Steroid biosynthesis by ovarian follicles of Xenopus laevis in Vitro during oogenesis

Mulner, Odile; Thibier, Catherine; Ozon, René

doi:10.1016/0016-6480(78)90250-2

Cited by 35 publications

(10 citation statements)

References 19 publications

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“…4). These results elaborate on earlier studies describing the presence of steroid metabolism in ovarian follicles (20)(21)(22)(23) by looking specifically at the metabolism of progesterone in isolated oocytes and by identifying CYP17 as the primary enzyme mediating this process. The rapid metabolism of progesterone injected directly into oocytes suggests that CYP17 might be expressed in the oocytes themselves, rather than in contaminating stromal cells; however, the ability of progesterone to rapidly enter and leave oocytes qualifies this conclusion.…”

Section: Discussionsupporting

confidence: 77%

Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation

Lutz

Cole

Gupta

et al. 2001

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

156

142

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Steroid-induced maturation of Xenopus oocytes has long served as a model for studying meiosis. Progesterone has been considered the relevant steroid controlling maturation, perhaps through interactions with classical progesterone receptors. In this study, we provide evidence that androgens, rather than progesterone, are the physiologic mediators of Xenopus oocyte maturation. Androgens were equal or more potent activators of maturation in vitro relative to progesterone and were significantly more abundant in the serum and ovaries of ␤-human chorionic growth hormone-stimulated frogs. Androgen action appeared to be mediated by classical androgen receptors (ARs) expressed in oocytes, as androgen-induced maturation and signaling was specifically attenuated by AR antagonists. Interestingly, we found that progesterone was rapidly converted to the androgen androstenedione in isolated oocytes by the enzyme CYP17, suggesting that androgens may be promoting maturation even under conditions typical for ''progesterone-mediated'' maturation assays. Androgens are thought to play an important role in ovarian development as well as pathology, and signaling through the AR may prove to be a major regulatory mechanism mediating these processes.T he phenomenon of progesterone-induced maturation of Xenopus oocytes has served as an in vitro experimental model for studying meiosis and cell cycle regulation for over 30 years (1-3), with recent work implicating the classical nuclear͞cytoplasmic progesterone receptor (PR) as the mediator of these processes (4, 5). Although progesterone is a potent promoter of Xenopus oocyte maturation in vitro, little is known about its role in mediating maturation in vivo. In other animals, progesterone does not appear to be the primary physiologic mediator of oocyte maturation. For example, oocyte maturation in fish is mediated by the progesterone metabolite 17␣, 20␤-dihydroxyprogesterone (6). In mice, ovaries from females lacking the PR gene still contain well-developed follicles with mature oocytes (7), suggesting that progesterone and its receptor are not necessary for oocyte maturation and that other factors are therefore important. Finally, mifepristone (RU486), a potent inhibitor of both mammalian and Xenopus PR-mediated transcription, does not block progesterone-mediated maturation (5), implying that, even in vitro, signaling via the PR may not be the only mechanism behind progesterone-induced maturation.In an effort to clarify the physiologic importance of progesterone in Xenopus oocyte maturation, we measured the serum and ovarian steroid content of female frogs injected with ␤-human chronic growth hormone (␤-hCG). We show that progesterone is barely detectable in the serum and ovaries of these animals but that androgen concentrations are Ͼ10 times higher than that of progesterone. Further, we demonstrate that oocytes are equally or more sensitive to signaling by androstenedione (AD) and testosterone than progesterone. We identify classical Xenopus androgen receptors (ARs) in oocytes and show t...

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Section: Discussionsupporting

confidence: 77%

Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation

Lutz

Cole

Gupta

et al. 2001

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

156

142

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“…No significant difference could be detected (using non-parametric MannWhitney U test). (Mulner et al 1978, Fortune 1983, Gohin et al 2010. Moreover, Xenopus intra-oocyte E 2 concentrations are in the range of E 2 content previously measured in the whole follicles (Fortune 1983) and in plasma varying from 1 to 28 ng/ml corresponding to a maximum of 100 nM (Pickford & Morris 1999, Hecker et al 2004, Urbatzka et al 2007).…”

Section: Modulation Of Xenopus Oocyte Maturation By Ementioning

confidence: 64%

Aromatase expression in Xenopus oocytes: a three cell-type model for the ovarian estradiol synthesis

