Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation

Vanderhyden, Barbara C.; Caron, Philip J.; Buccione, Roberto; Eppig, John J.

doi:10.1016/0012-1606(90)90081-s

Cited by 311 publications

(245 citation statements)

References 34 publications

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“…Hyaluronic acid synthesis and cumulus expansion can be stimulated in vitro by treatment with FSH (19,20). Granulosa cells of secondary or very early antral follicles do not undergo expansion when stimulated by FSH (21). Cumulus expansion, however, did occur when the oocytecumulus cell complexes were isolated from the large antral follicles of 12͞0 ovaries just 9 days after grafting (Fig.…”

Section: Resultsmentioning

confidence: 97%

The mammalian oocyte orchestrates the rate of ovarian follicular development

Eppig

Wigglesworth²,

Pendola³

2002

Proc. Natl. Acad. Sci. U.S.A.

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441

267

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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...

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Section: Resultsmentioning

confidence: 97%

The mammalian oocyte orchestrates the rate of ovarian follicular development

Eppig

Wigglesworth²,

Pendola³

2002

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

441

267

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“…Oocytes affect the development and function of all stages of follicles beginning with the formation of primordial follicles (Soyal et al, 2000). Oocytes promote the primary to secondary follicle transition (Dong et al, 1996;Elvin et al, 1999b;Galloway et al, 2000;Juengel et al, 2002;Latham et al, 2004), granulosa cell proliferation and differentiation before the luteinizing hormone (LH) surge (Gilchrist et al, 2003;Gilchrist et al, 2000;Gilchrist et al, 2001;Otsuka et al, 2005;Otsuka et al, 2000;Vanderhyden et al, 1992;Vitt et al, 2000), the preantral to antral follicle transition (Diaz et al, 2007a;Diaz et al, 2007b;Orisaka et al, 2006) and cumulus expansion and ovulation after the LH surge Diaz et al, 2006;Dragovic et al, 2005;Dragovic et al, 2007;Joyce et al, 2001;Su et al, 2004;Vanderhyden et al, 1990).…”

Section: Introductionmentioning

confidence: 99%

Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells

et al. 2008

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*Oocyte-derived bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) are key regulators of follicular development. Here we show that these factors control cumulus cell metabolism, particularly glycolysis and cholesterol biosynthesis before the preovulatory surge of luteinizing hormone. Transcripts encoding enzymes for cholesterol biosynthesis were downregulated in both Bmp15-/-and Bmp15 -/-Gdf9 +/-double mutant cumulus cells, and in wild-type cumulus cells after removal of oocytes from cumulus-cell-oocyte complexes. Similarly, cholesterol synthesized de novo was reduced in these cumulus cells. This indicates that oocytes regulate cumulus cell cholesterol biosynthesis by promoting the expression of relevant transcripts. Furthermore, in wild-type mice, Mvk, Pmvk, Fdps, Sqle, Cyp51, Sc4mol and Ebp, which encode enzymes required for cholesterol synthesis, were highly expressed in cumulus cells compared with oocytes; and oocytes, in the absence of the surrounding cumulus cells, synthesized barely detectable levels of cholesterol. Furthermore, coincident with reduced cholesterol synthesis in double mutant cumulus cells, lower levels were also detected in cumulus-cell-enclosed double mutant oocytes compared with wild-type oocytes. Levels of cholesterol synthesis in double mutant cumulus cells and oocytes were partially restored by co-culturing with wild-type oocytes. Together, these results indicate that mouse oocytes are deficient in synthesizing cholesterol and require cumulus cells to provide products of the cholesterol biosynthetic pathway. Therefore, oocyte-derived paracrine factors, particularly, BMP15 and GDF9, promote cholesterol biosynthesis in cumulus cells, probably as compensation for oocyte deficiencies in cholesterol production.

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“…Rat granulosa cells have been shown to consist of two distinct cell types that can be separated according to size (Telfer et al, 1988; Hartshorne, 1990;Vanderhyden et al, 1990;Rao et al, 1991). Rao et al (1991) consider that the two types of granulosa cell differ in their degree of differentiation, and that this is inde¬ pendent of the cell cycle within the follicle.…”

Section: Introductionmentioning

confidence: 99%