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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 higher auditory areas of adult male zebra finch telencephalon.A: Drawing of a parasagittal section at the level of the auditory areas NCM, Field L2a, and CMM. The dashed rectangle indicates the area shown in B. B–D: Bright-field views of parasagittal sections processed for RXRα in situ hybridization. Anterior is right, dorsal is up in all panels. B: Low power view of higher auditory areas, with strong labeling in NCM and CMM and lower labeling in L2a. C, D: High power views of NCM and CMM, respectively; black arrows depict strongly labeled cells in clusters, white arrows depict unlabeled cells. Scale bars  = 200µm in B; 20µm in C, D.
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pone-0111722-g005: RXRα expression in higher auditory areas of adult male zebra finch telencephalon.A: Drawing of a parasagittal section at the level of the auditory areas NCM, Field L2a, and CMM. The dashed rectangle indicates the area shown in B. B–D: Bright-field views of parasagittal sections processed for RXRα in situ hybridization. Anterior is right, dorsal is up in all panels. B: Low power view of higher auditory areas, with strong labeling in NCM and CMM and lower labeling in L2a. C, D: High power views of NCM and CMM, respectively; black arrows depict strongly labeled cells in clusters, white arrows depict unlabeled cells. Scale bars  = 200µm in B; 20µm in C, D.

Mentions: RXRα expression was also high in auditory NCM and CMM; fig. 5.A,B), in contrast to the low expression in the adjacent core thalamorecipient field L2a (fig. 5.B) and in the overlying hippocampus. Numerous high RXRα-expressing cells occurred throughout NCM and CMM (fig. 5.C,D), although negative cells were also present (see fig. 5.C,D; white arrows).


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 higher auditory areas of adult male zebra finch telencephalon.A: Drawing of a parasagittal section at the level of the auditory areas NCM, Field L2a, and CMM. The dashed rectangle indicates the area shown in B. B–D: Bright-field views of parasagittal sections processed for RXRα in situ hybridization. Anterior is right, dorsal is up in all panels. B: Low power view of higher auditory areas, with strong labeling in NCM and CMM and lower labeling in L2a. C, D: High power views of NCM and CMM, respectively; black arrows depict strongly labeled cells in clusters, white arrows depict unlabeled cells. Scale bars  = 200µm in B; 20µm in C, D.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0111722-g005: RXRα expression in higher auditory areas of adult male zebra finch telencephalon.A: Drawing of a parasagittal section at the level of the auditory areas NCM, Field L2a, and CMM. The dashed rectangle indicates the area shown in B. B–D: Bright-field views of parasagittal sections processed for RXRα in situ hybridization. Anterior is right, dorsal is up in all panels. B: Low power view of higher auditory areas, with strong labeling in NCM and CMM and lower labeling in L2a. C, D: High power views of NCM and CMM, respectively; black arrows depict strongly labeled cells in clusters, white arrows depict unlabeled cells. Scale bars  = 200µm in B; 20µm in C, D.
Mentions: RXRα expression was also high in auditory NCM and CMM; fig. 5.A,B), in contrast to the low expression in the adjacent core thalamorecipient field L2a (fig. 5.B) and in the overlying hippocampus. Numerous high RXRα-expressing cells occurred throughout NCM and CMM (fig. 5.C,D), although negative cells were also present (see fig. 5.C,D; white arrows).

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