Gohin¹,

Bodinier²,

Fostier³

et al. 2011

Journal of Molecular Endocrinology

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In contrast to the classical model describing the synthesis of androgens and estrogens as restricted to somatic cells, a previous study demonstrated that Xenopus laevis oocytes participate in androgen synthesis. The objective of our study was to determine whether Xenopus oocytes are also involved in estrogen synthesis. More precisely, we analyzed aromatase expression by in situ hybridization and RT-QPCR and measured aromatase activity. Aromatase, the enzyme responsible for estrogen synthesis, appears to be expressed and active not only in the follicular cells but also in the vitellogenic oocytes. During late oogenesis, aromatase oocyte expression and activity decreased concomitantly with the trend observed in surrounding follicular layers. In order to investigate the role of estradiol-17b (E 2 ), we studied its effect on oocyte meiotic resumption. It appears that, as in Rana pipiens, E 2 inhibited the follicle-enclosed maturation of Xenopus oocytes, likely through inhibition of LH-induced maturation-inducing steroid synthesis. In addition, E 2 exerted a slight enhancing action on denuded oocyte maturation whose biological significance remains unclear. Together, our results demonstrate that Xenopus oocyte significantly participates in ovarian E 2 synthesis and this may be a common feature of vitellogenic vertebrates.

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“…Concerning the last growth phase it has previously been demonstrated that the large follicle undergoes a change of differentiation with regard to its ability to respond to hormones. MULNER et al (9) observed that vitellogenic follicles (4 < 800 pm) produced 10 to 50 times more estrogens than full grown follicles (4 > 1,200 pm); WALLACE and Ho (15) have reported that progesterone inhibited vitellogenin uptake by oocytes greater than 1,000 pm but had no effect on oocytes 800-900 pm in diameter. Clearly there exists a change of the physiological status of the follicle when it grows from i,OOO to 1,100 pm; it may be unambiguously related to a change of growth rate as seen in Fig.…”

Section: Discussionmentioning

confidence: 99%

Kinetic Analysis of Entire Oogenesis in Xenopus Laevis

1980

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In our breeding conditions (without artificial hormonal stimulation) two years after metamorphosis are necessary for a Xcnopus luevis female to produce mature oocytes. Four periods of different growth rates can be distinguished into this first wave of oogenesis: I ) oocytes reach 120 Itm in diameter (early stage I according to DUMONT ( 5 ) ) in a few weeks after metamorphosis; 2) growth slows down and the size of 250-300 prn (late stage I) is obtained 6-7 months later; 3) a rapid growth resumes during vitellogenesis (stages 11, I11 and IV) and a 1,000-1.100 prn diameter is reached in 2-3 months; 4) the last period spans for a year and the oocyte grows up to 1,200 prn. This phase covers many physiological changes and it should be critical to size carefully the oocytes for biochemical investigations and comparisons.At last most of the oocytes in a young female do not proceed through this entire oogenesis, they are stopped at the end of the second growth phase (about 250 /rrn in diameter).The Xenopus luevis oocyte is in several respects one of the best known cells in eukaryotic organisms. Its structural and biochemical differentiation have been the subject of important works concerning the accumulation of organelles or macromolecules ; moreover this material has provided invaluable information about the expression of the genetic material, its controls and the study of the hormone metabolism and the maturation (for a review see DAVIDSON (3)). During the differentiation of this giant cell (which occurs primarily at the diplotene stage), different steps have been distinguished and correlated with obvious morphological criteria such as: the size, the presence of yolk, the presence and repartition of pigment. Including cytochemical, ultrastructural and some physiological data, the important work of classification carried out by DUMONT ( 5 ) constitutes at the present time the best framework for analyzing the complex process of Xenopus oogenesis. The DUMONT'S stages are now currently used when it is necessary to describe a sequence of differentiation events in the Xenopus oocyte.As a paradox, very few information is available concerning the whole length of oogenesis in this organism and little is known about the duration of most of the various morphologically defined stages. The most complete estimations are reported by FORD (6) who suggests that the total time required for the oocyte to differentiate is about 1.5-2 years; (the time is always counted from the metamorphosis since it is well known that the first wave of oogenesis starts immediately after this event). On the other hand, VAN GANSEN and SCHRAM (13) have proposed a duration of 7 months for the period required to progress from the pachytene stage (15-20 pm cells) to a large diplotene oocyte (1,000 pm). Concerning the duration of the different oogenesis stages it appears that the data are fragmentary if not contradictory: as outlined by KEEM el al. (8) who recently analyzed the growth rates of Xenopus oocytes, the results for the duration of the vitellogenesis m...

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Steroid biosynthesis by ovarian follicles of Xenopus laevis in Vitro during oogenesis

Cited by 35 publications

References 19 publications

Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation

Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation

Aromatase expression in Xenopus oocytes: a three cell-type model for the ovarian estradiol synthesis

Kinetic Analysis of Entire Oogenesis in Xenopus Laevis

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