Elsevier

Neuroscience

Volume 140, Issue 4, 2006, Pages 1381-1394
Neuroscience

Systems neuroscience
Plasticity in the expression of the steroid receptor coactivator 1 in the Japanese quail brain: Effect of sex, testosterone, stress and time of the day

https://doi.org/10.1016/j.neuroscience.2006.03.002Get rights and content

Abstract

Analysis of nuclear receptor action on the eukaryotic genome highlights the importance of coactivators on gene transcription. The steroid receptor coactivator-1 in particular is the focus of an intense research and physiological or behavioral studies have confirmed that it plays a major role in the modulation of steroid and thyroid receptors activity. However, little is known about the regulation of steroid receptor coactivator-1 expression the brain. The goal of this study was to determine the potential factors modulating steroid receptor coactivator-1 synthesis in Japanese quail by quantification of its mRNA with real time quantitative polymerase chain reaction and of the corresponding protein via Western blotting. Contrary to previously published results from our laboratory [Charlier TD, Lakaye B, Ball GF, Balthazart J (2002) The steroid receptor coactivator SRC-1 exhibits high expression in steroid-sensitive brain areas regulating reproductive behaviors in the quail brain. Neuroendocrinology 76:297–315], we found here that sexually mature females had a higher concentration of steroid receptor coactivator-1 in the preoptic area/hypothalamus compared with males. Steroid receptor coactivator-1 expression in the male preoptic area/hypothalamus was up-regulated by testosterone and tended to be decreased by stress. We also identified a significant correlation between the time of the day and the expression of the coactivator in the optic lobes, hippocampus, telencephalon and hindbrain but the pattern of changes in expression as a function of the time of the day varied from one brain area to another. Together, these data support the idea that steroid receptor coactivator-1 is not constitutively expressed but rather is finely regulated by steroids, stress and possibly other unidentified factors.

Section snippets

Animals and in vivo procedures

Four separate experiments (see below for specific protocols) were carried out on Japanese quail (Coturnix japonica) that were bought from a local breeder (Degros-Louppe Farm, Rechrival, Belgium) at the age of about 3 weeks. Throughout their life at the breeding colony and in the laboratory, birds were exposed to a photoperiod simulating long days (16 h light and 8 h dark per day) and had food and water available ad libitum. All experimental procedures were in agreement with the Belgian laws on

Experiment 1

We previously reported that SRC-1 is expressed at a higher level in the HPOA of M compared with F (Charlier et al., 2002). To determine the influence of adult steroid levels on the expression of the coactivator and on the sex difference affecting this expression, SRC-1 mRNA levels were quantified in quail of both sexes that were either gonadally intact (MI and FI), or MCX and FCX or MCX+T and FCX+T. Behavioral tests confirmed previously described sex differences in copulatory behavior (Adkins

Discussion

We demonstrated in the present studies that SRC-1 expression in several brain regions is not constitutive but, rather, is regulated by several endogenous and exogenous factors, including the sex of the subjects, testosterone and potentially the time of the day.

Conclusion

Together these data indicate that steroid hormones alter SRC-1 expression in a sex- and site-specific manner. SRC-1, and the SRC family in general, are shared by different receptor systems, suggesting that the regulation of the cofactor expression by one system may be important for the ability of other receptor systems to function at that time or later in life. For example, the regulation of SRC-1 by thyroid hormones or glucocorticoids during development may have important implications on sex

Acknowledgments

We would like to thank Drs. Ernst Heinen and Benaïssa El Moualij for the use of the ABI prism 5700 qPCR apparatus and for technical advice regarding qPCR techniques. This research was supported by grants from the National Institutes of Health (MH50388) to G.F.B. and J.B. and from the Belgian FRFC (2.4562.05) to J.B. T.D.C. was an FRIA grant recipient.

References (66)

  • I. Kurihara et al.

    Expression and regulation of nuclear receptor coactivators in glucocorticoid action

    Mol Cell Endocrinol

    (2002)
  • H. Ma et al.

    Hormone-dependant, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter

    Curr Biol

    (2001)
  • M.E. Meyer et al.

    Steroid hormone receptors compete for factors that mediate their enhancer function

    Cell

    (1989)
  • R.Y. Moore et al.

    Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat

    Brain Res

    (1972)
  • M.A. Ottinger

    Hormonal control of reproductive behavior in the avian male

    Poult Sci

    (1983)
  • M.A. Ottinger et al.

    Testosterone and sex-related behavior and morphologyrelationship during maturation and in the adult Japanese quail

    Horm Behav

    (1978)
  • M. Schumacher et al.

