DNA methylation regulates transcription factor specific neurodevelopmental but not sexually dimorphic gene expression dynamics in zebra finch telencephalon
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ABSTRACT:
ORGANISM(S): Taeniopygia guttata
PROVIDER: GSE147974 | GEO | 2021/04/07
REPOSITORIES: GEO
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Project description:Song learning in zebra finches (Taeniopygia guttata) is a prototypical example of a complex learned behavior, yet knowledge of the underlying molecular processes is limited. Therefore, we characterized transcriptomic (RNA-sequencing) and epigenomic (RRBS, reduced representation bisulfite sequencing; immunofluorescence) dynamics in matched zebra finch telencephalon samples of both sexes from 1 day post hatching (1 dph) to adulthood, spanning the critical period for song learning (20 and 65 dph). We identified extensive transcriptional neurodevelopmental changes during postnatal telencephalon development. DNA methylation was very low, yet increased over time, particularly in song control nuclei. Only a small fraction of the massive differential expression in the developing zebra finch telencephalon could be explained by differential CpG and CpH DNA methylation. However, a strong association between DNA methylation and age-dependent gene expression was found for various transcription factors (i.e., OTX2, AR, and FOS) involved in neurodevelopment. Incomplete dosage compensation, independent of DNA methylation, was found to be largely responsible for sexually dimorphic gene expression, with dosage compensation increasing throughout life. In conclusion, our results indicate that DNA methylation regulates neurodevelopmental gene expression dynamics through steering transcription factor activity, but does not explain sexually dimorphic gene expression patterns in zebra finch telencephalon.
| S-EPMC8017237 | biostudies-literature
Project description:Song learning in zebra finches is a prototypical example of a complex learned behavior, yet knowledge on the underlying molecular processes is limited. Therefore, we characterized transcriptomic (RNA sequencing) and epigenomic (RRBS, reduced representation bisulfite sequencing; immunofluorescence) dynamics in matched zebra finch telencephalon samples of both sexes from 1 day post hatching (1 dph) to adulthood, spanning the critical period for song learning (20 dph and 65 dph). We identified extensive transcriptional neurodevelopmental changes during postnatal telencephalon development. DNA (hydroxy)methylation was very low, yet increased over time, particularly in song control nuclei. Only a small fraction of the massive differential expression in the developing zebra finch telencephalon could be explained by differential CpG and CpH DNA methylation. However, a strong association between DNA methylation and age dependent gene expression was found for various transcription factors (i.a. OTX2, AR and FOS) involved in neurodevelopment. Additionally, genomic regions featured by age dependent differential methylation in differentially expressed genes were significantly enriched for specific transcription factor binding motifs. Incomplete dosage compensation was found to be largely responsible for sexually dimorphic gene expression, with dosage compensation increasing throughout life. In conclusion, our results indicate that DNA methylation regulates neurodevelopmental gene expression dynamics through steering transcription factor activity, but does not explain sexually dimorphic gene expression patterns in zebra finch telencephalon.
2021-04-07 | GSE147973 | GEO
Project description:Song learning in zebra finches is a prototypical example of a complex learned behavior, yet knowledge on the underlying molecular processes is limited. Therefore, we characterized transcriptomic (RNA sequencing) and epigenomic (RRBS, reduced representation bisulfite sequencing; immunofluorescence) dynamics in matched zebra finch telencephalon samples of both sexes from 1 day post hatching (1 dph) to adulthood, spanning the critical period for song learning (20 dph and 65 dph). We identified extensive transcriptional neurodevelopmental changes during postnatal telencephalon development. DNA (hydroxy)methylation was very low, yet increased over time, particularly in song control nuclei. Only a small fraction of the massive differential expression in the developing zebra finch telencephalon could be explained by differential CpG and CpH DNA methylation. However, a strong association between DNA methylation and age dependent gene expression was found for various transcription factors (i.a. OTX2, AR and FOS) involved in neurodevelopment. Additionally, genomic regions featured by age dependent differential methylation in differentially expressed genes were significantly enriched for specific transcription factor binding motifs. Incomplete dosage compensation was found to be largely responsible for sexually dimorphic gene expression, with dosage compensation increasing throughout life. In conclusion, our results indicate that DNA methylation regulates neurodevelopmental gene expression dynamics through steering transcription factor activity, but does not explain sexually dimorphic gene expression patterns in zebra finch telencephalon.
2021-04-07 | GSE147972 | GEO
Project description:DNA methylation regulates transcription factor specific neurodevelopmental but not sexually dimorphic gene expression dynamics in zebra finch telencephalon
| PRJNA622686 | ENA
Project description:DNA methylation regulates transcription factor specific neurodevelopmental but not sexually dimorphic gene expression dynamics in zebra finch telencephalon [RRBS]
| PRJNA622689 | ENA
Project description:DNA methylation regulates transcription factor specific neurodevelopmental but not sexually dimorphic gene expression dynamics in zebra finch telencephalon [RNA-Seq]
| PRJNA622690 | ENA
Project description:Sexual differentiation of the zebra finch (Taeniopygia guttata) neural song circuit is thought to be initiated by sex differences in sex chromosome gene expression in brain cells. One theory is that Z-linked genes, present in the male's ZZ genome at double the dose of females' (ZW), are expressed at higher levels and trigger masculine patterns of development. We report here that trkB (tyrosine kinase receptor B) is Z-linked in zebra finches. trkB is the receptor for neurotrophic factors BDNF and neurotrophin 4, and mediates their influence on neuronal survival, migration, and specification. trkB mRNA is expressed at a higher level in the male telencephalon or whole brain than in corresponding regions of the female in adulthood, and at posthatch day (P) 6, when the song circuit is undergoing sexual differentiation. Moreover, this expression is higher in the song nucleus high vocal center (HVC) than in the surrounding telencephalon at P6, and in males relative to females. In addition, trkB protein is expressed more highly in male than female whole brain at P6. These results establish trkB as a candidate factor that contributes to masculine differentiation of HVC because of its Z-linkage, which leads to sex differences in expression. BDNF is known to be stimulated by estrogen and to be expressed at higher levels in males than females at later ages in HVC. Thus, the trkB-BDNF system may be a focal point for convergent masculinizing influences of Z-linked factors and hormones.
