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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

zRalDH protein expression in areas of adult male zebra finch brain that express or lack zRalDH mRNA.A: Drawing indicates location of images shown in other panels. B: zRalDH mRNA expression by in situ hybridization, level similar to A. C–G: zRalDH protein detection through immunohistochemistry. C: HVC and RA, as well as the fiber tracts extending from HVC to RA (arrows) are labeled. D: lMAN and surrounding nidopallium, as well as Area X, are labeled; labeling in Area X is diffuse and not in somata. Thus, besides HVC and lMAN, which express zRalDH mRNA, protein is present in two song nuclei (X and RA) that lack zRalDH transcript (white arrows in B). E: Detail view of zRalDH protein in RA; labeling is diffuse and not in somata. F: Detail view of zRalDH protein in HVC, somata are labeled. G: High power view of zRalDH in lMAN, somata are labeled. In all panels, frontal is to the right, and dorsal is up. For abbreviations, see table 1.Scale bars for C = 0.5 mm; D–F = 100µm, G = 50µm.
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pone-0111722-g010: zRalDH protein expression in areas of adult male zebra finch brain that express or lack zRalDH mRNA.A: Drawing indicates location of images shown in other panels. B: zRalDH mRNA expression by in situ hybridization, level similar to A. C–G: zRalDH protein detection through immunohistochemistry. C: HVC and RA, as well as the fiber tracts extending from HVC to RA (arrows) are labeled. D: lMAN and surrounding nidopallium, as well as Area X, are labeled; labeling in Area X is diffuse and not in somata. Thus, besides HVC and lMAN, which express zRalDH mRNA, protein is present in two song nuclei (X and RA) that lack zRalDH transcript (white arrows in B). E: Detail view of zRalDH protein in RA; labeling is diffuse and not in somata. F: Detail view of zRalDH protein in HVC, somata are labeled. G: High power view of zRalDH in lMAN, somata are labeled. In all panels, frontal is to the right, and dorsal is up. For abbreviations, see table 1.Scale bars for C = 0.5 mm; D–F = 100µm, G = 50µm.

Mentions: To examine whether transport of zRalDH protein to brain sites distant from transcription sites could account for the broad distribution of ATRA-induced LacZ expression, we localized zRalDH protein using immunohistochemistry (fig. S3). Table S3 summarizes the birds used for zRalDH immunohistochemistry, and the treatments they underwent. We detected immunoreactivity not only in all brain areas that expressed the zRalDH transcript (i.e. the rostral nidopallium including lMAN, the hyperpallium, and HVC) but also in Area X and RA (fig. 10).


Long-distance retinoid signaling in the zebra finch brain.

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

zRalDH protein expression in areas of adult male zebra finch brain that express or lack zRalDH mRNA.A: Drawing indicates location of images shown in other panels. B: zRalDH mRNA expression by in situ hybridization, level similar to A. C–G: zRalDH protein detection through immunohistochemistry. C: HVC and RA, as well as the fiber tracts extending from HVC to RA (arrows) are labeled. D: lMAN and surrounding nidopallium, as well as Area X, are labeled; labeling in Area X is diffuse and not in somata. Thus, besides HVC and lMAN, which express zRalDH mRNA, protein is present in two song nuclei (X and RA) that lack zRalDH transcript (white arrows in B). E: Detail view of zRalDH protein in RA; labeling is diffuse and not in somata. F: Detail view of zRalDH protein in HVC, somata are labeled. G: High power view of zRalDH in lMAN, somata are labeled. In all panels, frontal is to the right, and dorsal is up. For abbreviations, see table 1.Scale bars for C = 0.5 mm; D–F = 100µm, G = 50µm.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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pone-0111722-g010: zRalDH protein expression in areas of adult male zebra finch brain that express or lack zRalDH mRNA.A: Drawing indicates location of images shown in other panels. B: zRalDH mRNA expression by in situ hybridization, level similar to A. C–G: zRalDH protein detection through immunohistochemistry. C: HVC and RA, as well as the fiber tracts extending from HVC to RA (arrows) are labeled. D: lMAN and surrounding nidopallium, as well as Area X, are labeled; labeling in Area X is diffuse and not in somata. Thus, besides HVC and lMAN, which express zRalDH mRNA, protein is present in two song nuclei (X and RA) that lack zRalDH transcript (white arrows in B). E: Detail view of zRalDH protein in RA; labeling is diffuse and not in somata. F: Detail view of zRalDH protein in HVC, somata are labeled. G: High power view of zRalDH in lMAN, somata are labeled. In all panels, frontal is to the right, and dorsal is up. For abbreviations, see table 1.Scale bars for C = 0.5 mm; D–F = 100µm, G = 50µm.
Mentions: To examine whether transport of zRalDH protein to brain sites distant from transcription sites could account for the broad distribution of ATRA-induced LacZ expression, we localized zRalDH protein using immunohistochemistry (fig. S3). Table S3 summarizes the birds used for zRalDH immunohistochemistry, and the treatments they underwent. We detected immunoreactivity not only in all brain areas that expressed the zRalDH transcript (i.e. the rostral nidopallium including lMAN, the hyperpallium, and HVC) but also in Area X and RA (fig. 10).

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