Transcription and DNA methylation signatures of paternal behavior in hippocampal dentate gyrus of prairie voles.

Transcription and DNA methylation signatures of paternal behavior in hippocampal dentate gyrus of prairie voles.
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DOI:
10.1038/s41598-023-37521-2
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发表时间:
2023-07-07
期刊:
影响因子:
4.6
通讯作者:
Feng, Jian
Feng, Jian
中科院分区:
综合性期刊3区
文献类型:
--
作者:
Waddell, Nicholas J. J.;Liu, Yan;Chitaman, Javed M. M.;Kaplan, Graham J. J.;Wang, Zuoxin;Feng, Jian

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在社会性一夫一妻制的草原田鼠(Microtus ochrogaster)中,亲职行为不仅发生在母亲和父亲身上,而且也存在于一些未交配的雄性中。与此相反,其他处女男性表现出攻击性的行为对同种幼崽。然而,人们对这种行为二分法的分子基础知之甚少,例如基因表达变化及其调控机制。为了解决这个问题,我们分析了四个草原田鼠组,即攻击处女男性,父母处女男性,父亲和母亲的海马齿状回的转录组和DNA甲基化。虽然我们发现父母之间的处女男性和父亲的一致的基因表达模式,攻击处女男性有一个更偏离的转录组。此外,在四组之间的成对比较中发现了许多DNA甲基化变化。我们发现一些DNA甲基化的变化与转录差异重叠,跨越基因体和启动子区域。此外,基因表达变化和甲基化组改变选择性地富集在某些生物学途径中,例如Wnt信号传导,这表明DNA甲基化在父系行为中的典型转录调节作用。因此,我们的研究提出了草原田鼠齿状回转录组和表观基因组的综合观点,提供了一个基于DNA表观遗传的父系行为的分子见解。
In socially monogamous prairie voles (Microtus ochrogaster), parental behaviors not only occur in mothers and fathers, but also exist in some virgin males. In contrast, the other virgin males display aggressive behaviors towards conspecific pups. However, little is known about the molecular underpinnings of this behavioral dichotomy, such as gene expression changes and their regulatory mechanisms. To address this, we profiled the transcriptome and DNA methylome of hippocampal dentate gyrus of four prairie vole groups, namely attacker virgin males, parental virgin males, fathers, and mothers. While we found a concordant gene expression pattern between parental virgin males and fathers, the attacker virgin males have a more deviated transcriptome. Moreover, numerous DNA methylation changes were found in pair-wise comparisons among the four groups. We found some DNA methylation changes overlapping with transcription differences, across gene-bodies and promoter regions. Furthermore, the gene expression changes and methylome alterations are selectively enriched in certain biological pathways, such as Wnt signaling, which suggest a canonical transcription regulatory role of DNA methylation in paternal behavior. Therefore, our study presents an integrated view of prairie vole dentate gyrus transcriptome and epigenome that provides a DNA epigenetic based molecular insight of paternal behavior.
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