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See detailCoordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria)
Sartor, Jennifer J.; Balthazart, Jacques ULg; Ball, Gregory F.

in Hormones & Behavior (2005), 47(4), 467-476

Temperate zone songbirds that breed seasonally exhibit pronounced differences in reproductive behaviors including song inside and outside the breeding season. Springlike long daylengths are associated ... [more ▼]

Temperate zone songbirds that breed seasonally exhibit pronounced differences in reproductive behaviors including song inside and outside the breeding season. Springlike long daylengths are associated with increases in plasma testosterone (T) concentrations, as well as with increases in singing and in the volume of several brain nuclei known to control this behavior. The mechanisms whereby T can induce changes in behavior and brain, and whether or not these effects are differentially regulated, have recently begun to be examined, as has the question of the relative contributions of T and its androgenic and estrogenic metabolites to the regulation of this seasonal behavioral and neural plasticity. In this experiment, we examined the effects of T, 5 alpha-dihydrotestosterone, or 17 beta-estradiol treatment on castrated male canaries housed on short days and compared neural and behavioral effects in these males to similarly-housed males given only blank implants. We observed that only T treatment was effective in eliciting significant increases in singing behavior after 11 days of hormone exposure. In addition, T alone was effective in increasing the volume of a key song production nucleus, HVC. However, at this time, none of the steroids had any effects on the volumes of two other song control nuclei, Area X of the medial striatum and the robust nucleus of the arcopallium (RA), that are efferent targets of HVC, known to be regulated by androgen in canaries and also to play a role in the control of adult song. T can thus enhance singing well before concomitant androgen-induced changes in the song control system are complete. (c) 2004 Elsevier Inc. All rights reserved. [less ▲]

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See detailInhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sex behavior and associated brain plasticity.
Charlier, Thierry ULg; Ball, Gregory F; Balthazart, Jacques ULg

in Journal of Neuroscience (2005), 25(4), 906-13

Studies of eukaryotic gene expression demonstrate the importance of nuclear steroid receptor coactivators in mediating efficient gene transcription. However, little is known about the physiological role ... [more ▼]

Studies of eukaryotic gene expression demonstrate the importance of nuclear steroid receptor coactivators in mediating efficient gene transcription. However, little is known about the physiological role of these coactivators in vivo. In Japanese quail, the steroid receptor coactivator-1 (SRC-1) is broadly expressed in steroid-sensitive brain areas that control the expression of male copulatory behavior, and we investigated the role of this coactivator by antisense technology. Daily intracerebroventricular injections of locked nucleic acid (LNA) antisense (AS) oligonucleotides targeting SRC-1 significantly reduced the expression of androgen- and estrogen-dependent male-typical sexual behaviors compared with control animals that received the vehicle alone or scrambled oligonucleotides. Sexual behavior was restored and even enhanced within 48 h after interruption of LNA injections. Western blot analysis confirmed the decrease of SRC-1 expression in AS animals and suggested an overexpression 48 h after the end of injections. The effects of SRC-1 knock-down on behavior correlated with a reduction in volume of the preoptic medial nucleus (POM) when its borders were defined by Nissl staining or by aromatase immunohistochemistry. The amount of aromatase-immunoreactive material in POM was also reduced in the AS compared with the control group. Previous work on SRC-1 knock-out mice raised questions about the importance of this specific coactivator in the regulation of reproductive behavior and development of sexually dimorphic structures in the CNS. Together, the present findings indicate that SRC-1 modulates steroid-dependent gene transcription and behavior and highlight the rapid time course of steroid-induced brain plasticity in adult quail. [less ▲]

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See detailDaily changes in the expression of the steroid receptor coactivator SRC-1.
Charlier, Thierry ULg; Ball, Gregory F.; Balthazart, Jacques ULg

in Hormones & Behavior (2005), 48

Steroid receptor coactivators such as SRC-1 significantly modulate the expression of steroid-dependent physiological and behavioral characteristics in birds and mammals. Changes in coactivator protein ... [more ▼]

