Becoming monogamous quickly: Adaptive evolution of a pallidal enhancer at the prairie vole Avpr1a locus
Ontology highlight
ABSTRACT:
ORGANISM(S): Microtus ochrogaster
PROVIDER: GSE85826 | GEO | 2018/01/31
REPOSITORIES: GEO
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Project description:An Infinium microarray platform (GPL28271, HorvathMammalMethylChip40) was used to generate DNA methylation data from several tissues from prairie voles (Microtus ochrogaster). Ear, liver, and brain samples from the Cornell University prairie vole colony were collected from 48 male and female prairie voles at various life stages: neonatal (<1 month old), sub-adult (2-4 months old), mature adult (4-10 months old), and middle aged/old adult (>10 months old). The pair bonded male and female prairie voles used in our study cohabitated with their partners for several months and produced at least three generations of litters. Animals were euthanized via rapid decapitation, their tissues rapidly extracted and frozen on dry ice before being stored at -80C until further processing for genomic DNA extraction. Brains were coronally sectioned and brain regions from the pair bonding circuit (PBC) were micro-dissected and pooled for each animal. The PBC brain regions included the prefrontal cortex, nucleus accumbens, lateral septum, ventral pallidum, and medial amygdala, and ventral tegmental area. Genomic DNA was isolated and purified using the phenol-chloroform extraction and ethanol precipitation method. A total of 144 tissue samples were collected and processed for DNA methylation analysis. Tissues: Brain, Ear, Liver
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Project description:Background: The ability to form enduring social bonds is characteristic of human nature and as a result, impairments in social affiliation are central features of severe neuropsychiatric disorders including autism spectrum disorders and schizophrenia. Due to its ability to form long-term pair-bonds, the socially monogamous prairie vole (Microtus ochrogaster) has emerged as an excellent model to study the neurobiology of social attachment. Despite the enduring nature of the bond, however, surprisingly few genes have been implicated in the pair-bonding process in either sex. Results: Using RNA-sequencing, we aimed at identifying the transcriptomic regulations in the nucleus accumbens (NAc) underlying the formation and maintenance of a pair-bond in male and female prairie voles and found sex-specific response patterns despite similar behavioral indicators of pair-bond establishment. Indeed, 24 hrs of cohabitation with an opposite-sex partner induced widespread transcriptomic changes that remained sustained to some extent in females after 3 weeks, but returned to baseline before a second set of regulations in males. This led to a highly sexually-biased NAc transcriptome in the later phase of the bond related to processes such as neurotransmission, protein turnover, and DNA transcription. In particular, we found sex-specific alterations of mitochondrial dynamics following cohabitation, with a shift towards fission in males. Conclusions: In addition to identifying the genes, networks, and pathways involved in the pair-bonding process in the NAc, our work illustrates the vast extent of sex differences in the molecular mechanisms underlying pair-bonding in prairie voles, and paves the way to further our understanding of the complex social bonding process.
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Project description:This dataset contains RNA sequencing results from adult male prairie voles that were in either opposite-sex or same-sex pairs that were subsequently either separated from or remained paired with their partner for either 48 hours or 4 weeks prior to collecting nucleus accumbens tissue. The goal of this experiment was to determine the nucleus accumbens transcriptional response specific to separation from an opposite-sex partner. RNA sequencing was done on polyA enriched transcripts using Illumina single-end sequencing. Samples from 3 groups were from a Ribo-seq protocol using a virally delievered, vole optimized Translating Ribosome Affinity Purification construct (Heiman et al., 2008). These samples contain files for both the input fraction and the pulldown fraction (denoted with a _P suffix).
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Project description:We use ChIP-seq targeting histone 3 lysine 4 mono-methylation (H3K4me1) to identify putative enhancer sites genome-wide, in the retrosplenial cortex of adult prairie vole males. ChIP samples were generated by targeting a known enhancer mark (H3K4me1) in chromatin extracted from the retrosplenial cortex of 8 males. Illumina libraries were prepared from ChIP and INPUT DNA and sequenced on Illimuna HiSeq 2500 platform.
