Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades

All metazoans that reproduce sexually have the ability to form gametes. The two types of gametes, the egg and the sperm, arise from germ cells, undergo extensive differentiation, and are destined to unite. The outcome of their union, the zygote, maintains and propagates the characteristics of the species. The zygote inherits from the egg not only genetic material but also its cytoplasm, which supports the development of the early embryo through precise expression patterns of maternally inherited messages. The hierarchical organization of these translation regulatory mechanisms is unveiled in the report by Padmanabhan and Richter (2006) in this issue of Genes & Development.

Mechanisms for establishing the germline and carrying out oogenesis in evolutionarily distant animals exhibit certain common themes. Gametes develop from primordial germ cells (PGC) that are set aside during early embryogenesis (Matova and Cooley 2001). In most metazoans, PGCs have an extragonadal origin and migrate to reach the somatic gonad, where they proliferate by mitosis to form oocytes in females (Matova and Cooley 2001). Oocytes, in turn, enter meiosis, only to be arrested at the prophase of the first meiotic division (Sagata 1996). This first meiotic arrest may last up to a few years in Xenopus or several decades in humans, and is characterized by synthesis and storage of large quantities of dormant mRNA (LaMarca et al. 1973; Rodman and Bachvarova 1976). When later translated, these maternal mRNAs drive the oocyte's re-entry into meiosis (Gebauer et al. 1994; Stebbins-Boaz et al. 1996; Mendez et al. 2000) and control the rate of mitosis during the cleavage divisions after fertilization (Groisman et al. 2000; Oh et al. 2000; Uto and Sagata 2000).

The resumption of meiosis marks the onset of oocyte maturation and is stimulated by progesterone in Xenopus (Bayaa et al. …