Steroid receptor coactivators such as SRC-1 significantly modulate the expression of steroid-dependent physiological and behavioral characteristics in birds and mammals. Changes in coactivator protein expression are therefore likely to affect receptor-mediated transcriptional activity. We previously reported a tissue-dependent regulation of SRC-1 mRNA and protein levels by sex, stress and testosterone in the quail brain. In addition, SRC-1 expression has been shown to vary in mammals during development or in adulthood as a function of seasonal variation in photoperiod. We describe here tissue-specific changes of SRC-1 expression over the course of the day in quail. SRC-1 protein quantified by Western blots in the hindbrain gradually increased in the morning, reached a peak around midday and declined significantly in the afternoon. In contrast, SRC-1 protein levels in the optic lobes progressively decreased in the morning to reach their lowest values around midday before rising in the afternoon. The coactivator concentration in the hippocampus exhibited a progressive increase throughout the day. No change in the SRC-1 protein was detected during the day in the preoptic area and in the cerebellum. The functional significance and the mechanisms of regulation underlying such changes remain to be understood. An important unresolved question is whether this diurnal variation in SRC-1 expression is circadian in nature and if so if SRC-1 is an active player linked to clock genes in the generation of circadian rhythms or if the observed changes in SRC-1 expression are a consequence of the rhythms generated by these genes. [less ▲]

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See detailModulation of steroid-dependent male sexual behavior and neural gene expression: A role for steroid receptor co-activators
Charlier, Thierry ULg; Ball, Gregory F; Balthazart, Jacques ULg

in Trabajos del Instituto Cajal (2005), 80

One of the best-characterized actions of steroids is the regulation of brain areas involved in endocrine function and in the activation of reproductive behaviors in male and female vertebrates. Progress ... [more ▼]

One of the best-characterized actions of steroids is the regulation of brain areas involved in endocrine function and in the activation of reproductive behaviors in male and female vertebrates. Progress in the understanding of the mechanisms that control the expression of the eukaryotic genome by nuclear receptors has brought forward the importance of steroid receptor coactivators in mediating efficient gene transcription. However, little is know about the specific physiological requirements of these coactivators in vivo. In Japanese quail, testosterone treatment of castrated males restores the full copulatory behavior and increases the volume of the sexually dimorphic medial preoptic nucleus (POM) to the level observed in intact males [1]. Testosterone also affects a number of sexually dimorphic neurochemical characteristics such as the vasotocineric innervation of the septum and meadial preoptic nucleus [2]. The quail therefore provides an excellent model to study steroid-dependent sexual behavior and the associated neuroplasticity and should provide insights into the modulation of steroid action by steroid receptor coactivators. The present studies were focused on the steroid receptor co-activator-1 (SRC-1), which was already shown to be involved in the process of sexual differentiation of brain and behavior in rats [3]. We first amplified by RT-PCR from quail brains a 3,411bp fragment highly homologous with the chicken (94.5%) and mammalian (70%) SRC-1 and designed digoxigenin-labeled oligonucleotides for in situ hybridization. A broad distribution of SRC-1 transcripts was observed throughout the male quail brain. A particularly dense coactivator expression was observed in limbic (e.g. POM, nucleus striae terminalis) and mesencephalic (e.g. substantia grisea centralis) nuclei associated with the control of male sexual behavior [4]. Because male and female quail exhibit a very pronounced sexual dimorphism in the steroid-dependent mechanisms that activate male-typical copulatory behavior, we investigated the potential role of SRC-1 in the sexually differentiated responses to steroids by quantifiying the SRC-1 mRNA by real time quantitative polymerase chain reaction (qPCR) and the corresponding protein by western blot (WB). Contrary to previous results, which had identified a higher SRC-1 mRNA expression in the POM of males compared to females [4], we found in two separate experiments that sexually mature females had higher concentrations of SRC-1 in the preoptic area-hypothalamus (HPOA) compared to males. Additional studies should be carried out to identify the origins of this discrepancy but seasonality and time of the day when brains were collected are potentially involved. We also quantified the SRC-1 mRNA and protein in the preoptic area-hypothalamus (HPOA) of castrated males treated or not with testosterone. SRC-1 mRNA was increased by testosterone in two independent experiments but not in a third one. This difference is likely due to the differential manipulations of the birds during these experiments. Birds had been repeatedly handled to test their sexual behavior in the first experiment and we showed that stress tends to decrease the coactivator expression in the male HPOA. This interpretation is strengthened by recent work in rats indicating that stress regulates SRC-1 expression in hypothalamus and hippocampus [5]. More surprisingly, we found a significant correlation between the expression of SRC-1 and the time of the day when birds were killed in the optic lobes, hippocampus and hindbrain. The expression of SRC-1 in the optic lobes increased throughout the day, independently of sex, testosterone treatment or stress. In the hippocampus and hindbrain, the coactivator concentration varied in opposite directions during the morning and afternoon and reached respectively its lowest or highest concentration around the middle of the day, here again independently of sex, stress and hormonal treatment. Together, these data support the idea that SRC-1 is not constitutively expressed but regulated by steroids, stress and possibly other unidentified factors. Differential controls also appear to take place in specific brain nuclei and these differential controls should be further analyzed by immunohistochemistry and in situ hybridization. A second part of our work was dedicated to the study of the physiological significance of SRC-1 whith the use of daily intra-cerebroventricular injections of modified antisense (AS) oligonucleotides (Locked nucleic acid LNA) to disrupt SRC-1 expression in the POM. AS injections significantly reduced the expression of male copulatory behavior in response to exogenous testosterone compared to control animals (Ctrl group) that received the vehicle alone or scrambled (SC) oligonucleotides. Moreover, sexual behavior was restored and even enhanced within 48 hours after interruption of AS injection (ASSC group). Western blot analysis confirmed the decrease of SRC-1 expression in AS animals and demonstrated an over-expression of the coactivator in ASSC animals. The effects of SRC-1 knock down on behavior was related to a reduced POM volume defined by Nissl-staining and aromatase immunohistochemistry. The aromatase index, indicative of the relative amount of aromatase in the POM as well as the vasotocinergic innervation of this nucleus were higher in the Ctrl group. Taken together, these findings indicate that SRC-1 functions as a critical regulatory molecule in the brain to modulate steroid-dependent gene transcription and behavior. The study of the modulation of nuclear receptors activity by different co-regulatory proteins is still in its infancy. Abnormal co-activator expression or function is currently being linked to some endocrine/neurological disorders in humans and it is thus critical to understand how co-activator expression and function are controlled in the developing as well as in the adult brain. [less ▲]

