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Adrenocorticotropic hormone suppresses gonadotropin-stimulated estradiol release from zebrafish ovarian follicles.

Alsop D, Ings JS, Vijayan MM - PLoS ONE (2009)

Bottom Line: ACTH neither affected cortisol nor unstimulated E(2) release from ovarian follicles.This effect of ACTH on E(2) release was not observed in the presence of either 8-bromo-cAMP or forskolin, suggesting that the mechanism(s) involved in steroid attenuation was upstream of adenylyl cyclase activation.Overall, our results suggest that a stress-induced rise in plasma ACTH levels may initiate a rapid down-regulation of acute stimulated E(2) biosynthesis in the zebrafish ovary, underscoring a novel physiological role for this pituitary peptide in modulating reproductive activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Waterloo, Waterloo, Ontario, Canada.

ABSTRACT
While stress is known to impact reproductive performance, the pathways involved are not entirely understood. Corticosteroid effects on the functioning of the hypothalamus-pituitary-gonadal axis are thought to be a key aspect of stress-mediated reproductive dysfunction. A vital component of the stress response is the pituitary secretion of adrenocorticotropic hormone (ACTH), which binds to the melanocortin 2 receptor (MC2R) in the adrenal glands and activates cortisol biosynthesis. We recently reported MC2R mRNA abundance in fish gonads leading to the hypothesis that ACTH may be directly involved in gonadal steroid modulation. Using zebrafish (Danio rerio) ovarian follicles, we tested the hypothesis that acute ACTH stimulation modulates cortisol and estradiol (E(2)) secretion. ACTH neither affected cortisol nor unstimulated E(2) release from ovarian follicles. However, ACTH suppressed human chorionic gonadotropin (hCG)-stimulated E(2) secretion in a dose-related manner, with a maximum decrease of 62% observed at 1 I.U. ACTH mL(-1). This effect of ACTH on E(2) release was not observed in the presence of either 8-bromo-cAMP or forskolin, suggesting that the mechanism(s) involved in steroid attenuation was upstream of adenylyl cyclase activation. Overall, our results suggest that a stress-induced rise in plasma ACTH levels may initiate a rapid down-regulation of acute stimulated E(2) biosynthesis in the zebrafish ovary, underscoring a novel physiological role for this pituitary peptide in modulating reproductive activity.

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Temporal (3 or 8 h incubations) cortisol production by zebrafish ovarian follicles.Cortisol (grey bars) is not detected in the culture media of control or ACTH treated follicles, but is detected in the human chorionic gonadotropin (hCG, 10 I.U./mL) and hCG plus adrenocorticotropic hormone (ACTH, 1.5 I.U./mL; hatched bars) treatments. Control (open bar) and hCG-stimulated (black bar) estradiol (E2) media concentrations after 3 h are provided as a reference. Values represent mean ± SEM (N = 3; each N is a pool of follicles from three fish). Treatments with different letters are significantly different, as determined by one-way ANOVA at each time point followed by Student-Newman-Keuls test for multiple comparisons (P<0.05). An asterisk (*) with the E2 measurements indicates a significant difference determined by a Student's t test (P<0.05).
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pone-0006463-g002: Temporal (3 or 8 h incubations) cortisol production by zebrafish ovarian follicles.Cortisol (grey bars) is not detected in the culture media of control or ACTH treated follicles, but is detected in the human chorionic gonadotropin (hCG, 10 I.U./mL) and hCG plus adrenocorticotropic hormone (ACTH, 1.5 I.U./mL; hatched bars) treatments. Control (open bar) and hCG-stimulated (black bar) estradiol (E2) media concentrations after 3 h are provided as a reference. Values represent mean ± SEM (N = 3; each N is a pool of follicles from three fish). Treatments with different letters are significantly different, as determined by one-way ANOVA at each time point followed by Student-Newman-Keuls test for multiple comparisons (P<0.05). An asterisk (*) with the E2 measurements indicates a significant difference determined by a Student's t test (P<0.05).

Mentions: Cortisol was not detected in media from control and ACTH-treated ovarian follicles after 3 h or 8 h of incubation (Fig. 2). Cortisol was detected in follicles treated with human chorionic gonadotropin (hCG), although the levels were only significantly different from the control at 3 h of incubation (Fig. 2).


