Estradiol-17β production in amago salmon (Oncorhynchus rhodurus) ovarian follicles: Role of the thecal and granulosa cells
TL;DR: A two-cell-type model for the production of follicular estrogens, the thecal layer possibly contributing to estradiol-17β production by synthesizing androgens which are transferred to the granulosa layer and aromatized to est radiol- 17β is suggested.
About: This article is published in General and Comparative Endocrinology.The article was published on 1982-08-01. It has received 217 citations till now. The article focuses on the topics: Granulosa cell & Follicular phase.
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TL;DR: The lability of sex-determination systems in fish makes some species sensitive to environmental pollutants capable of mimicking or disrupting sex hormone actions, and such observations provide important insight into potential impacts from endocrine disruptors, and can provide useful monitoring tools for impacts on aquatic environments.
2,283 citations
TL;DR: The mechanisms that control oocyte growth are addressed in this review, albeit that the available information, as in all other vertebrates, is very limited.
Abstract: Oocyte growth and development is an important issue in fish and fisheries biology. This paper reviews the information available on oocyte growth patterns and the rates and dynamics of oocyte growth in teleosts. In synchronous spawners, the weight of the gonad may represent as much as 40% of the overall body weight of the fish. In asynchronous spawners, the weight of the mature ovary is considerably less than in synchronous ovulators, but the ovary shows a more regular periodicity and may grow repeatedly many times during the breeding season. There is a huge variability in egg size in teleosts, with the largest known measuring up to 8 cm in diameter. Within the limits of variance set by genetic constraints, egg size may vary between populations of the same species. Oocytes in all teleosts undergo the same basic pattern of growth: oogenesis, primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation and ovulation. The mechanisms that control oocyte growth are addressed in this review, albeit that the available information, as in all other vertebrates, is very limited. The main hormones that have been shown to affect ovarian growth are gonadotrophin, thyroid hormones, growth hormone, insulin and insulin-like growth factors. An overview of the determinants of fecundity, with particular reference to oocyte recruitment and atresia, is the focus of the second part of the paper. Genetics and nutrition have major effects on fecundity, and studies so far suggest that the determinants of fecundity usually operate during the early part of gametogenesis. The role of atresia in determining fecundity is less clear. The final part of this review highlights some areas of study that are priorities for research on ovarian development in fish.
782 citations
TL;DR: Findings on the identification of steroidal mediators involved in each process of gametogenesis, and the sites and mechanisms of action of the mediators are reviewed.
Abstract: The pituitary-gonadal axis plays an important role in regulating gametogenesis in vertebrates. In most cases, gonadotropins act through the biosynthesis of gonadal steroid hormones which in turn mediate various stages of gametogenesis. A series of studies in our laboratory using several species of teleost fishes as experimental animals has provided new information about the endocrine regulation of gametogenesis, including oocyte growth, oocyte maturation, spermatogenesis and sperm maturation. This article briefly reviews our findings on the identification of steroidal mediators involved in each process of gametogenesis, and the sites and mechanisms of action of the mediators. These observations collectively demonstrate the appropriateness of using teleost fishes as valid models for examining hormonal influences on gametogenesis. Such models could also have applications and validity for vertebrates in general.
733 citations
TL;DR: This article showed that oocyte maturation is a three-step induction process involving gonadotropin (LH), maturation-inducing hormone (MIH), and maturationpromoting factor (MPF).
Abstract: A period of oocyte growth is followed by a process called oocyte maturation (the resumption of meiosis) which occurs prior to ovulation and is a prerequisite for successful fertilization. Our studies using fish models have revealed that oocyte maturation is a three-step induction process involving gonadotropin (LH), maturation-inducing hormone (MIH), and maturation-promoting factor (MPF). LH acts on the ovarian follicle layer to produce MIH (17α, 20β-dihydroxy-4-pregnen-3-one, 17α, 20β-DP, in most fishes). The interaction of ovarian thecal and granulosa cell layers (two-cell type model), is required for the synthesis of 17α,20β-DP. The dramatic increase in the capacity of postvitellogenic follicles to produce 17α,20β-DP in response to LH is correlated with decreases in P450c17 (P450c17-I) and P450 aromatase (oP450arom) mRNA and increases in the novel form of P450c17 (P450c17-II) and 20β-hydroxysteroid dehydrogenase (20β-HSD) mRNA. Transcription factors such as Ad4BP/SF-1, Foxl2, and CREB may be involved in the regulation of expression of these steroidogenic enzymes. A distinct family of G-protein-coupled membrane-bound MIH receptors has been shown to mediate non-genomic actions of 17α, 20β-DP. The MIH signal induces the de novo synthesis of cyclin B from the stored mRNA, which activates a preexisting 35 kDa cdc2 kinase via phosphorylation of its threonine 161 by cyclin-dependent kinase activating kinase, thus producing the 34 kDa active cdc2 (active MPF). Upon egg activation, MPF is inactivated by degradation of cyclin B. This process is initiated by the 26S proteasome through the first cut in its NH2 terminus at lysine 57.
