Single-cell transcriptome and translatome dual-omics reveals potential mechanisms of human oocyte maturation

Nat Commun. 2022 Aug 30;13(1):5114. doi: 10.1038/s41467-022-32791-2.

Wenqi Hu ^# ¹, Haitao Zeng ^# ², Yanan Shi ², Chuanchuan Zhou ², Jiana Huang ², Lei Jia ², Siqi Xu ¹, Xiaoyu Feng ¹, Yanyan Zeng ², Tuanlin Xiong ³, Wenze Huang ³, Peng Sun ², Yajie Chang ², Tingting Li ², Cong Fang ², Keliang Wu ⁴, Lingbo Cai ⁵, Wuhua Ni ⁶, Yan Li ⁶, Zhiyong Yang ⁷, Qiangfeng Cliff Zhang ³, RiCheng Chian ⁷, Zijiang Chen ⁴, Xiaoyan Liang ⁸, Kehkooi Kee ⁹

Affiliations

1 Center for Stem Cell Biology and Regenerative Medicine, Department of Basic Medical Sciences, School of Medicine, Tsinghua University, 100084, Beijing, China.
2 Reproductive Medicine Research Center, The Sixth Affiliated Hospital of Sun Yat-sen University, 510655, Guangzhou, China.
3 MOE Key Laboratory of Bioinformatics, Beijing Advanced Innovation Center for Structural Biology and Frontier Research Center for Biological Structure, Center for Synthetic and Systems Biology, School of Life Sciences, Tsinghua University, 100084, Beijing, China.
4 Center for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, 250012, Jinan, Shandong, China.
5 State Key Laboratory of Reproductive Medicine, Center of Clinical Reproductive Medicine, First Affiliated Hospital, Nanjing Medical University, 210029, Nanjing, China.
6 Reproductive Medicine Center, The First Affiliated Hospital of Wenzhou Medical University, 325000, Wenzhou, Zhejiang Province, China.
7 Center for Reproductive Medicine, Shanghai Tenth People's Hospital of Tongji University, 200072, Shanghai, China.
8 Reproductive Medicine Research Center, The Sixth Affiliated Hospital of Sun Yat-sen University, 510655, Guangzhou, China. liangxy2@mail.sysu.edu.cn.
9 Center for Stem Cell Biology and Regenerative Medicine, Department of Basic Medical Sciences, School of Medicine, Tsinghua University, 100084, Beijing, China. kkee@tsinghua.edu.cn.
# Contributed equally.

PMID: 36042231 DOI: 10.1038/s41467-022-32791-2

Abstract

The combined use of transcriptome and translatome as indicators of gene expression profiles is usually more accurate than the use of transcriptomes alone, especially in cell types governed by translational regulation, such as mammalian oocytes. Here, we developed a dual-omics methodology that includes both transcriptome and translatome Sequencing (T&T-seq) of single-cell oocyte samples, and we used it to characterize the transcriptomes and translatomes during mouse and human oocyte maturation. T&T-seq analysis revealed distinct translational expression patterns between mouse and human oocytes and delineated a sequential gene expression regulation from the cytoplasm to the nucleus during human oocyte maturation. By these means, we also identified a functional role of OOSP2 inducing factor in human oocyte maturation, as human recombinant OOSP2 induced in vitro maturation of human oocytes, which was blocked by anti-OOSP2. Single-oocyte T&T-seq analyses further elucidated that OOSP2 induces specific signaling pathways, including small GTPases, through translational regulation.

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