The piRNA pathway is essential for generating functional oocytes in golden hamsters

• Published in: Nature cell biology Vol. 23; no. 9; pp. 1013 - 1022
• Main Authors: Zhang, Hongdao, Zhang, Fengjuan, Chen, Qinghua, Li, Mingzhe, Lv, Xiaolong, Xiao, Yali, Zhang, Zhaozhen, Hou, Li, Lai, Yana, Zhang, Ying, Zhang, Aihua, Gao, Shiqi, Fu, Heling, Xiao, Wen, Zhou, Jianli, Diao, Feiyang, Shi, Aimin, Su, You-Qiang, Zeng, Wentao, Wu, Ligang, Li, Jianmin
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.09.2021; Nature Publishing Group
• Subjects: 13/1; 13/51; 14/32; 14/34; 38/77; 38/90; 38/91; 631/136/2434/1706; 631/136/2434/1822; 631/337/384/2054; Analysis; Animal models in research; Biomedical and Life Sciences; Cancer Research; Cell Biology; Developmental Biology; Embryogenesis; Embryonic growth stage; Embryos; Endogenous retroviruses; Fertility; Gametocytes; Gametogenesis; Genetic aspects; Genomes; Germ cells; Hamsters; Infertility; Life Sciences; Mammals; Oocytes; Oogenesis; Perturbation; RNA; Spermatogenesis; Stem Cells; Transcriptomics; Transposons; China
• ISSN: 1465-7392; 1476-4679
• DOI: 10.1038/s41556-021-00750-6

Piwi-interacting RNAs (piRNAs) are predominantly expressed in germ cells and function in gametogenesis in various species. However, Piwi -deficient female mice are fertile and mouse oocytes express a panel of small RNAs that do not appear to be widely representative of mammals. Thus, the function of piRNAs in mammalian oogenesis remains largely unclear. Here, we generated Piwil1 - and Mov10l1 -deficient golden hamsters and found that all female and male mutants were sterile, with severe defects in embryogenesis and spermatogenesis, respectively. In Piwil1 -deficient female hamsters, the oocytes and embryos displayed aberrant transposon accumulation and extensive transcriptomic dysregulation, and the embryos were arrested at the two-cell stage with impaired zygotic genome activation. Moreover, PIWIL1-piRNAs exert a non-redundant function in silencing endogenous retroviruses in the oocytes and embryos. Together, our findings demonstrate that piRNAs are indispensable for generating functional germ cells in golden hamsters and show the value of this model species for piRNA studies in gametogenesis, especially those related to female infertility. A set of three papers reports that the piRNA pathway is essential for mammalian female fertility based on genetic perturbation experiments performed in golden hamsters.