Survey of gene, lncRNA and transposon transcription patterns in four mouse organs highlights shared and organ-specific sex-biased regulation

Qinwei Kim-Wee Zhuang, Klara Bauermeister, Jose Hector Galvez Lopez, Najla AlOgayil, Enkhjin Batdorj, Fernando Pardo-Manuel de Villena, Teruko Taketo, Guillaume Bourque, Anna K Naumova
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Abstract

Background. Sex-biased gene regulation is the basis of sexual dimorphism in phenotypes and has been studied across different cell types and different developmental stages. However, sex-biased expression of transposable elements (TEs) that represent nearly half of the mammalian genome and have the potential of influencing genome integrity and regulation, remains underexplored. Results. Here, we report a survey of gene, lncRNA and TE expression in four organs from mice with different combinations of gonadal and genetic sex. Data show remarkable variability among organs with respect to the impact of gonadal sex on transcription with the strongest effects observed in liver. In contrast, the X-chromosome dosage alone had modest influence on sex-biased transcription across different organs, albeit interaction between X-dosage and gonadal sex cannot be ruled out. The presence of the Y chromosome influenced TE, but not gene or lncRNA expression in liver. Notably, 90% of sex-biased TEs (sDETEs) reside in clusters. Moreover, 54% of these clusters overlap or reside close (<100 kb) to sex-biased genes or lncRNAs, share the same sex bias, and also have higher expression levels than sDETE clusters that do not co-localize with other types of sex-biased transcripts. We also tested the heterochromatic sink hypothesis that predicts higher expression of TEs in XX individuals and found no evidence to support it. Conclusions. Our data show that sex-biased expression of TEs varies among organs with highest numbers of sDETEs found in liver following the trends observed for genes and lncRNAs. It is enhanced by proximity to other types of sex-biased transcripts.
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对小鼠四个器官中基因、lncRNA 和转座子转录模式的调查凸显了共同的和器官特异性的性别差异调控
背景。有性别偏向的基因调控是表型中性双态性的基础,已在不同细胞类型和不同发育阶段进行了研究。然而,对于占哺乳动物基因组近一半并有可能影响基因组完整性和调控的转座元件(TEs)的性别偏向表达,研究仍然不足。研究结果在此,我们报告了对具有不同性腺和遗传性别组合的小鼠四个器官中基因、lncRNA 和 TE 表达的调查。数据显示,在性腺性别对转录的影响方面,不同器官之间存在明显差异,肝脏的影响最大。相比之下,尽管不能排除 X 染色体剂量与性腺性别之间的相互作用,但单独的 X 染色体剂量对不同器官的性别偏向转录影响不大。Y染色体的存在会影响TE,但不会影响肝脏中基因或lncRNA的表达。值得注意的是,90%的性别偏向TEs(sDETEs)存在于基因簇中。此外,这些集群中有54%与性别偏倚基因或lncRNA重叠或邻近(100 kb),具有相同的性别偏倚,其表达水平也高于不与其他类型性别偏倚转录本共定位的sDETE集群。我们还测试了异染色质汇假说,该假说预测 TEs 在 XX 个体中的表达量较高,但没有发现支持该假说的证据。我们的数据显示,TEs的性别偏向表达在不同器官之间存在差异,肝脏中的sDETEs数量最多,这与基因和lncRNAs的趋势一致。与其他类型的性别偏向转录本接近会增强这种表达。
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