Molecular and cellular changes associated with maturation and early development of sheep eggs

It has long been postulated in non-mammalian species that successful embryogenesis depends directly on an ordered sequence of events in oogenesis (Wilson, 1925). Oogenesis in these species is recognized as the phase of synthesis and storage of intracellular components whilst early embryogenesis is the period of distribution and utilization of stored product. A clear example of the interrelationship between oogenesis and embryogenesis is provided by the eggs of the toad, Xenopus laevis. In this species the single-celled egg at fertilization contains all the components and information required for the development of the swimming tadpole which consists of approximately 50 000 cells (Gurdon. 1974). Although this extreme degree of independence from extracellular support is unlikely to apply directly to mammals, it is nevertheless critical to identify the extent to which mammalian embryogenesis is regulated by the products of oogenesis. It is our purpose to answer this question by describing the intracellular events during oogenesis in sheep and relating these to the control of fertilization and early development. Over what developmental time-scale does oogenesis occur in mammals? The process is initiated when the primordial germ cells invade the genital ridge of the embryo. After colonization of the early gonad the germ cells undergo a period of mitotic activity before entering meiosis and progressing to the dictyate stage of meiotic prophase. At this point the cell cycle is interrupted and the oocyte, containine a large nucleus referred to as a germinal vesicle (GV), remains in meiotic arrest for all but the last few hours of oogenesis. In addition to nuclear arrest the oocyte, surrounded by a single layer of flattened cells, constitutes part of the non-growing or resting pool of primordial Follicles for much of its postnatal existence. The limited amount of biochemical evidence available about oocytes in primordial follicles suggests that they are merely synthesizing 'housekeeping' proteins during the resting period. However, a small number of primordial follicles enter the growing pool each day. It is with the developmental events initiated in the oocyte at this time and terminating during embryogenesis when maternal regulation ceases that this paper deals. Although the sheep oocyte and embryo will serve as a model for the paper, information from other mammals is used to compensate for deficiences in our knowledge of oogenesis in this species. At least three distinct developmental programmes direct the molecular changes which occur during oogenesis and early embryogenesis. A growth programme regulates differentiation in the immature oocyte (Canipari et al., 1984) while a separate maturation programme regulates the reprogramming of the oocyte before ovulation. The entry of the spermatozoon initiates an early embryonic programme which persists until maternal regulation is terminated and development becomes directed by the embryonic genome (Howlett & Bolton, 1985). A later embryonic programme, which will not be discussed in this communication, begins with the expression of the