Biology of Reproduction, Vol 10, 150-178, Copyright © 1974 by Society for the Study of Reproduction

Role of Hormones in Oocyte Maturation

¹ Johns Hopkins University, Department of Population Dynamics, School of Hygiene and Public Health, 615 N. Wolfe Street, Baltimore, Maryland 21205

In order for normal fertilization and embryonic development to occur, oocytes, during the course of meiosis, undergo a strict sequence of morphological and physiological transformations in the cytoplasm, nucleus, and at the cell surface. The nature of these maturational changes at various stages of meiosis and the role hormones play in them have been discusssed primarily on the basis of in vitro data. Gametogenic and endocrine functions are performed by the gonads of most species, and evidence presented here leads to the general conclusion that certain aspects of these two processes occur as a result of an interaction between germinal and somatic cells. Typically, gametic and somatic endocrine cells are in physical juxtaposition within an ovarian follicle, and structural and functional changes which occur in these cells during the course of gametogenesis appear to be important for allowing oocyte maturation to proceed as well as for regulating the process. A central event in the oocyte maturational process is interruption of oocyte arrest as characterized by the disintegration of the nucleus or germinal vesicle. Oocytes, prior to this event, differentiate through prophase I of meiosis and undergo the major portion of cytoplasmic and nuclear growth. Subsequent to nuclear breakdown, chromosomes proceed through the remaining meiotic events and differentiation of new functions occurs in the cytoplasm. Considerable evidence in nonmammalian species indicates that particular steroids or other low molecular weight substances mediate certain aspects of the cytoplasmic and nuclear maturation processes in oocytes. In mammals, a direct involvement of hormones (pituitary and/or ovarian) in initiating nuclear or cytoplasmic maturation has not been established, although the data are suggestive. Spontaneous oocyte maturation is a complicating factor in many species, and its relevance is discussed in terms of processes of follicular and oocyte differentiation. In amphibians, the nature of the steroids, the time at which they function, and the functions they perform vary in relation to particular stages of meiosis. Thus, ovarian estrogenic steroids are required (indirectly) for oocyte growth, their function being to stimulate hepatic synthesis of vitellogenin, the major cytoplasmic yolk platelet precursor. Subsequent to its release into the circulation, vitellogenin is sequestered into the oocyte by a micropinocytotic process at the oocyte surface and undergoes transformation into yolk within the oocyte. In contrast, reinitiation of the meiotic process (germinal vesicle breakdown) occurs in direct response to certain nonestrogenic steroids (progestational, adrenocortical, androgenic) and proceeds in vitro to the typical in vivo stage of second metaphase arrest. Somatic follicle cells appear to be the cellular source of both the estrogenic steroids required for vitellogenesis or oocyte growth and the "progestational-like" steroids involved in nuclear and cytoplasmic maturation including and proceeding from nuclear breakdown. Presumably, follicle cells alter their steroidogenic function during the course of oocyte and follicle differentiation. Following and/or in synchronization with induced nuclear disintegration and meiosis, numerous time-dependent maturational changes occur in the nuclear contents, oocyte cytoplasm (including cortical granules), and in the relationship between the oocyte surface and associated membranes. These are important in establishing conditions for fertilization or activation, ovulation, block to polyspermy, cleavage, and embryogenesis. Although many of these maturational processes are responses to the same steroidal stimuli which initiate nuclear breakdown, mediation of these changes in many cases occurs in the cytoplasm independent of the nucleus.