Stress and trauma have been reported to exert long-lasting psychological and physiological effects that persist across multiple generations. To model hypothalamic–pituitary–adrenal (HPA) axis activation under chronic stress conditions, we employed a mouse model involving corticosterone (CORT) supplementation in drinking water. Our group had previously demonstrated that Paternal CORT treatment leads to transgenerational molecular and behavioural modifications. Knowing how stress effects are being inherited is the first step towards stopping this transmission.
In the present study, we sequenced mouse sperm DNA with Oxford Nanopore Technologies (ONT) long-read sequencing to determine the impact of CORT treatment on DNA methylation. We sequenced both sperm DNA from CORT treated fathers (F0) and their male offspring (F1). This technique allowed direct characterization of the methylation (5mC) and hydroxymethylation (5hmC) status of more than 20 million CpG in the genome without bisulphite conversion.
Differentially methylated region (DMR) analysis revealed that PatCORT exposure resulted in predominately decreased 5mC levels at specific loci accompanied by localized increases in 5hmC, although the magnitude of the 5hmC changes was smaller. F1 PatCORT showed the same pattern of increased 5hmC but less bias towards demethylation. Notably, 17 DMRs were consistent between F0 and F1 sperm suggesting inheritance of PatCORT effects. There were no common differentially hydroxymethylated regions (DhMRs) to both generations. Intra-generational comparisons of DMRs and DhMRs revealed an overlap of up to 20%.
Motif enrichment analysis of overlapping DMRs identified an overrepresentation of transcription factor binding motifs implicated in embryonic development, suggesting potential functional relevance of these regions.
In summary, we have demonstrated alterations in sperm cytosine modification patterns in both F0 and F1 generations in our model of paternal chronic stress. Collectively, these findings contribute to the growing body of evidence on epigenetic inheritance and provides further insight into the mechanisms underlying the intergenerational transmission of stress effects.