Comparative cellular biology of vertebrate primordial oocytes

Resum

In sexually reproducing animals, female germline cells called primordial oocytes are formed before the time of birth. They represent the fixed reserve from which fertilizable eggs are produced during the entire reproductive lifespan of the animal. In mammals, primordial oocytes have the remarkable ability to remain dormant for a long time, spanning just a few weeks in mice to several decades in humans. As the donor of virtually all the organelles in the developing embryo, it is necessary to understand the mechanisms by which oocytes maintain fitness for decades and why they eventually fail with age. Moreover, in the primordial oocytes of several species studied thus far, a Balbiani body, a phase-separated compartment consisting of organelles including mitochondria and Golgi apparatus, and ribonucleoprotein (RNP) particles has been observed. The Balbiani body is present only in primordial oocytes and is disassembled in growing oocytes. Thus, the Balbiani body is linked to dormancy. However, the cellular biology of primordial oocytes still remains largely unexplored. In this project, we developed enabling methods for live-imaging based comparative characterization of Xenopus, mouse and human primordial oocytes. This allowed us to address key questions about the cell biology of primordial oocytes such as the activity and dynamics of organelles and their association with dormancy. We show that primordial oocytes in all three vertebrate species contain active lysosomes, Golgi apparatus and mitochondria. While human and Xenopus oocytes have a Balbiani body characterized by a dense accumulation of mitochondria in their cytoplasm, we did not find a Balbiani body in mouse oocytes. Instead, we demonstrate what was previously used as a marker for the Balbiani body in mouse primordial oocytes is in fact a ring-shaped Golgi apparatus that is not functionally associated with oocyte dormancy. Our work provides the first insights into the organisation of the cytoplasm in mammalian primordial oocytes, and clarifies relative advantages and limitations of choosing different model organisms for studying oocyte dormancy.