    The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail

    Physiol Behav

    (1983)
  • M. Schumacher et al.

    The postnatal demasculinization of sexual behavior in the Japanese quail

    Horm Behav

    (1984)
  • L.P. Shearman et al.

    Expression of basic helix-loop-helix/PAS genes in the mouse suprachiasmatic nucleus

    Neuroscience

    (1999)
  • M.J. Tetel et al.

    Photoperiodic regulation of androgen receptor and steroid receptor coactivator-1 in Siberian hamster brain

    Mol Brain Res

    (2004)
  • M.L. Acevedo et al.

    Mediator and p300/CBP steroid receptor coactivator complexes have distinct roles, but function synergistically, during estrogen receptor α-dependent transcription with chromatine templates

    Mol Cell Biol

    (2003)
  • E.K. Adkins et al.

    Hormonal control of behavior in the Japanese quail

    J Comp Physiol Psychol

    (1972)
  • E.K. Adkins et al.

    Control of reproductive behavior by sex steroids in male quail

    J Comp Physiol Psychol

    (1978)
  • D. Auboeuf et al.

    Differential recruitment of nuclear receptor coactivators may determine alternative RNA splice site choice in target genes

    Proc Natl Acad Sci U S A

    (2004)
  • A.P. Auger et al.

    Steroid receptor coactivator-1 (SRC-1) mediates the development of sex-specific brain morphology and behavior

    Proc Natl Acad Sci U S A

    (2000)
  • A.P. Auger et al.

    Differential expression of nuclear receptor co-activator in neonatal male and female rat brain

    Soc Neurosci Abstr

    (2001)
  • S. Azadi et al.

    Thyroid-β2 and the retinoid RAR-α, RXR-γ and ROR-β2 receptor mRNAs; expression profiles in the mouse retina, retinal explants and neocortex

    Neuroreport

    (2002)
  • J.C.G. Blanco et al.

    The histone acetylase PCAF is a nuclear receptor coactivator

    Genes Dev

    (1998)
  • J. Boissin et al.

    Circadian rhythm in adrenal cortical activity in the quail

    J Interdiscipl Cycle Res

    (1970)
  • H.M. Chan et al.

    p300/CBP proteinsHATs for transcriptional bridges and scaffolds

    J Cell Sci

    (2001)
  • T.D. Charlier et al.

    Inhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sexual behavior and associated brain plasticity

    J Neurosci

    (2005)
  • T.D. Charlier et al.

    The steroid receptor coactivator SRC-1 exhibits high expression in steroid-sensitive brain areas regulating reproductive behaviors in the quail brain

    Neuroendocrinology

    (2002)
  • P. Clair et al.

    Daily variations of plasma sex hormone-binding globulin capacity, testosterone and luteinizing hormone concentrations in healthy rested adult males

    Horm Res

    (1985)
  • Cited by (33)

    • Sex Differences in the Neurobiology of Stress

      2023, Psychiatric Clinics of North America
    • Dose-dependent regulation of steroid receptor coactivator-1 and steroid receptors by testosterone propionate in the hippocampus of adult male mice

      2016, Journal of Steroid Biochemistry and Molecular Biology
      Citation Excerpt :

      Tetel et al. reported that in the bed nucleus of the stria terminalis and medial amygdale of Siberian hamster brain, expression of SRC-1 was decreased by short days [39]. Charlier et al. reported that in the hypothalamus of male Japanese quail, expression of SRC-1 was upregulated by testosterone [40]. In our previous studies, we showed that hippocampal SRC-1 was regulated by postnatal development and aging [28,29,33], indicating that developmental- and aging-related alterations of circulating and/or hippocampal sex hormones may be closely related to the changes in SRC-1.

    • Steroid receptor coactivator-1 mediates letrozole induced downregulation of postsynaptic protein PSD-95 in the hippocampus of adult female rats

      2015, Journal of Steroid Biochemistry and Molecular Biology
      Citation Excerpt :

      It is widely distributed in the brain [10,26,27,30,45] and has been shown to be involved in the regulation of sexual behavior through binding with steroid hormone receptors [46,47]. Intraventricular injection of SRC-1 antisense oligonucleotides can significantly reduce the typical male sexual behaviors [47–50]. SRC-1 knockout induced moderate motor dysfunction and delayed Purkinje cells development [45].

    View all citing articles on Scopus
    1

    Present address: University of British Columbia, Department of Psychology, 2136 West Mall, Vancouver, BC, Canada V6T 1Z4.

    View full text