Transcriptome analysis of meiotic and post-meiotic spermatogenic cells reveals the potential hub genes of aging on the decline of male fertility

Yiqian Gui; Xixiang Ma; Mengneng Xiong; Yujiao Wen; Congcong Cao; Liang Zhang; Xiaoli Wang; Chunyan Liu; Huiping Zhang; Xunbin Huang; Chengliang Xiong; Feng Pan; Shuiqiao Yuan

doi:10.1016/j.gene.2023.147883

Transcriptome analysis of meiotic and post-meiotic spermatogenic cells reveals the potential hub genes of aging on the decline of male fertility

Gene. 2024 Jan 30:893:147883. doi: 10.1016/j.gene.2023.147883. Epub 2023 Oct 13.

Authors

Yiqian Gui¹, Xixiang Ma², Mengneng Xiong¹, Yujiao Wen¹, Congcong Cao¹, Liang Zhang³, Xiaoli Wang¹, Chunyan Liu¹, Huiping Zhang¹, Xunbin Huang⁴, Chengliang Xiong⁵, Feng Pan⁶, Shuiqiao Yuan⁷

Affiliations

¹ Institute of Reproductive Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China.
² Institute of Reproductive Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China; Laboratory Animal Center, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China.
³ Department of Medical Genetics, China Medical University, Shenyang, Liaoning 110122, China.
⁴ Institute of Reproductive Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China; Wuhan Tongji Reproductive Hospital, Wuhan, Hubei 430013, China.
⁵ Wuhan Tongji Reproductive Hospital, Wuhan, Hubei 430013, China.
⁶ Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, China.
⁷ Institute of Reproductive Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China; Laboratory Animal Center, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China. Electronic address: shuiqiaoyuan@hust.edu.cn.

PMID: 37839768
DOI: 10.1016/j.gene.2023.147883

Abstract

Genetic and epigenetic changes in sperm caused by male aging may be essential factors affecting semen parameters, but the effects and specific molecular mechanisms of aging on male reproduction have not been fully clarified. In this study, to explore the effect of aging on male fertility and seek the potential molecular etiology, we performed high-throughput RNA-sequencing in isolated spermatogenic cells, including pachytene spermatocytes (marked by the completion of chromosome synapsis) and round spermatids (produced by the separation of sister chromatids) from the elderly and the young men. Functional enrichment analysis of differentially expressed genes (DEGs) in round spermatids between the elderly and young showed that they were significantly enriched in gamete generation, spindle assembly, and cilium movement involved in cell motility. In addition, the expression levels of DEGs in round spermatids (post-meiotic cells) were found to be more susceptible to age. Furthermore, ten genes (AURKA, CCNB1, CDC20, CCNB2, KIF2C, KIAA0101, NR5A1, PLK1, PTTG1, RAD51AP1) were identified to be the hub genes involved in the regulation of sperm quality in the elderly through Protein-Protein Interaction (PPI) network construction and measuring semantic among GO terms and gene products. Our data provide aging-related molecular alterations in meiotic and post-meiotic spermatogenic cells, and the information gained from this study may explain the abnormal aging-related male fertility decline.

Keywords: Hub genes; Male fertility; Pachytene spermatocytes; Round spermatid; Transcriptome analysis.

MeSH terms

Aged
Fertility / genetics
Gene Expression Profiling
Humans
Male
Semen*
Spermatids* / metabolism
Spermatogenesis / genetics
Spermatozoa / metabolism