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Long-distance retinoid signaling in the zebra finch brain.

Roeske TC, Scharff C, Olson CR, Nshdejan A, Mello CV - PLoS ONE (2014)

Bottom Line: Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts.This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling.Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Hunter College, City University of New York, New York, New York, United States of America.

ABSTRACT
All-trans retinoic acid (ATRA), the main active metabolite of vitamin A, is a powerful signaling molecule that regulates large-scale morphogenetic processes during vertebrate embryonic development, but is also involved post-natally in regulating neural plasticity and cognition. In songbirds, it plays an important role in the maturation of learned song. The distribution of the ATRA-synthesizing enzyme, zRalDH, and of ATRA receptors (RARs) have been described, but information on the distribution of other components of the retinoid signaling pathway is still lacking. To address this gap, we have determined the expression patterns of two obligatory RAR co-receptors, the retinoid X receptors (RXR) α and γ, and of the three ATRA-degrading cytochromes CYP26A1, CYP26B1, and CYP26C1. We have also studied the distribution of zRalDH protein using immunohistochemistry, and generated a refined map of ATRA localization, using a modified reporter cell assay to examine entire brain sections. Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts. This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling. Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

No MeSH data available.


Related in: MedlinePlus

RXRα expression in song control nuclei of adult male zebra finch.A: Schematic of a parasagittal section at the level of song nuclei HVC, RA, Area X, and lMAN. The dashed rectangles indicate the areas shown in B, D, and G. Photos in B–H are bright field views of parasagittal sections hybridized with digoxigenin-labeled RXRα antisense probe. Anterior is right, dorsal is up in all panels. B, C: Expression in RA. Many cells were strongly labeled; the surrounding arcopallium showed less labeling. D-F: Expression in lMAN and Area X. Expression is comparable to the surrounding areas, but lower in Area X/striatum than in lMAN/nidopallium. G, H: Expression in HVC. The high expression is comparable to the adjacent nidopallium. In C, E, F, and H, black arrows depict strongly labeled cells, gray arrows weakly labeled cells, and white arrows unlabeled cells. Scale bars  = 200µm in B, D, G; 20µm in C, E, F, H.
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pone-0111722-g004: RXRα expression in song control nuclei of adult male zebra finch.A: Schematic of a parasagittal section at the level of song nuclei HVC, RA, Area X, and lMAN. The dashed rectangles indicate the areas shown in B, D, and G. Photos in B–H are bright field views of parasagittal sections hybridized with digoxigenin-labeled RXRα antisense probe. Anterior is right, dorsal is up in all panels. B, C: Expression in RA. Many cells were strongly labeled; the surrounding arcopallium showed less labeling. D-F: Expression in lMAN and Area X. Expression is comparable to the surrounding areas, but lower in Area X/striatum than in lMAN/nidopallium. G, H: Expression in HVC. The high expression is comparable to the adjacent nidopallium. In C, E, F, and H, black arrows depict strongly labeled cells, gray arrows weakly labeled cells, and white arrows unlabeled cells. Scale bars  = 200µm in B, D, G; 20µm in C, E, F, H.

Mentions: RXRα expression was moderately high in pallial HVC, RA, and lMAN and very low in striatal Area X (fig. 4). Within HVC, most strongly labeled cells were large with a neuron-like shape, but cells with different degrees of labeling, as well as non-labeled cells, were found as well (fig. 4.G,H). In RA, many cells showed high expression, but weakly or unlabeled cells also existed (fig. 4.B,C). In lMAN, only the large cells were strongly labeled, the several unlabeled smaller cells contributing to the apparent lower overall expression than in the adjacent nidopallium. (fig. 4.D,E). Area X lacked strongly labeled cells altogether; instead, many weakly labeled and non-labeled cells were seen (fig. 4.F). Staining in RA differed markedly from its surrounds, where labeling was weaker (fig. 4.B and 3.D,E), while staining was more similar between Area X, lMAN, HVC, and their surrounds (fig. 4.D,G). lMAN expression differed markedly across individuals, ranging from distinctively lower to comparable to the surrounding nidopallium (fig. 4.D, for further analysis of expression variability in lMAN, see below).