| S-EPMC1140405 | biostudies-literature
Project description:BackgroundIn Drosophila, male courtship behavior is regulated in large part by the gene fruitless (fru). fru encodes a set of putative transcription factors that promote male sexual behavior by controlling the development of sexually dimorphic neuronal circuitry. Little is known about how Fru proteins function at the level of transcriptional regulation or the role that isoform diversity plays in the formation of a male-specific nervous system.ResultsTo characterize the roles of sex-specific Fru isoforms in specifying male behavior, we generated novel isoform-specific mutants and used a genomic approach to identify direct Fru isoform targets during development. We demonstrate that all Fru isoforms directly target genes involved in the development of the nervous system, with individual isoforms exhibiting unique binding specificities. We observe that fru behavioral phenotypes are specified by either a single isoform or a combination of isoforms. Finally, we illustrate the utility of these data for the identification of novel sexually dimorphic genomic enhancers and novel downstream regulators of male sexual behavior.ConclusionsThese findings suggest that Fru isoform diversity facilitates both redundancy and specificity in gene expression, and that the regulation of neuronal developmental genes may be the most ancient and conserved role of fru in the specification of a male-specific nervous system.
| S-EPMC3969260 | biostudies-literature
Project description:The expression of the recently identified neuropeptide, amylin, is restricted in rodents to the postpartum preoptic area and may play a role in the control of parental behaviours and food intake. These processes are substantially different between bird and rodent parents as birds do not lactate but often show biparental care of the offspring. To establish the presence and role of amylin in the bird brain, in the present study, we investigated the distribution of amylin in brains of adult male and female zebra finches in three different reproductive stages (i.e. paired without young, incubating eggs or provisioning nestlings) and in unpaired control birds living in same sex flocks. Amylin mRNA was identified in the hypothalamus of zebra finch by RT-PCR, which was also used to produce probes for in situ hybridisation. Subsequently, in situ hybridisation histochemistry was performed in brain sections, and the labelling signal was quantified and compared between the groups. Amylin showed a much wider brain distribution than that of rodents. A strong and, in some regions, sexually dimorphic label was found in the striatum and several brain regions of the social behavioural network in both males and females. Many regions responsible for the learning of birdsong also contained amylin-positive neurons, and some regions showed sex differences reflecting the fact that vocalisation is sexually dimorphic in the zebra finch: only males sing. Area X (Ar.X), a striatal song centre present only in males, was labelled in paired but not unpaired male. Ar.X, another song centre, the lateral part of the magnocellular nucleus of the anterior nidopallium (lMAN) also contained amylin and had higher amylin label in paired, as opposed to unpaired birds. The wider distribution of amylin in birds as compared to rodents suggests a more general role of amylin in social or other behaviours in avian species than in mammals. Alternatively, parental care in birds may be a more complex behavioural trait involving a wider set of brain regions. The sex differences in song centres, and the changes with reproductive status suggest a participation of amylin in social behaviours and related changes in the singing of males.
| S-EPMC6971405 | biostudies-literature
Project description:Cannabinoids are well-established to alter processes of sensory perception; however neurophysiological mechanisms responsible remain unclear. Arc, an immediate-early gene (IEG) product involved in dendritic spine dynamics and necessary for plasticity changes such as long-term potentiation, is rapidly induced within zebra finch caudal medial nidopallium (NCM) following novel song exposure, a response that habituates after repeated stimuli. Arc appears unique in its rapid postsynaptic dendritic expression following excitatory input. Previously, we found that vocal development-altering cannabinoid treatments are associated with elevated dendritic spine densities in motor-(HVC) and learning-related (Area X) song regions of zebra finch telencephalon. Given Arc's dendritic morphological role, we hypothesized that cannabinoid-altered spine densities may involve Arc-related signaling. To test this, we examined the ability of the cannabinoid agonist WIN55212-2 (WIN) to (1) acutely disrupt song-induced Arc expression, (2) interfere with habituation to auditory stimuli, and (3) alter dendritic spine densities in auditory regions. We found that WIN (3mg/kg) acutely reduced Arc expression within both NCM and Field L2 in an antagonist-reversible manner. WIN did not alter Arc expression in thalamic auditory relay nucleus ovoidalis (Ov), suggesting that cannabinoid signaling selectively alters responses to auditory stimulation. Novel song stimulation rapidly increased dendritic spine densities within auditory telencephalon, an effect blocked by WIN pretreatments. Taken together, cannabinoid inhibition of both Arc induction and its habituation to repeated stimuli, combined with prevention of rapid increases in dendritic spine densities, implicates cannabinoid signaling in modulation of physiological processes important to auditory responsiveness and memory.
| S-EPMC3891467 | biostudies-other