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See detailTestosterone rapidly increases the volume of the medial preoptic nucleus in male Japanese quail
Charlier, Thierry ULg; Ball, Gregory F.; Balthazart, Jacques ULg

Poster (2005)

In many vertebrate species, testosterone (T) influences the volume and cellular characteristics of a variety steroid-dependent nuclei, including the medial preoptic nucleus (POM) of male Japanese quail ... [more ▼]

In many vertebrate species, testosterone (T) influences the volume and cellular characteristics of a variety steroid-dependent nuclei, including the medial preoptic nucleus (POM) of male Japanese quail. The quail POM is a key nucleus in the control of male sexual behavior and exhibits a sex difference (larger in males than in females). In castrated quail, the POM volume is markedly increased by T but previous studies always assessed this effect after a period of 8-14 days and its specific time-course is unknown. We recently reported that antisense treatments suppressing steroid receptor coactivator-1 expression block T effects on POM volume but when treatment was discontinued, a significant increase of POM size occurred within two days. We therefore asked whether this rapid neuroanatomical change was specifically linked to the SCR-1 modulation or reflected the normal rate of T-induced effects. We collected brains from castrated male quail after 1, 2, 8 and 15 days of T treatment (CX+T) while in untreated castrates (CX) brains were collected after 1 or 15 days. The POM volume defined by Nissl staining increased in a time-dependent fashion in CX+T to reach a 40% increase after 15 days while no change was observed in CX. An increase in the average POM volume was detected on day 1 (13%) and this increase was statistically significant (25%) after only 2 days of exposure to T. No volume change was observed in the steroid-insensitive nucleus rotundus. The activation of male sexual behavior was positively correlated with the increase in POM volume. Because new neurons are not incorporated in the adult avian hypothalamus, these rapid volumetric changes must reflect increases in soma size, neuropile or extracellular space. The mechanisms underlying this unexpectedly rapid neural plasticity are currently under study, focusing in particular on the potential modifications of the steroid sensitive aromatase expressing cells. [less ▲]

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See detailModulation of steroid-dependent male sexual behavior and neural gene expression: a role for steroid receptor co-activators
Charlier, Thierry ULg; Ball, Gregory F.; Balthazart, Jacques ULg

in Dawson, Alister; Sharp, Peter J. (Eds.) Functional anvian endocrinology (2005)

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See detailThe roles of testosterone and singing in the regulation of seasonal neuroplasticity in songbirds
Sartor, Jennifer J.; Balthazart, Jacques ULg; Riters, L. V. et al

in Hormones & Behavior (2004, June), 46(1), 121

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See detailSeasonal plasticity in the song control system - Multiple brain sites of steroid hormone action and the importance of variation in song behavior
Ball, Gregory F.; Auger, Catherine J.; Bernard, Daniel J. et al

in Annals of the New York Academy of Sciences (2004), 1016

Birdsong, in non-tropical species, is generally more common in spring and summer when males sing to attract mates and/or defend territories. Changes in the volumes of song control nuclei, such as HVC and ... [more ▼]