Long-distance retinoid signaling in the zebra finch brain.

Roeske TC, Scharff C, Olson CR, Nshdejan A, Mello CV - PLoS ONE (2014)

RXRα expression in song control nuclei of adult male zebra finch.A: Schematic of a parasagittal section at the level of song nuclei HVC, RA, Area X, and lMAN. The dashed rectangles indicate the areas shown in B, D, and G. Photos in B–H are bright field views of parasagittal sections hybridized with digoxigenin-labeled RXRα antisense probe. Anterior is right, dorsal is up in all panels. B, C: Expression in RA. Many cells were strongly labeled; the surrounding arcopallium showed less labeling. D-F: Expression in lMAN and Area X. Expression is comparable to the surrounding areas, but lower in Area X/striatum than in lMAN/nidopallium. G, H: Expression in HVC. The high expression is comparable to the adjacent nidopallium. In C, E, F, and H, black arrows depict strongly labeled cells, gray arrows weakly labeled cells, and white arrows unlabeled cells. Scale bars  = 200µm in B, D, G; 20µm in C, E, F, H.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4230966&req=5

pone-0111722-g004: RXRα expression in song control nuclei of adult male zebra finch.A: Schematic of a parasagittal section at the level of song nuclei HVC, RA, Area X, and lMAN. The dashed rectangles indicate the areas shown in B, D, and G. Photos in B–H are bright field views of parasagittal sections hybridized with digoxigenin-labeled RXRα antisense probe. Anterior is right, dorsal is up in all panels. B, C: Expression in RA. Many cells were strongly labeled; the surrounding arcopallium showed less labeling. D-F: Expression in lMAN and Area X. Expression is comparable to the surrounding areas, but lower in Area X/striatum than in lMAN/nidopallium. G, H: Expression in HVC. The high expression is comparable to the adjacent nidopallium. In C, E, F, and H, black arrows depict strongly labeled cells, gray arrows weakly labeled cells, and white arrows unlabeled cells. Scale bars  = 200µm in B, D, G; 20µm in C, E, F, H.
Mentions: RXRα expression was moderately high in pallial HVC, RA, and lMAN and very low in striatal Area X (fig. 4). Within HVC, most strongly labeled cells were large with a neuron-like shape, but cells with different degrees of labeling, as well as non-labeled cells, were found as well (fig. 4.G,H). In RA, many cells showed high expression, but weakly or unlabeled cells also existed (fig. 4.B,C). In lMAN, only the large cells were strongly labeled, the several unlabeled smaller cells contributing to the apparent lower overall expression than in the adjacent nidopallium. (fig. 4.D,E). Area X lacked strongly labeled cells altogether; instead, many weakly labeled and non-labeled cells were seen (fig. 4.F). Staining in RA differed markedly from its surrounds, where labeling was weaker (fig. 4.B and 3.D,E), while staining was more similar between Area X, lMAN, HVC, and their surrounds (fig. 4.D,G). lMAN expression differed markedly across individuals, ranging from distinctively lower to comparable to the surrounding nidopallium (fig. 4.D, for further analysis of expression variability in lMAN, see below).

Bottom Line: Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts.This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling.Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Hunter College, City University of New York, New York, New York, United States of America.

ABSTRACT
All-trans retinoic acid (ATRA), the main active metabolite of vitamin A, is a powerful signaling molecule that regulates large-scale morphogenetic processes during vertebrate embryonic development, but is also involved post-natally in regulating neural plasticity and cognition. In songbirds, it plays an important role in the maturation of learned song. The distribution of the ATRA-synthesizing enzyme, zRalDH, and of ATRA receptors (RARs) have been described, but information on the distribution of other components of the retinoid signaling pathway is still lacking. To address this gap, we have determined the expression patterns of two obligatory RAR co-receptors, the retinoid X receptors (RXR) α and γ, and of the three ATRA-degrading cytochromes CYP26A1, CYP26B1, and CYP26C1. We have also studied the distribution of zRalDH protein using immunohistochemistry, and generated a refined map of ATRA localization, using a modified reporter cell assay to examine entire brain sections. Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts. This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling. Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

No MeSH data available.


Related in: MedlinePlus