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Background  The neuropeptide oxytocin regulates mammalian social behavior. Disruptions in oxytocin signaling are a feature of many psychopathologies. One commonly studied biomarker for oxytocin involvement in psychiatric diseases is DNA methylation at the oxytocin receptor gene ( OXTR ). Such studies focus on DNA methylation in two regions of  OXTR , exon 3 and a region termed MT2 which overlaps exon 1 and intron 1. However, the relative contribution of exon 3 and MT2 in regulating  OXTR  gene expression in the brain is currently unknown.    Results  Here, we use the prairie vole as a translational animal model to investigate genetic, epigenetic, and environmental factors affecting  Oxtr  gene expression in a region of the brain that has been shown to drive  Oxtr  related behavior in the vole, the nucleus accumbens. We show that the genetic structure of  Oxtr  in prairie voles resembles human  OXTR . We then studied the effects of early life experience on DNA methylation in two regions of a CpG island surrounding the  Oxtr  promoter: MT2 and exon 3. We show that early nurture in the form of parental care results in DNA hypomethylation of  Oxtr  in both MT2 and exon 3, but only DNA methylation in MT2 is associated with  Oxtr  gene expression. Network analyses indicate that CpG sites in the 3′ portion of MT2 are most highly associated with  Oxtr  gene expression. We also identify two novel SNPs in exon 3 of  Oxtr  in prairie voles and a novel alternative transcript originating from the third intron of the gene. Expression of the novel alternative transcript is associated with genotype at SNP KLW2.    Conclusions  These results identify putative regulatory features of  Oxtr  in prairie voles which inform future studies examining  OXTR  in human social behaviors and disorders. These studies indicate that in prairie voles, DNA methylation in MT2, particularly in the 3′ portion, is more predictive of  Oxtr  gene expression than DNA methylation in exon 3. Similarly, in human temporal cortex, we find that DNA methylation in the 3′ portion of MT2 is associated with  OXTR  expression. Together, these results suggest that among the CpG sites studied, DNA methylation of MT2 may be the most reliable indicator of  OXTR  gene expression. We also identify novel features of prairie vole  Oxtr , including SNPs and an alternative transcript, which further develop the prairie vole as a translational model for studies of  OXTR .

Genetic, epigenetic, and environmental factors controlling oxytocin receptor gene expression