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. 2019 Feb;31(2):e12681.
doi: 10.1111/jne.12681. Epub 2019 Feb 1.

Steroid profiles in quail brain and serum: Sex and regional differences and effects of castration with steroid replacement

Philippe Liere  1 , Charlotte A Cornil  2 , Marie Pierre de Bournonville  2 , Antoine Pianos  1 , Matthieu Keller  3 , Michael Schumacher  1 , Jacques Balthazart  2
Affiliations

Steroid profiles in quail brain and serum: Sex and regional differences and effects of castration with steroid replacement

Philippe Liere et al. J Neuroendocrinol. 2019 Feb.

Abstract

Both systemic and local production contribute to the concentration of steroids measured in the brain. This idea was originally based on rodent studies and was later extended to other species, including humans and birds. In quail, a widely used model in behavioural neuroendocrinology, it was demonstrated that all enzymes needed to produce sex steroids from cholesterol are expressed and active in the brain, although the actual concentrations of steroids produced were never investigated. We carried out a steroid profiling in multiple brain regions and serum of sexually mature male and female quail by gas chromatography coupled with mass spectrometry. The concentrations of some steroids (eg, corticosterone, progesterone and testosterone) were in equilibrium between the brain and periphery, whereas other steroids (eg, pregnenolone (PREG), 5α/β-dihydroprogesterone and oestrogens) were more concentrated in the brain. In the brain regions investigated, PREG sulphate, progesterone and oestrogen concentrations were higher in the hypothalamus-preoptic area. Progesterone and its metabolites were more concentrated in the female than the male brain, whereas testosterone, its metabolites and dehydroepiandrosterone were more concentrated in males, suggesting that sex steroids present in quail brain mainly depend on their specific steroidogenic pathways in the ovaries and testes. However, the results of castration experiments suggested that sex steroids could also be produced in the brain independently of the peripheral source. Treatment with testosterone or oestradiol restored the concentrations of most androgens or oestrogens, respectively, although penetration of oestradiol in the brain appeared to be more limited. These studies illustrate the complex interaction between local brain synthesis and the supply from the periphery for the steroids present in the brain that are either directly active or represent the substrate of centrally located enzymes.

Keywords: brain aromatisation; brain steroid concentrations; gas chromatography; mass spectrometry; preoptic area.

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Figures

Figure 1.
Figure 1.
Concentrations of pregnenolone and its metabolites pregnenolone sulfate and 20α-dihydropregnenolone measured by GC/MS in the serum, hypothalamus-preoptic area (POA), whole telencephalon (TEL), cerebellum (CB) and optic lobes (OL) of adult sexually mature male and female Japanese quail. Data for brain areas were analyzed by a two-way ANOVA for each steroid with the brain area and sex as independent factors. Overall effects of sex are indicated under the name of the steroid considered (M>F or F>M). Results of Bonferroni post-hoc tests performed when a significant effect of brain areas was detected without interaction with sex are reported by a letter above the corresponding pairs of bars corresponding to the area of interest in both males and females (a=p<0.05 compared to the POA). Results of Tukey’s post-hoc tests performed when there was a significant interaction between sex and brain areas are reported by numbers above the bar associated with the sex and nucleus considered as follows: 1= p<0.05 compared to POA in the same sex, 2= p<0.05 compared to TEL in the same sex and 3= p<0.05 compared to CB in the same sex. Asterisks indicate sex differences within an area as detected by Tukey’s post hoc tests following a significant interaction between sex and area in the brain or by t-tests for the serum. ND above a bar indicates that the steroid was not detectable in any sample of the tissue and sex considered. These samples were for statistical and graphing purposes assigned a concentration equal to the threshold of detection.
Figure 2.
Figure 2.
Concentrations of progesterone (PROG) and its reduced metabolites and corticosterone measured by GC/MS in the serum, hypothalamus-preoptic area (POA), whole telencephalon (TEL), optic lobes (OL) and cerebellum (CB) of adult sexually mature male and female Japanese quail. See also figure 1 for the detail of statistical analyses.
Figure 3.
Figure 3.
Concentrations of DHEA, androstenediol, T and its metabolites measured by GC/MS in the serum, hypothalamus-preoptic area (POA), whole telencephalon (TEL), optic lobes (OL) and cerebellum (CB) of adult sexually mature male and female Japanese quail. See also figure 1 for the detail of statistical analyses.
Figure 4.
Figure 4.
Concentrations of the estrogens measured by GC/MS in the serum, hypothalamus-preoptic area (POA), and whole telencephalon (TEL of adult sexually mature male and female Japanese quail. See also figure 1 for the detail of statistical analyses.
Figure 5.
Figure 5.
Comparison of the steroid concentrations measured in dialysate collected in vivo from the male preoptic area (A) with the tissue concentrations in the same general brain region (POA) of males (B).
Figure 6.
Figure 6.
Concentrations of pregnenolone, T, E2 and androstenedione in the hypothalamus-preoptic area (POA), telencephalon (TEL) and serum of castrated male Japanese quail or castrated male quail treated with Silastic implants filled with T (T40) or with two doses of E2 (E40 and E80). Data for each steroid were analyzed by a two-way ANOVA with the two brain area considered (2 levels) and treatment of the subjects (4 levels) as independent factors or by a one-way ANOVA for the serum concentrations (4 levels). Results of Bonferroni post-hoc tests performed when a significant effect of brain areas was detected without interaction with treatment (PREG, E2) are reported by an underlined asterisk above the corresponding bars or by an asterisk above the bar if there was an interaction between treatment and brain area (T, androstenedione). Results of Tukey’s post-hoc tests performed when there was a significant overall effect of treatment are reported by numbers above the bar associated with the area and treatment considered as follows: 1= p<0.05 compared to CX same area, 2= p<0.05 compared to CX+T same area, 3= p<0.05 compared to CX+E40 same area and *= p<0.05 compared to POA same treatment.
Figure 7.
Figure 7.
Concentrations of 5 steroids detected in the telencephalon (TEL) and serum (first three lines) and of 7 steroids detected in the TEL only (last three lines) in castrated males or castrated Japanese quail treated with Silastic implants filled with T (T40) or with two doses of E2 (E40 and E80). Data for each steroid were analyzed by a one-way ANOVA for each type of samples (TEL or Serum). Results of Tukey post-hoc tests performed when a significant effect of treatment was detected are reported by numbers above the bar associated with the treatment (and tissue) considered as follows: 1= p<0.05 compared to CX, 2= p<0.05 compared to CX+T40 and 3= p<0.05 compared to CX+E40.
Figure 8.
Figure 8.
Metabolic pathways describing the putative synthesis pathways of steroids that could be reliably identified in the quail brain and serum.
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