Endosomal-lysosomal organellar assembly (ELYSA) structures coordinate lysosomal degradation systems through mammalian oocyte-to-embryo transition

Abstract Mouse oocytes undergo drastic changes in organellar composition and their activities during maturation from the germinal vesicle (GV) to meiosis II (MII) stage. After fertilization, the embryo degrades parts of the maternal components via lysosomal degradation systems, including autophagy and endocytosis, as zygotic gene expression begins during embryogenesis. Here, we demonstrate that endosomal-lysosomal organelles form large spherical assembly structures, termed ELYSAs, in mouse oocytes. ELYSAs are observed in GV oocytes, attaining sizes up to 7–8 μm in diameter in MII oocytes. ELYSAs comprise tubular-vesicular structures containing endosomes, lysosomes, autophagosome-like membranes in the outer layer, with cytosolic components contained within. The V1-subunit of vacuolar ATPase tends to localize to the periphery of ELYSAs in MII oocytes. After fertilization, the V1-subunit is recruited to immature endosomes and lysosomes as ELYSAs are gradually disassembled at the 2-cell stage, which leads to further acidification of endosomal-lysosomal organelles. These findings suggest that the ELYSAs maintain endosomal-lysosomal activity in a static state in oocytes for timely activation during early development.