698 citations
TL;DR: This chapter discusses the functional morphology of teleost gonads and a two cell-type model involving thecal and granulosa cell layers has been proposed for the production of these two steroids for the first time in lower vertebrates.
Abstract: Publisher Summary This chapter discusses the functional morphology of teleost gonads. Information presented in this chapter indicates that there are several processes of germ cell development, which are closely associated with changes in cellular activities of somatic cell elements. Recent studies on biochemical aspects of vitellogenesis in teleosts have shown that the hepatic and ovarian yolk proteins are similar to those of amphibian species. An in vitro method involving the separation of the follicular components has facilitated investigations of the detailed mechanism of the production of two major follicular steroid hormones. As a result of the usage of this technique, a two cell-type model involving thecal and granulosa cell layers has been proposed for the production of these two steroids for the first time in lower vertebrates. With further refinements this well characterized incubation procedure should provide an excellent system for studying the molecular basis of the mechanism of gonadotropin action on follicular steroidogenesis.
573 citations
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TL;DR: The results indicated that follicular development and granulosa cell differentiation are dependent on steroid-protein hormone regulation of hormone specific receptors.
Abstract: The effects of estradiol, FSH and LH on ovarian follicular development and granulosa cell differentiation were examined in the immature rat hypophysectomized on day 24 of age. Administration of estradiol to hypophysectomized rats for 4 days stimulated the growth of large preantral follicles with a concomitant 1.5-fold increase in FSH receptor content and a 4-fold decrease in LH receptor content in the granulosa cells. When highly purified hFSH was administered alone, receptor content for FSH increased progressively for 4 days while receptor for LH remained essentially unchanged. However, when rats were pretreated with estradiol, the response of follicles to FSH was markedly enhanced as indicated by the appearance of large, antral follicles and elevated receptor content for both FSH and LH. Receptor content for FSH increased markedly in response to hFSH following only one day of estradiol pretreatment, while receptor content for LH increased most rapidly in response to hFSH after 3 days of estradiol pretreatment. LH administered to rats possessing large preovulatory follicles caused luteinization of granulosa cells and a marked decline in receptor content for both gonadotropins within 24 h. Receptor content remained low even 48 h after LH administration when granulosa cells were fully luteinized. These results indicated that follicular development and granulosa cell differentiation are dependent on steroid-protein hormone regulation of hormone specific receptors.
513 citations
TL;DR: Results suggest that FSH administered in vivo may act on granulosa cells to induce or activate receptors for I_H (hCG) and 3β-hydroxysteroid dehydrogenase activity as well as stimulate follicle-stimulating hormone in ovarian development.
Abstract: The role of follicle-stimulating hormone (FSH) in ovarian development was studied in immature rats. Autoradiographic analysis of gonadotropin binding sites revealed that FSH bound to granulosa cells while human chorionic gonadotropin (hCG) bound to thecal and interstitial cells in 25-day-old rats. Following 2 days of treatment with rat FSH (rFSH), hCG binding was observed in the granulosa cells of stimulated follicles. Histochemical localization of 3β-hydroxysteroid dehydrogenase activity also was apparent in granulosa cells from animals treated with FSH. Granulosa cells from rats treated with either hCG or diethylstilbestrol for 2 days failed to show consistent hCG binding. Isolated granulosa cells from intact and hypophysectomized rats treated with FSH demonstrated a greater binding capacity for hCG than granulosa cells removed from saline-treated animals. These results suggest that FSH administered in vivo may act on granulosa cells to induce or activate receptors for I_H (hCG) and 3β-hydroxysteroid de...
425 citations
TL;DR: It is concluded that the theca interna gland cells and the interstitial gland cells most probably constitute the oestrogen-producing system in the ovary but that these cells are functionally dependent on the system granulosa-corpus luteum cells.
Abstract: SUMMARY
The present paper is concerned with an investigation on the site of production of oestrogen in the rat ovary by a method designed to yield more direct evidence than hitherto available.
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A dissection technique was devised permitting isolation of small cell aggregates from the rat ovary containing only one endocrine cell system.
