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Post-transcriptional regulation of zenk expression associated with zebra finch vocal development.

ABSTRACT: In the male zebra finch, highly variable juvenile song and stereotyped adult song induce mRNA expression of the immediate early gene zenk in telencephalon. However, the functional consequences of this behavior-driven gene expression remain unknown. Here we characterize the developmental expression of zenk mRNA and protein in two forebrain song regions (HVC, the higher vocal center, and RA, the robust nucleus of the archistriatum). In HVC, singing results in similar percentages of cells producing zenk mRNA and zenk protein at different stages of vocal development. Similarly, song behavior at all stages of vocal development induces a comparable percentage of RA cells expressing zenk mRNA. However, the percentage of RA zenk immunoreactive cells is low during early vocal learning, increasing only as the vocal pattern matures. Early induction of a stereotyped vocal pattern in juvenile birds is associated with increased zenk immunoreactivity in RA, indicating that it is the form of the behavior (and not the age of the bird) that correlates with changes in zenk immunoreactivity. Together, our findings reveal a previously unrecognized relationship between behavioral development and post-transcriptional gene regulation.

SUBMITTER: Whitney O

PROVIDER: S-EPMC4249626 | biostudies-literature | 2000 Sep

REPOSITORIES: biostudies-literature

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Post-transcriptional regulation of zenk expression associated with zebra finch vocal development.

Whitney O O Soderstrom K K Johnson F F

Brain research. Molecular brain research 20000901 2

In the male zebra finch, highly variable juvenile song and stereotyped adult song induce mRNA expression of the immediate early gene zenk in telencephalon. However, the functional consequences of this behavior-driven gene expression remain unknown. Here we characterize the developmental expression of zenk mRNA and protein in two forebrain song regions (HVC, the higher vocal center, and RA, the robust nucleus of the archistriatum). In HVC, singing results in similar percentages of cells producing ...[more]

PMID: 11038263

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Project description:Among songbirds, the zebra finch (Taeniopygia guttata) is an excellent model system for investigating the neural mechanisms underlying complex behaviours such as vocal communication, learning and social interactions. Neuropeptides and peptide hormones are cell-to-cell signalling molecules known to mediate similar behaviours in other animals. However, in the zebra finch, this information is limited. With the newly-released zebra finch genome as a foundation, we combined bioinformatics, mass-spectrometry (MS)-enabled peptidomics and molecular techniques to identify the complete suite of neuropeptide prohormones and final peptide products and their distributions.Complementary bioinformatic resources were integrated to survey the zebra finch genome, identifying 70 putative prohormones. Ninety peptides derived from 24 predicted prohormones were characterized using several MS platforms; tandem MS confirmed a majority of the sequences. Most of the peptides described here were not known in the zebra finch or other avian species, although homologous prohormones exist in the chicken genome. Among the zebra finch peptides discovered were several unique vasoactive intestinal and adenylate cyclase activating polypeptide 1 peptides created by cleavage at sites previously unreported in mammalian prohormones. MS-based profiling of brain areas required for singing detected 13 peptides within one brain nucleus, HVC; in situ hybridization detected 13 of the 15 prohormone genes examined within at least one major song control nucleus. Expression mapping also identified prohormone messenger RNAs in areas associated with spatial learning and social behaviours. Based on the whole-genome analysis, 40 prohormone probes were found on a commonly used zebra finch brain microarray. Analysis of these newly annotated transcripts revealed that six prohormone probes showed altered expression after birds heard song playbacks in a paradigm of song recognition learning; we partially verify this result experimentally.The zebra finch peptidome and prohormone complement is now characterized. Based on previous microarray results on zebra finch vocal learning and synaptic plasticity, a number of these prohormones show significant changes during learning. Interestingly, most mammalian prohormones have counterparts in the zebra finch, demonstrating that this songbird uses similar biochemical pathways for neurotransmission and hormonal regulation. These findings enhance investigation into neuropeptide-mediated mechanisms of brain function, learning and behaviour in this model.

Project description:BACKGROUND:In order to understand patterns of adaptation and molecular evolution it is important to quantify both variation in gene expression and nucleotide sequence divergence. Gene expression profiling in non-model organisms has recently been facilitated by the advent of massively parallel sequencing technology. Here we investigate tissue specific gene expression patterns in the zebra finch (Taeniopygia guttata) with special emphasis on the genes of the major histocompatibility complex (MHC). RESULTS:Almost 2 million 454-sequencing reads from cDNA of six different tissues were assembled and analysed. A total of 11,793 zebra finch transcripts were represented in this EST data, indicating a transcriptome coverage of about 65%. There was a positive correlation between the tissue specificity of gene expression and non-synonymous to synonymous nucleotide substitution ratio of genes, suggesting that genes with a specialised function are evolving at a higher rate (or with less constraint) than genes with a more general function. In line with this, there was also a negative correlation between overall expression levels and expression specificity of contigs. We found evidence for expression of 10 different genes related to the MHC. MHC genes showed relatively tissue specific expression levels and were in general primarily expressed in spleen. Several MHC genes, including MHC class I also showed expression in brain. Furthermore, for all genes with highest levels of expression in spleen there was an overrepresentation of several gene ontology terms related to immune function. CONCLUSIONS:Our study highlights the usefulness of next-generation sequence data for quantifying gene expression in the genome as a whole as well as in specific candidate genes. Overall, the data show predicted patterns of gene expression profiles and molecular evolution in the zebra finch genome. Expression of MHC genes in particular, corresponds well with expression patterns in other vertebrates.

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Post-transcriptional regulation of zenk expression associated with zebra finch vocal development.

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Post-transcriptional regulation of zenk expression associated with zebra finch vocal development.

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