Birdsong, in non-tropical species, is generally more common in spring and summer when males sing to attract mates and/or defend territories. Changes in the volumes of song control nuclei, such as HVC and the robust nucleus of the arcopallium (RA), are observed seasonally. Long photoperiods in spring stimulate the recrudescence of the testes and the release of testosterone. Androgen receptors, and at times estrogen receptors, are present in HVC and RA as are co-factors that facilitate the transcriptional activity of these receptors. Thus testosterone can act directly to induce changes in nucleus volume. However, dissociations have been identified at times among long photoperiods, maximal concentrations of testosterone, large song control nuclei, and high rates of song. One explanation of these dissociations is that song behavior itself can influence neural plasticity in the song system. Testosterone can act via brain-derived neurotrophic factor (BDNF) that is also released in HVC as a result of song activity. Testosterone could enhance song nucleus volume indirectly by acting in the preoptic area, a region regulating sexual behaviors, including song, that connects to the song system through catecholaminergic cells. Seasonal neuroplasticity in the song system involves an interplay among seasonal state, testosterone action, and behavioral activity. [less ▲]

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See detailGene knock down via antisense oligonucleotides to the steroid receptor coactivator SRC-1 modulates testosterone-dependent male sexual behavior and neural gene expression
Charlier, Thierry ULg; Ball, Gregory F; Balthazart, Jacques ULg

in Hormones & Behavior (2004), 46

Studies of eukaryotic genome expression demonstrate the importance of steroid receptor coactivators in mediating efficient gene transcription. Little is know about the physiological role of these ... [more ▼]

Studies of eukaryotic genome expression demonstrate the importance of steroid receptor coactivators in mediating efficient gene transcription. Little is know about the physiological role of these coactivators in vivo. We recently showed that the Steroid Receptor Coactivator SRC-1 is densely expressed in steroid-sensitive brain areas in birds and its expression is steroid-dependent and sexually differentiated. We tested the role of SRC-1 in the activation by testosterone of male sexual behavior in quail. Daily injections of LNA antisense oligonucleotides in the third ventricle (AS group) significantly reduced the expression of male copulatory behavior in response to exogenous testosterone compared to control animals (Ctrl group) receiving the vehicle alone or scrambled LNA. Sexual behavior was restored and even enhanced within 48 hours after interruption of LNA injection (ASSC group). Western blot analysis confirmed the decrease of SRC-1 expression in AS animals and suggested an over-expression of the coactivator in ASSC animals. The effect of SRC-1 knock down on behavior was correlated with a reduced volume of the medial preoptic nucleus (POM) defined by Nissl-staining and aromatase immunohistochemistry. In addition, the amount of aromatase-immunoreactive material in POM, defined as the relative optical density of the aromatase immunoreactivity multiplied by the percentage of surface covered within the nucleus and by the total POM volume of the POM, was decreased in the AS compared to the Ctrl group, suggesting a blockade of aromatase transcription. Together, these data indicate that SRC-1 functions as a critical regulatory molecule in the brain that modulates steroid-dependent gene transcription and behavior. [less ▲]

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See detailSex differences in the distribution of the steroid receptor coactivator SRC-1 in the song control nuclei of male and female canaries
Charlier, Thierry ULg; Balthazart, Jacques ULg; Ball, Gregory F

in Brain Research (2003), 959(2), 263-274

The steroid receptor coactivator SRC-1 modulates ligand-dependent transactivation of several nuclear receptors, including the receptors for sex steroid hormones. The distribution of SRC-1 transcripts was ... [more ▼]

The steroid receptor coactivator SRC-1 modulates ligand-dependent transactivation of several nuclear receptors, including the receptors for sex steroid hormones. The distribution of SRC-1 transcripts was analyzed here by in situ hybridization in coronal sections through the brain of male and female canaries. A broad but heterogeneous distribution of SRC-1 transcripts was observed with high numbers of densely labeled cells being present in many steroid-sensitive areas including the medial preoptic nucleus, several hypothalamic nuclei, five song control nuclei (HVc, the lateral and medial portion of the magnocellular nucleus of the anterior neostriatum, area X and the nucleus uvaeformis) and several catecholaminergic areas (area ventralis of Tsai, substantia nigra, locus coeruleus). The volume of two song control nuclei, HVc and area X were reconstructed based on the boundaries of the cell groups exhibiting a denser SRC-1 expression as compared to the surrounding areas. Sex differences in the expression of SRC-1 were also detected in several song control nuclei. In particular, the volume of HVc based on the high density of SRC-1 expression was significantly larger in males than in females. The effect of steroids on the song control system could be, at least in part, indirect and result from a modulation by steroids of the catecholaminergic inputs to the song control nuclei. The presence of the steroid receptor coactivator SRC-1 in the telencephalic song control nuclei and in the catecholaminergic cell groups that innervate the song system supports the idea that SRC-1 expression could play an active role in the control of singing behavior by modulating estrogen and androgen receptor action at both locations. (C) 2002 Elsevier Science B.V. All rights reserved. [less ▲]