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Such cell systems alone or in certain combinations were auto-transplanted to the anterior chamber of the eye of spayed animals, a contiguous vaginal autotransplant serving as an indicator of the oestrogenic activity of the ovarian grafts. The specificity of this indicator system to oestrogen is discussed.
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As to the ovarian grafts, only in exceptional cases did they produce systemic hormonal effects, and interference by oestrogenic substances from other sources or by metabolites from steroids released in the grafts was excluded by the appearance of the vagina in situ and a control vaginal transplant in the other eye.
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The following isolated cell systems were transplanted: interstitial cells, theca interna cells, corpus luteum cells and granulosa cells. All of these cell types were able to survive when grafted. In spite of the complex topography of the rat ovary, it proved possible to secure a certain number of grafts consisting of interstitial cells only or of theca interna cells only. Uncontaminated grafts of granulosa cells and corpus luteum cells could be readily obtained. The dissection technique thus provides a tool for studying ovarian tumours experimentally induced in grafts originally containing only one type of endocrine cells.
The transplanted granulosa cells were luteinised and formed cell aggregates of the same histological structure as the normal corpus luteum. The following combinations of cell systems were studied: interstitial cells + corpus luteum cells and theca interna cells + granulosa cells or corpus luteum cells.
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Secretion of oestrogen was never recorded in transplants of the pure cell systems but only in transplants containing theca interna cells or interstitial cells combined with granulosa cells or corpus luteum cells. The validity of these results is discussed and it is excluded that errors in the experimental method might have caused the negative results with the isolated cell systems.
Isolated follicles were not transplanted, but the material permitted an indirect analysis of the oestrogen-producing capacity of follicles in different developmental stages, showing that this probably arises with the development of the theca interna gland cells.
It was found that a single follicle with few theca interna cells could produce a local oestrogenic effect on the indicator epithelium, while a single follicle of preovulatory size and well-developed thecal gland was able to produce full oestrous reaction of the vagina and uterus in situ.
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It is concluded from these results that the production of oestrogen is dependant on an interplay between theca interna gland cells or interstitial cells and corpus luteum cells or granulosa cells.
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The primary source of oestrogen in the ovary is discussed against the background of the literature and the present findings. It is concluded that the theca interna gland cells and the interstitial gland cells most probably constitute the oestrogen-producing system in the ovary but that these cells are functionally dependent on the system granulosa-corpus luteum cells.
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The possibility of intra-ovarian mechanisms operating in both directions between the two principal cell-systems — the oestrogen- and the progestin-producing — is discussed.
230 citations
TL;DR: Plasma cortisol levels are at a high during the season of poor feeding when mobilisation of energy reserves is likely to be greatest and steroid concentration in males showed small significant seasonal changes.
215 citations
TL;DR: It is concluded that the theca is the site of follicular androgen production and that LH regulates androgen secretion by rat ovarian follicles, and provides the androgen precursor needed for follicular estradiol-17beta synthesis.
Abstract: Theca and granulosa isolated from proestrous rat ovarian follicles were cultured for 72 h in the presence or absence of highly purified luteinizing hormone (LH, 0.1 microng/ml) and/or follicle-stimulating hormone (FSH, 0.1 microng/ml). Medium was collected and replaced at 3, 6, 12, 24, 48, and 72 h of culture and measured for testosterone by radioimmunoassay. Pieces of isolated theca secreted androgen; androgen production was greatest during the first 12 h of culture. Addition of highly purified LH to the culture medium produced a significant increase (P less than 0.001) in the thecal androgen secretion, while addition of highly purified FSH had no significant effect. Addition of LH + FSH to culture medium produced the same effect as addition of LH alone. The response of the theca to LH was dose-dependent with doses of 0.01 microng/ml or greater eliciting a maximum response. The addition of eoxgenous progesterone (5 x 10(-7)M) to culture medium had no effect on thecal androgen production. Thecal androgen secretion was the same in the presence or absence of fetal calf serum. Since the testosterone antibody used was not entirely specific for testosterone, testosterone and the cross-reacting androgen, 17beta-hydroxy-5alpha-androstan-3-one (DHT), were chromatographically isolated from samples and assayed separately. The androgen measured in culture medium was found to consist primarily of testosterone; DHT was present in much lower concentrations. Granulosa cells isolated from the same follicles as the theca and grown in monolayer culture produced negligible amounts of androgen. It is concluded that the theca is the site of follicular androgen production and that LH regulates androgen secretion by rat ovarian follicles. The results suggest that the theca provides the androgen precursor needed for follicular estradiol-17beta synthesis.
195 citations