Estradiol‐17β interference with meiotic maturation in Rana pipiens ovarian follicles: Evidence for inhibition of 3β‐hydroxysteroid dehydrogenase

Abstract

Increasing doses of estradiol-17 beta added to in vitro incubations inhibited pregnenolone-induced germinal vesicle breakdown in Rana pipiens ovarian follicles. The inhibition was reversed with increasing concentrations or pregnenolone added to the medium. Because no evidence of estradiol-17 beta inhibition or interaction with progesterone-induced GVBD was observed, the effect of estradiol-17 beta on the conversion of 3H-pregnenolone to 3H-progesterone was investigated. Estradiol-17 beta in doses as low as 10(-7) M significantly inhibited the conversion of 3H-pregnenolone to 3H-progesterone in follicles incubated in vitro. It is suggested that estradiol-17 beta is a feedback inhibitor of 3 beta-hydroxysteroid dehydrogenase-isomerase, the enzyme complex that converts pregnenolone to progesterone, a necessary step in the initiation of GVBD.

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

“…The physiological function of oocyte E 2 remains unclear, particularly during oocyte maturation. As reported in Rana pipiens (Schuetz 1972, Spiegel et al 1978, Lin & Schuetz 1983, E 2 appeared to inhibit Xenopus follicle-enclosed oocyte maturation likely through an inhibition of gonadotropin/cAMP-induced progestin synthesis by follicular layers (Lin et al 1988). However, a direct inhibitory effect of E 2 on the oocyte could not be ruled out, as demonstrated in previous studies in Xenopus (Baulieu et al 1978) and in Rana pipiens (Lin & Schuetz 1983).…”

“…More recently, E 2 was also shown to enhance progesterone-induced ovulation, possibly through a stimulatory effect on gonadotropin synthesis (Ogawa et al 2011). In addition to E 2 endocrine effects, E 2 may have autocrine and/or paracrine effects, as E 2 inhibits follicle-enclosed oocyte maturation through inhibition of maturation-inducing steroid (MIS) synthesizing enzymes in vitellogenic species such as Rana pipiens (Schuetz 1972, Spiegel et al 1978, Lin & Schuetz 1983 or Oncorhynchus mykiss ( Jalabert et al 1984). This steroid may also activate transcription of particular genes within the oocyte that would play a role in oocyte development, such as IGFBP3, the expression of which has been shown to be positively regulated by E 2 in trout oocytes (Kamangar et al 2006).…”

Expression of Messenger Ribonucleic Acid (mRNA) Encoding 3β-Hydroxysteroid Dehydrogenase Δ 4,Δ 5 Isomerase (3β-HSD) during Recruitment and Selection of Bovine Ovarian Follicles: Identification of Dominant Follicles by Expression of 3β-HSD mRNA within the Granulosa Cell Layer1

“…Studies in rats and humans have shown that LH or hCG is the major stimulator of 3-HSD mRNA expression in granulosa cells [24,25]. FSH [32] and estradiol [33] increased 3-HSD activity, whereas progesterone decreased 3P-HSD activity in humans [34]. These studies imply that expression of 3P-HSD mRNA or enzyme activity may be regulated by both LH and FSH as well as by steroid hormones.…”

Effects of endocrine-disrupting contaminants on amphibian oogenesis: methoxychlor inhibits progesterone-induced maturation of Xenopus laevis oocytes in vitro.

“…For example, gonadotropin-induced GVBD in follide cell-encdosed oocytes from Rana pipiens is strongly antagonized by estrogen without pretreatment (30,45). The mechanism of this antagonism appears to be feedback inhibition of follicle cell 33-hydroxysteroid dehydrogenase activity (46), which is involved in generating the paracrine progesterone signal that stimulates GVBD in response to gonadotropin (47 A variety of EDCs were also tested in this assay to assess their effect on progesteroneinduced oocyte maturation. Octylphenol, o,p'-DDT, di-n-butyl phthalate, and bisphenol A are environmentally persistent chemicals that exhibit innate estrogenic activity (7,(48)(49)(50).…”