Inactivation of glucocorticoids by 11β-hydroxysteroid dehydrogenase enzymes increases during the meiotic maturation of porcine oocytes

Webb, Rachel J.; Sunak, N; Wren, Lisa; Michael, Anthony E.

doi:10.1530/rep-08-0289

Cited by 14 publications

(13 citation statements)

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“…In mammals, high levels of free glucocorticoids are present in the ovarian follicle antral fluid and glucocorticoid receptors (GRs) are present in ovarian tissues [5][6][7][8][9][10][11][12], suggesting an essential role for the glucocorticoid in oocyte development and maturation, possibly by modulating the meiotic competence of the oocyte [7]. Elevated ovarian glucocorticoids were found to have adverse affects on the maturation of oocytes and increased anovulation [13][14][15][16][17], but it is not clear whether these responses can be attributed to a direct action of the glucocorticoids on ovarian steroidogenesis.…”

Section: Introductionmentioning

confidence: 99%

Cortisol Inhibition of 17b-Estradiol Secretion by Rainbow Trout Ovarian Follicles Involves Modulation of Star and P450scc Gene Expression

Barkataki¹,

Aluru²

2013

J Aquac Res Development

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Maternal stress associated with elevated maternal cortisol levels has well-demonstrated adverse affects on reproduction in vertebrates, including impaired ovarian steroidogenesis. Currently, the potential sites of action of cortisol on ovarian function are not known. Studies were carried out to examine the mechanism(s) by which cortisol suppresses steroidogenesis by mid-vitellogenic stage rainbow trout (Oncorhynchus mykiss) ovarian follicles. 17b-Estradiol and testosterone synthesis, and the expression of key steroidogenesis-related genes (using real time RT-PCR) were measured. Follicles were also incubated in the presence of several tritium-labelled steroids, and the tritium-labeled steroid products were separated by reverse-phase HPLC to look for possible affects of cortisol on specific steroidogenic enzyme function. Cortisol inhibited 17b-estradiol and testosterone synthesis, but had no affect on the formation of tritium-labelled estrogens from any of the tritium-labeled substrates, suggesting that the suppressive action of the glucocorticoid did not operate by inhibiting estrogen synthesis from androgens. Conversely, in the presence of cortisol in the medium, the relative expression of genes encoding for steroidogenic acute regulatory (StAR) protein and P450 side chain cleavage (P450scc) enzyme was suppressed, suggesting that the cortisol inhibition of steroidogenesis is prior to the synthesis of progestogens, possibly inhibiting either the expression and/or turnover of the genes encoding for StAR and P450scc proteins. The study shows that maternal stress during the critical phase of follicle vitellogenesis will have deleterious effects on oocyte development and growth.

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Section: Introductionmentioning

confidence: 99%

Cortisol Inhibition of 17b-Estradiol Secretion by Rainbow Trout Ovarian Follicles Involves Modulation of Star and P450scc Gene Expression

Barkataki¹,

Aluru²

2013

J Aquac Res Development

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“…Consequently, if the oocytes and early embryos are unable to metabolize cortisol, embryogenesis may be compromised (Leatherland et al 2010. The antral fluid of the ovarian follicles in mammals contains relatively high concentrations of unconjugated cortisol, the levels of which are regulated within narrow limits by the actions of two forms of 11b-hydroxysteroid dehydrogenase (11b-HSD) that are co-expressed in the mural granulosa cells (Michael et al 2003, Sunak et al 2007, Michael & Papageorghiou 2008, Webb et al 2008. The maintenance of a stable high concentration of cortisol suggests that the glucocorticoid plays an important role in the 'normal' development and maturation of the oocyte.…”

Section: Introductionmentioning

confidence: 99%

The in vitro metabolism of cortisol by ovarian follicles of rainbow trout (Oncorhynchus mykiss): comparison with ovulated oocytes and pre-hatch embryos

