes, link them appropriately to nurse cells and enable them to acquire high-quality organelles and cytoplasm. We report that mouse cysts develop an asymmetric Golgi, endoplasmic reticulum (ER), and microtubule-associated ‘fusome,’ similar to the oocyte-determining fusome in Drosophila cysts. The mouse fusome distributes asymmetrically among cyst cells and enriches in future oocytes with Pard3 and Golgi-endosomal UPR (unfolded protein response) proteins. Spindle remnants rich in stable acetylated microtubules, like those building the Drosophila and Xenopus fusomes, transiently link early mouse cyst cells for part of each cell cycle. A non-random gap in these microtubules predicts that initial cysts fragment into similar six-cell derivatives, providing a potential mechanism for producing uniform oocytes. Together with previous studies, these results argue that a polarized fusome underlies the development of female gametes from the PGC to follicular oocyte stages in diverse animals including mammals.