2015-12-11 | E-GEOD-73670 | biostudies-arrayexpress
Project description:We use ChIP-seq targeting histone 3 lysine 4 mono-methylation (H3K4me1) to identify putative enhancer sites genome-wide, in the retrosplenial cortex of adult prairie vole males.
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Project description:In socially monogamous prairie voles (Microtus ochrogaster), parental behaviors not only occur in mothers and fathers, but also can exist in virgin males. However, some virgin males display aggressive behaviors towards conspecific pups. Although this behavioral dichotomy in response to pup exposure has been well documented in male virgin voles, little is known about the gene expression changes underlie the parental behavioral differences and their regulatory mechanisms. To address this, we profiled the transcriptome and DNA methylome of hippocampal dentate gyrus of four prairie vole groups, attacker virgin males, parental virgin males, fathers, and mothers. We found a concordant pattern of gene transcription in parental virgin males and fathers, when comparing to the attacker group. The methylome analysis also revealed pathways with genes enriched for epigenetic changes involving both receptor-mediated and secondary messenger signaling across both behavioral phenotypes and sexual experiences. Furthermore, we found correlations between gene expression changes and DNA methylation differences between attacker and parental virgin males, which suggests a canonical gene expression regulatory role of DNA methylation in paternal care. Therefore, our study presents an integrated view of transcriptome and epigenome that provides a DNA epigenetic based molecular insight of paternal behavior.
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Project description:In socially monogamous prairie voles (Microtus ochrogaster), parental behaviors not only occur in mothers and fathers, but also can exist in virgin males. However, some virgin males display aggressive behaviors towards conspecific pups. Although this behavioral dichotomy in response to pup exposure has been well documented in male virgin voles, little is known about the gene expression changes underlie the parental behavioral differences and their regulatory mechanisms. To address this, we profiled the transcriptome and DNA methylome of hippocampal dentate gyrus of four prairie vole groups, attacker virgin males, parental virgin males, fathers, and mothers. We found a concordant pattern of gene transcription in parental virgin males and fathers, when comparing to the attacker group. The methylome analysis also revealed pathways with genes enriched for epigenetic changes involving both receptor-mediated and secondary messenger signaling across both behavioral phenotypes and sexual experiences. Furthermore, we found correlations between gene expression changes and DNA methylation differences between attacker and parental virgin males, which suggests a canonical gene expression regulatory role of DNA methylation in paternal care. Therefore, our study presents an integrated view of transcriptome and epigenome that provides a DNA epigenetic based molecular insight of paternal behavior.
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Project description:The importance of fathers' engagement in care and its critical role in the offspring’s cognitive and emotional development is now well established. Yet, little is known on the underlying neurobiology due to the lack of appropriate animal models. In the socially monogamous and bi-parental prairie vole (Microtus ochrogaster), while most virgin males show spontaneous paternal behaviors (Paternal), others display pup-directed aggression (Attackers). Here we took advantage of this phenotypic dichotomy and used RNA-sequencing in three important brain areas to characterize gene expression associated with paternal behaviors of Paternal males and compare it to experienced fathers and mothers. This strategy allowed the identification of spontaneous paternal behaviors independently from fatherhood and pair-bonding. While Paternal males displayed the same range and extent of paternal behaviors than experienced Fathers, the nucleus accumbens (NAc) and medial preoptic area (MPOA) transcriptomes mainly reflected pair-bonded status or sex differences, respectively. The lateral septum (LS) transcriptome, however, primarily reflected phenotypic differences between Paternal and Attackers and suggested the involvement of the mitochondria, RNA translation, and protein degradation processes. Altogether, these observations highlight a marked structure- and phenotype-specific pattern of gene expression underlying paternal behaviors in prairie voles and highlight similarities and differences from those underlying fatherhood.
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Project description:Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early parental care on social behavior development in prairie voles. We find widespread male specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens.
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