Rare damaging variants in the sex differences of congenital heart disease: an exome sequencing studyResearch in context

Summary: Background: Congenital heart disease (CHD) exhibits a marked male predominance in birth prevalence, yet the genetic mechanisms underlying this sex disparity remain poorly understood. This study investigates the contribution of rare damaging variants on autosomes and the X chromosome to sex...

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Main Authors: Hairui Sun, Xiaoyan Hao, Hankui Liu, Siyao Zhang, Jiancheng Han, Ye Zhang, Tingting Liu, Xian Yang, Hairui Wang, Jiaqi Fan, Yuxuan Guan, Ni Peng, Jiaoyang Xie, Hongmei Xia, Xueqin Ji, Yan Xu, Jianguo Zhang, Jianbin Wang, Feng Lan, Hongjia Zhang, Xiaoyan Gu, Yihua He
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S235239642500180X
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Summary:Summary: Background: Congenital heart disease (CHD) exhibits a marked male predominance in birth prevalence, yet the genetic mechanisms underlying this sex disparity remain poorly understood. This study investigates the contribution of rare damaging variants on autosomes and the X chromosome to sex differences in foetal CHD. Methods: Parents of foetuses with CHD were recruited for the study. Rare damaging variants were identified by analysing whole-exome sequencing data from foetus-parental trios, and their contributions to sex differences were estimated through case–control studies. Functional enrichment analysis was conducted to assess functional differences in genetic variants between sexes. Findings: 820 foetal probands with CHD were recruited, including 487 males and 333 females. We identified a significant enrichment of X-linked rare damaging variants, primarily driven by maternally inherited hemizygous variants (MIHVs) in male probands (OR = 1·84, P < 0·05), which accounted for 7·2% of male cases in our cohort. These variants were not found to be enriched in female probands. Additionally, X-linked rare damaging de novo variants (DNVs) were not enriched in either male or female probands (female probands: 1·8% versus female controls: 0·7%, P = 0·6789; no DNVs observed in males). Gene-level variant burden analysis revealed three X-linked CHD candidate genes: DCX, CACNA1F, and MAP3K15. Autosomal rare variants did not show significant differences in variant burdens between sexes. Notably, male probands showed specific functional enrichments in cilia-related pathways for autosomal recessive variants, as well as in chromatin remodelling and nervous system development pathways for autosomal DNVs. Interpretation: Male and female foetal CHD have significantly different genetic landscapes. The enrichment of X-linked rare damaging MIHVs in males provides a genetic explanation for the higher prevalence of CHD in males. This finding highlights the importance of incorporating sex-stratified approaches in clinical diagnostics and research. Funding: Natural Science Foundation of China and Key research and development project of Hebei Province.
ISSN:2352-3964