The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte

Key Points The growth and the onset of meiotic maturation of the mammalian oocyte are controlled by bidirectional interactions between the oocyte and the surrounding somatic cells. Junctional complexes and transzonal projections (TZPs) form the structural basis for the passage of signalling molecules and metabolic substrates that support oocyte growth. The meiotic spindle forms through self-organization of microtubules and motor proteins in response to a RAN GTPase-mediated chromatin signal in the absence of centriole-containing centrosomes. Meiotic chromatin provides a signal for the establishment of oocyte cortical polarity, which required for asymmetric meiotic cell divisions and leads to polar body extrusion. Asymmetric positioning of the meiosis I spindle is established through actin-based forces that are regulated by actin nucleating factors, including a formin-family protein and the actin-related protein 2/3 (ARP2/3) complex. Actin-driven cytoplasmic streaming contributes to the establishment and maintenance of oocyte polarity, and the parameters of post-fertilization streaming may be prognostic of the developmental potential of the embryo. The growth and maturation of mammalian oocytes rely on the communication with ovarian somatic cells as well as on dynamic cytoskeleton-based events. Increasing evidence suggests that self-organizing microtubules and motor proteins direct meiotic spindle assembly and actin filaments control spindle positioning and oocyte polarity, while meiotic chromatin provides key instructive signals. Mammalian oocytes go through a long and complex developmental process while acquiring the competencies that are required for fertilization and embryogenesis. Recent advances in molecular genetics and quantitative live imaging reveal new insights into the molecular basis of the communication between the oocyte and ovarian somatic cells as well as the dynamic cytoskeleton-based events that drive each step along the pathway to maturity. Whereas self-organization of microtubules and motor proteins direct meiotic spindle assembly for achieving genome reduction, actin filaments are instrumental for spindle positioning and the establishment of oocyte polarity needed for extrusion of polar bodies. Meiotic chromatin provides key instructive signals while being 'chauffeured' by both cytoskeletal systems.