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journal article·2026-07Open access

Paternal Circadian Disruption Impairs Offspring Cognition via Sperm microRNAs

Kexin Zou, Sisi Luo, Binliang Tang, Zhiqiang Liu, Yuchuan Zhou, Yicong Meng, Zhengmu Wu, Zheng Sun, Weihui Shi, Jianzhong Sheng, Chuanjin Yu, Zhenhua Li, Siyi Wei, Mo Zhang, Yujie Luo, Jing Yan, Xueyun Qin, Jiahang Mo, Chengliang Zhou, Jinsong Li, Hefeng Huang, Yifu Ding, Guolian Ding

Advanced Science· Volume 13· Issue 37
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Source abstract

Abstract

ABSTRACT A father's lifestyle can impact offspring's health. However, it is unclear whether and how paternal circadian rhythm disruption affects offspring neural development and cognitive function. Here, we show that male mice exposed to constant light (LL‐F0) led to memory dysfunction and impaired hippocampal synaptic plasticity in male, but not female, F1 offspring (LL‐F1). Paternal circadian disruption altered expression profiles of small RNAs, especially microRNAs (miRNAs), in mouse sperm. These miRNA changes were associated with chromatin accessible regions in spermatogonial stem cells, pointing to an early germline origin of the disrupted epigenetic state. In human sperm, we identified and validated upregulation of miR‐92a‐3p. Microinjection of total small RNAs from LL‐F0 sperm or synthetic miR‐92a‐3p/miR‐25‐3p into zygotes was sufficient to phenocopy offspring cognitive impairment, whereas inhibition of these miRNAs in zygotes partially reversed the phenotype. These findings support a role for sperm‐borne miRNAs in the intergenerational transmission of neurobehavioral deficits induced by paternal circadian disruption.
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Research context

OpenAlex topics: Circadian rhythm and melatonin · Sperm and Testicular Function · Stress Responses and Cortisol

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Institute of Reproduction and Development Shanghai Key Laboratory of Reproduction and Development Obstetrics and Gynecology Hospital Fudan University Shanghai China

Shanghai First Maternity and Infant Hospital Tongji University Shanghai China

Center for Rehabilitation Medicine Rehabilitation & Sports Medicine Research Institute of Zhejiang Province Department of Rehabilitation Medicine Zhejiang Provincial People's Hospital Affiliated People's Hospital Hangzhou Medical College Hangzhou Zhejiang China

Shanghai Institute of Biochemistry and Cell Biology Center for Excellence in Molecular Cell Science Chinese Academy of Sciences University of Chinese Academy of Sciences Shanghai China

The International Peace Maternity and Child Health Hospital Shanghai Jiao Tong University School of Medicine Shanghai China

Department of Medicine – Endocrinology Baylor College of Medicine Houston Texas USA

Institute of Medical Genetics and Development Key Laboratory of Reproductive Genetics (Ministry of Education) and Women's Hospital Zhejiang University School of Medicine Zhejiang China

Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases Shanghai China

Key Laboratory of Systems Health Science of Zhejiang Province School of Life Science Hangzhou Institute for Advanced Study University of Chinese Academy of Sciences Hangzhou China

Funding

National Natural Science Foundation of China

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