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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

RXRγ expression in Area X of adult male zebra finch.A: Drawing of a parasagittal section of adult brain, indicating detail area shown in B; anterior is to the right, dorsal is up. For abbreviations see table 1. B: Detail view of Area X and surrounding area in section processed for RXRγ ISH showing sparse labeled cells in Area X. D: High-magnification view of Area X; black and white arrows depict labeled and unlabeled cells, respectively. Scale bars: 2mm in B, 200µm in C, 50µm in D.
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pone-0111722-g006: RXRγ expression in Area X of adult male zebra finch.A: Drawing of a parasagittal section of adult brain, indicating detail area shown in B; anterior is to the right, dorsal is up. For abbreviations see table 1. B: Detail view of Area X and surrounding area in section processed for RXRγ ISH showing sparse labeled cells in Area X. D: High-magnification view of Area X; black and white arrows depict labeled and unlabeled cells, respectively. Scale bars: 2mm in B, 200µm in C, 50µm in D.

Mentions: RXRγ expression was low and could not be visualized with phosphorimager autoradiography. However, high-power examination of sections reacted with digoxigenin-labeled riboprobes revealed expression in a discrete cell population within Area X (fig. 6); no other RXRγ positive cells were found in the subpallium or pallium. These RXRγ positive cells were large and sparsely distributed (fig. 6.B,C). The same pattern was found in juvenile males (42 and 64 days old; not shown).


Long-distance retinoid signaling in the zebra finch brain.

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

RXRγ expression in Area X of adult male zebra finch.A: Drawing of a parasagittal section of adult brain, indicating detail area shown in B; anterior is to the right, dorsal is up. For abbreviations see table 1. B: Detail view of Area X and surrounding area in section processed for RXRγ ISH showing sparse labeled cells in Area X. D: High-magnification view of Area X; black and white arrows depict labeled and unlabeled cells, respectively. Scale bars: 2mm in B, 200µm in C, 50µm in D.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0111722-g006: RXRγ expression in Area X of adult male zebra finch.A: Drawing of a parasagittal section of adult brain, indicating detail area shown in B; anterior is to the right, dorsal is up. For abbreviations see table 1. B: Detail view of Area X and surrounding area in section processed for RXRγ ISH showing sparse labeled cells in Area X. D: High-magnification view of Area X; black and white arrows depict labeled and unlabeled cells, respectively. Scale bars: 2mm in B, 200µm in C, 50µm in D.
Mentions: RXRγ expression was low and could not be visualized with phosphorimager autoradiography. However, high-power examination of sections reacted with digoxigenin-labeled riboprobes revealed expression in a discrete cell population within Area X (fig. 6); no other RXRγ positive cells were found in the subpallium or pallium. These RXRγ positive cells were large and sparsely distributed (fig. 6.B,C). The same pattern was found in juvenile males (42 and 64 days old; not shown).

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