Adrenocorticotropic hormone suppresses gonadotropin-stimulated estradiol release from zebrafish ovarian follicles.

Alsop D, Ings JS, Vijayan MM - PLoS ONE (2009)

Temporal (3 or 8 h incubations) cortisol production by zebrafish ovarian follicles.Cortisol (grey bars) is not detected in the culture media of control or ACTH treated follicles, but is detected in the human chorionic gonadotropin (hCG, 10 I.U./mL) and hCG plus adrenocorticotropic hormone (ACTH, 1.5 I.U./mL; hatched bars) treatments. Control (open bar) and hCG-stimulated (black bar) estradiol (E2) media concentrations after 3 h are provided as a reference. Values represent mean ± SEM (N = 3; each N is a pool of follicles from three fish). Treatments with different letters are significantly different, as determined by one-way ANOVA at each time point followed by Student-Newman-Keuls test for multiple comparisons (P<0.05). An asterisk (*) with the E2 measurements indicates a significant difference determined by a Student's t test (P<0.05).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2714464&req=5

pone-0006463-g002: Temporal (3 or 8 h incubations) cortisol production by zebrafish ovarian follicles.Cortisol (grey bars) is not detected in the culture media of control or ACTH treated follicles, but is detected in the human chorionic gonadotropin (hCG, 10 I.U./mL) and hCG plus adrenocorticotropic hormone (ACTH, 1.5 I.U./mL; hatched bars) treatments. Control (open bar) and hCG-stimulated (black bar) estradiol (E2) media concentrations after 3 h are provided as a reference. Values represent mean ± SEM (N = 3; each N is a pool of follicles from three fish). Treatments with different letters are significantly different, as determined by one-way ANOVA at each time point followed by Student-Newman-Keuls test for multiple comparisons (P<0.05). An asterisk (*) with the E2 measurements indicates a significant difference determined by a Student's t test (P<0.05).
Mentions: Cortisol was not detected in media from control and ACTH-treated ovarian follicles after 3 h or 8 h of incubation (Fig. 2). Cortisol was detected in follicles treated with human chorionic gonadotropin (hCG), although the levels were only significantly different from the control at 3 h of incubation (Fig. 2).

Bottom Line: ACTH neither affected cortisol nor unstimulated E(2) release from ovarian follicles.This effect of ACTH on E(2) release was not observed in the presence of either 8-bromo-cAMP or forskolin, suggesting that the mechanism(s) involved in steroid attenuation was upstream of adenylyl cyclase activation.Overall, our results suggest that a stress-induced rise in plasma ACTH levels may initiate a rapid down-regulation of acute stimulated E(2) biosynthesis in the zebrafish ovary, underscoring a novel physiological role for this pituitary peptide in modulating reproductive activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Waterloo, Waterloo, Ontario, Canada.

ABSTRACT
While stress is known to impact reproductive performance, the pathways involved are not entirely understood. Corticosteroid effects on the functioning of the hypothalamus-pituitary-gonadal axis are thought to be a key aspect of stress-mediated reproductive dysfunction. A vital component of the stress response is the pituitary secretion of adrenocorticotropic hormone (ACTH), which binds to the melanocortin 2 receptor (MC2R) in the adrenal glands and activates cortisol biosynthesis. We recently reported MC2R mRNA abundance in fish gonads leading to the hypothesis that ACTH may be directly involved in gonadal steroid modulation. Using zebrafish (Danio rerio) ovarian follicles, we tested the hypothesis that acute ACTH stimulation modulates cortisol and estradiol (E(2)) secretion. ACTH neither affected cortisol nor unstimulated E(2) release from ovarian follicles. However, ACTH suppressed human chorionic gonadotropin (hCG)-stimulated E(2) secretion in a dose-related manner, with a maximum decrease of 62% observed at 1 I.U. ACTH mL(-1). This effect of ACTH on E(2) release was not observed in the presence of either 8-bromo-cAMP or forskolin, suggesting that the mechanism(s) involved in steroid attenuation was upstream of adenylyl cyclase activation. Overall, our results suggest that a stress-induced rise in plasma ACTH levels may initiate a rapid down-regulation of acute stimulated E(2) biosynthesis in the zebrafish ovary, underscoring a novel physiological role for this pituitary peptide in modulating reproductive activity.

Show MeSH
Related in: MedlinePlus