The mammalian oocyte orchestrates the rate of ovarian follicular development

Abstract

The development of both the mammalian oocyte and the somatic cell compartments of the ovarian follicle is highly coordinated; this coordination ensures that the ovulated oocyte is ready to undergo fertilization and subsequent embryogenesis. Disruption of this synchrony results in oocyte developmental failure. Communication between the oocyte and companion somatic cells is essential for successful development of both follicular compartments. However, it was not previously known whether one cell type, either the somatic or the germ cell compartment, determines the overall rate of follicular development. To test the hypothesis that the oocyte orchestrates the rate of follicle development, mid-sized oocytes isolated from secondary follicles were transferred back to primordial follicles, the earliest stage of follicular development. This transfer doubled the rate of follicular development and the differentiation of follicular somatic cells. Oocyte development in these accelerated follicles appeared normal; recovered oocytes were competent to undergo fertilization and embryonic development. These results demonstrate that oocytes orchestrate and coordinate the development of mammalian ovarian follicles and that the rate of follicular development is based on a developmental program intrinsic to the oocyte.C omplex cell-to-cell interactions coordinate the development of ovarian follicles. The pathways of cellular communication include endocrine, autocrine, and paracrine regulators, and gap junctions. Coordination of the development of oocyte and somatic follicular compartments ensures that the ovulated oocyte is ready to undergo fertilization and subsequent embryogenesis. Disruption of this synchrony by inappropriately timed administration of exogenous gonadotropins can produce oocyte developmental failure (1). Communication between the oocyte and companion somatic cells is essential for successful development of both follicular compartments (2). The oocyte depends on its association with companion somatic granulosa cells to support its growth and development and to regulate the progression of meiosis. Likewise, oocytes promote granulosa cell proliferation, differentiation, and function. The communication between granulosa cells and oocytes is, therefore, bidirectional and occurs throughout follicular development (2, 3). In fact, follicular formation itself appears coordinated by a transcription factor, factor in the germline ␣ (FIG␣), expressed by the oocyte (4). Early follicular development depends on oocyte-secreted members of the transforming growth factor ␤ family, growth differentiation factor (GDF)-9, and bone morphogenic protein (BMP)-15 (5-7). These oocyte-derived paracrine factors also promote follicular somatic cell proliferation and steroidogenesis (8-10) and locally regulate gene expression in granulosa cells (10-13). Thus, communication between the oocyte and companion somatic cells is crucial for the development of both cell types, but how this complex interaction is coordinated was not previously known.At...

Effects of IGF-I bioavailability on bovine preantral follicular development in vitro

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FOXL2 versus SOX9: A lifelong “battle of the sexes”

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Identification of a novel C2 domain factor in ovaries of orange-spotted grouper (Epinephelus coioides)

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