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See detailModulation of steroid activity by transcription coactivators in songbirds
Charlier, Thierry ULg; Auger, Catherine J; Balthazart, Jacques ULg et al

in Hormones & Behavior (2003), 44

Songbirds have developed a specialized, steroid-dependent telencephalic vocal control system for the production of learned vocalization. Recent progress in the study of the mechanisms by which steroid ... [more ▼]

Songbirds have developed a specialized, steroid-dependent telencephalic vocal control system for the production of learned vocalization. Recent progress in the study of the mechanisms by which steroid receptors act on the eukaryotic genome has highlighted the role of a newly discovered protein family, the Nuclear Receptor Coactivators. More specifically, the CREB-binding protein (CBP) and the Steroid Receptor Coactivator-1 (SRC-1) have been shown to be actively involved in mediating steroid hormone action in the developing rat brain. The distribution of the coactivator SRC-1 was analyzed in canaries by in situ hybridization. A very broad but heterogeneous distribution of the transcript was observed, mainly in steroid-sensitive areas of the hypothalamus, the song control system and several catecholaminergic areas. The presence of SRC-1 in these regions was also confirmed by immunocytochemistry. A similar very high concentration of the coactivator CBP protein was also found in steroid-sensitive areas of the hypothalamus and in the song system. Sex differences in SRC-1 mRNA concentration were detected in HVC and in area X. Moreover, preliminary data obtained independently in starlings (CBP) and in quail (SRC-1) suggest that the expression of coactivators is regulated by steroids as well as by photoperiod. The presence of these steroid receptor coactivators in the telencephalic song control nuclei and in catecholaminergic cell groups that innervate the song system and their possible regulation by photoperiod and/or steroids support the idea that SRC-1 and CBP could play an important role in the control of singing behavior by modulating estrogen and androgen receptor action. [less ▲]

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See detailCloning and identification of functional domains in quail Brain aromatase
Charlier, Thierry ULg; Baillien, Michelle; Ball, Gregory F. et al

Poster (2003)

Recent evidence indicates that aromatase activity (AA) in the hypothalamus is not only modulated by slow (hours to days) genomic actions but also through fast (seconds to minutes) non-genomic mechanisms ... [more ▼]

Recent evidence indicates that aromatase activity (AA) in the hypothalamus is not only modulated by slow (hours to days) genomic actions but also through fast (seconds to minutes) non-genomic mechanisms. We recently showed that Calcium (Ca2+)-dependent phosphorylations catalyzed by multiple protein kinases including PKC, and possibly PKA and CAMK, rapidly down-regulate AA in quail hypothalamic homogenates. Western blotting experiments also indicated that phosphorylations affect the aromatase molecule itself but it was impossible to fully characterize the putative phosphorylation sites on the quail enzyme because its sequence was unknown. We therefore cloned and sequenced the quail brain aromatase. We identified a 1541-bp open reading frame that encodes a predicted 490-amino acid protein containing all functional domains previously described in mammalian and other avian aromatases. Multiple motifs match consensus sequences corresponding to several protein kinases including those that were shown to affect AA during pharmacological experiments with specific kinase inhibitors (e.g., PKC, PKA, MAPK, Myosine light chain kinase, Tyr. kinase). Another potential control pathway of AA, independent from phosphorylations, could involve a direct control by Ca2+-dependent calmodulin (CAM), as suggested by the identification in Western blots of CAM on purified aromatase from quail hypothalamic homogenates. Accordingly, two Ca2+-dependent calmodulin binding motifs (1-8-14b) as defined by Rhoads and Friedberg (FASEB, 1997, 11:331-340) are present and conserved in most vertebrates including quail aromatase. These results suggest that the phosphorylation of some residues as well as the direct binding of calmodulin on the aromatase protein represent part of the mechanism(s) underlying the rapid changes in AA. [less ▲]

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See detailSeasonal changes in the songbird brain are modulated by song performance via testosterone-dependent and independent action
Sartor, Jennifer J; Charlier, Thierry ULg; Pytte, Caroline L et al

Poster (2002)

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