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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 immunoreactivity in HVC and lMAN neurons that project to RA (HVCRA and LMANRA).Schematic drawing on top illustrates injection of the retrograde tracer cholera toxin subunit B (CTB) and location of retrogradely labeled neurons. A and B: High power views of HVC (A) and lMAN (B) in zRalDH-immunolabeled sections from an adult male zebra finch that received an CTB injection into RA resulting in retrogradely labeled neurons in HVC and lMAN. Left panels show bright field views of zRalDH protein expression, right panels show CTB signal (red) and cell nuclei stained with DAPI (blue) in the same fields. Arrowheads point to zRalDH-immunoreactive cells that are retrogradely labeled. Scale bars: 20µm.
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pone-0111722-g011: zRalDH immunoreactivity in HVC and lMAN neurons that project to RA (HVCRA and LMANRA).Schematic drawing on top illustrates injection of the retrograde tracer cholera toxin subunit B (CTB) and location of retrogradely labeled neurons. A and B: High power views of HVC (A) and lMAN (B) in zRalDH-immunolabeled sections from an adult male zebra finch that received an CTB injection into RA resulting in retrogradely labeled neurons in HVC and lMAN. Left panels show bright field views of zRalDH protein expression, right panels show CTB signal (red) and cell nuclei stained with DAPI (blue) in the same fields. Arrowheads point to zRalDH-immunoreactive cells that are retrogradely labeled. Scale bars: 20µm.

Mentions: A close look revealed that while zRalDH immunolabeling in HVC and lMAN was concentrated in cell somata (fig. 10.F,G), it was diffuse in RA (fig. 10.E), a pattern consistent with zRalDH distribution at synaptic endings of afferent projection fibers. When we combined zRalDH immunohistochemistry with retrograde tracer injections into RA, zRalDH-labeled cells in HVC and lMAN co-localized with the retrogradely-labeled cell somata in these nuclei, corresponding to HVCRA and lMANRA projection neurons (fig. 11). Area X also exhibited a diffuse zRalDH immunostaining (fig. 10.D), which could stem from either lMAN or HVC. In the case of Area X, however, no zRalDH positive fiber tracts were visible (fig. 10.D).


Long-distance retinoid signaling in the zebra finch brain.

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

zRalDH immunoreactivity in HVC and lMAN neurons that project to RA (HVCRA and LMANRA).Schematic drawing on top illustrates injection of the retrograde tracer cholera toxin subunit B (CTB) and location of retrogradely labeled neurons. A and B: High power views of HVC (A) and lMAN (B) in zRalDH-immunolabeled sections from an adult male zebra finch that received an CTB injection into RA resulting in retrogradely labeled neurons in HVC and lMAN. Left panels show bright field views of zRalDH protein expression, right panels show CTB signal (red) and cell nuclei stained with DAPI (blue) in the same fields. Arrowheads point to zRalDH-immunoreactive cells that are retrogradely labeled. Scale bars: 20µm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0111722-g011: zRalDH immunoreactivity in HVC and lMAN neurons that project to RA (HVCRA and LMANRA).Schematic drawing on top illustrates injection of the retrograde tracer cholera toxin subunit B (CTB) and location of retrogradely labeled neurons. A and B: High power views of HVC (A) and lMAN (B) in zRalDH-immunolabeled sections from an adult male zebra finch that received an CTB injection into RA resulting in retrogradely labeled neurons in HVC and lMAN. Left panels show bright field views of zRalDH protein expression, right panels show CTB signal (red) and cell nuclei stained with DAPI (blue) in the same fields. Arrowheads point to zRalDH-immunoreactive cells that are retrogradely labeled. Scale bars: 20µm.
Mentions: A close look revealed that while zRalDH immunolabeling in HVC and lMAN was concentrated in cell somata (fig. 10.F,G), it was diffuse in RA (fig. 10.E), a pattern consistent with zRalDH distribution at synaptic endings of afferent projection fibers. When we combined zRalDH immunohistochemistry with retrograde tracer injections into RA, zRalDH-labeled cells in HVC and lMAN co-localized with the retrogradely-labeled cell somata in these nuclei, corresponding to HVCRA and lMANRA projection neurons (fig. 11). Area X also exhibited a diffuse zRalDH immunostaining (fig. 10.D), which could stem from either lMAN or HVC. In the case of Area X, however, no zRalDH positive fiber tracts were visible (fig. 10.D).

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