Li¹,

Christie²,

Leatherland³

2012

Reproduction

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REPRODUCTION RESEARCHThe in vitro metabolism of cortisol by ovarian follicles of rainbow trout (Oncorhynchus mykiss): comparison with ovulated oocytes and pre-hatch embryos Mao Li, Heather L Christie and John F Leatherland Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada N1G 2W1Correspondence should be addressed to M Li who is now at Department of Integrated Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1; Email: mao@uoguelph.ca AbstractMid-vitellogenic stage rainbow trout (Oncorhynchus mykiss) ovarian follicles (both intact and yolk free (YF)), ovulated oocytes and embryos were co-incubated with [2,4,6,7-3 H]cortisol for 18 h to determine the degree and nature of the metabolism and biotransformation of the glucocorticoid. There was evidence of the conversion of cortisol to the less biologically potent glucocorticoid, cortisone, and the formation of glucocorticoid sulphates (both cortisol and cortisone) for all cell and tissue samples, suggesting the presence of 11b-hydroxysteroid dehydrogenase (11b-HSD) and glucocorticoid sulphotransferase (GST) activity at all stages; however, GST activity was particularly marked in both intact and YF ovarian follicles, suggesting an important role of follicles in limiting the exposure of oocyte to maternal cortisol. As there was no evidence of 11b-HSD or GST activity in ovarian fluid, the findings affirm that ovarian follicles (probably the thecal and granulosa cells) provide a barrier against the transfer of cortisol to the oocytes by forming sulphated steroids, whereas ovulated oocytes and early embryos have a more limited capacity to either metabolize or conjugate cortisol and are therefore more vulnerable at the post-ovulatory and early embryonic stages to increases in exposure to the glucocorticoid. (2012)). The relationship between the maternal stress response, maternal hypercortisolism and reproductive and embryonic outcomes is complex and still the object of ongoing research; however, some of the outcomes are most likely caused by metabolic or immune system-related actions of cortisol that indirectly impact the maternal involvement in the reproductive process; however, other responses can be attributed to the direct actions of cortisol on the developing embryo or fetus. In mammals, the antral fluid of the ovarian follicle regulates the exposure of the pre-ovulatory oocyte to cortisol, and the placental tissues act as a partial barrier to the transfer of maternal cortisol to the embryo and fetus. Because these protective barriers are not present in oviparous vertebrate species, there is the potential for the transfer of maternal cortisol to the oocytes. Consequently, if the oocytes and early embryos are unable to metabolize cortisol, embryogenesis may be compromised (Leatherland et al. 2010. The antral fluid of the ovarian follicles in mammals contains relatively high concentrations of unconjugated cortisol, the levels of which are regulated within narrow limits by the actions of two forms of 1...

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“…Recently, it has been demonstrated that primarily the HSD11B enzyme system acts within porcine oocytes, converting cortisol to cortisone, and this enzymatic inactivation increases during oocyte maturation [48]. This HSD11B activity may also have limited the potentially harmful effect of physiological levels of cortisol in the oocyte in the present work.…”

Section: Discussionmentioning

confidence: 69%

Effect of blood plasma collected after adrenocorticotropic hormone administration during the preovulatory period in the sow on oocyte in vitro maturation

González

2013

Theriogenology

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Reproduction may be affected by stressful events changing the female endocrine or metabolic profile. An altered environment during oocyte development could influence the delicate process of oocyte maturation. Here, the effect of simulated stress by media supplementation with blood plasma from sows after adrenocorticotropic hormone (ACTH) administration during the preovulatory period was assessed. Oocytes were matured for 46 h in the presence of plasma from ACTH-treated sows, or plasma from NaCl-treated control sows, or medium without plasma (BSA group). The plasma used had been collected at 36 h and 12 h (± 2 h) before ovulation (for the first 24 h + last 22 h of maturation, respectively).Subsequent fertilisation and embryo development were evaluated. Actin cytoskeleton and mitochondrial patterns were studied by confocal microscopy both in the oocytes and the resulting blastocysts. Nuclear maturation did not differ between treatments. Subtle differences were observed in the actin microfilaments in oocytes; however, mitochondrial patterns were associated with the treatment (P<0.001). These differences in mitochondrial patterns were not reflected by in vitro outcomes, which were similar in all groups. In conclusion, an altered hormonal environment provided by a brief exposure to plasma from ACTH-treated sows during in vitro oocyte maturation, could induce alterations in actin cytoskeleton and mitochondrial patterns in oocytes. However, these changes might not hamper the subsequent in vitro embryo development.[217 words]

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Inactivation of glucocorticoids by 11β-hydroxysteroid dehydrogenase enzymes increases during the meiotic maturation of porcine oocytes

Cited by 14 publications

References 64 publications

Cortisol Inhibition of 17b-Estradiol Secretion by Rainbow Trout Ovarian Follicles Involves Modulation of Star and P450scc Gene Expression

Cortisol Inhibition of 17b-Estradiol Secretion by Rainbow Trout Ovarian Follicles Involves Modulation of Star and P450scc Gene Expression

The in vitro metabolism of cortisol by ovarian follicles of rainbow trout (Oncorhynchus mykiss): comparison with ovulated oocytes and pre-hatch embryos

Effect of blood plasma collected after adrenocorticotropic hormone administration during the preovulatory period in the sow on oocyte in vitro maturation

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