The non-redundant functions of PIWI family proteins in gametogenesis in golden hamsters

Xiaolong Lv, Wen Xiao, Yana Lai, Zhaozhen Zhang, Hongdao Zhang, Chen Qiu, Li Hou, Qin Chen, Duanduan Wang, Yun Gao, Yuanyuan Song, Xinjia Shui, Qinghua Chen, Ruixin Qin, Shuang Liang, Wentao Zeng, Aimin Shi (), Jianmin Li () and Ligang Wu ()
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Xiaolong Lv: University of Chinese Academy of Sciences
Wen Xiao: University of Chinese Academy of Sciences
Yana Lai: Nanjing Medical University
Zhaozhen Zhang: Nanjing Medical University
Hongdao Zhang: University of Chinese Academy of Sciences
Chen Qiu: Nanjing Medical University
Li Hou: University of Chinese Academy of Sciences
Qin Chen: Nanjing Medical University
Duanduan Wang: University of Chinese Academy of Sciences
Yun Gao: Nanjing Medical University
Yuanyuan Song: University of Chinese Academy of Sciences
Xinjia Shui: University of Chinese Academy of Sciences
Qinghua Chen: Nanjing Medical University
Ruixin Qin: Nanjing Medical University
Shuang Liang: Nanjing Medical University
Wentao Zeng: Nanjing Medical University
Aimin Shi: Nanjing Medical University
Jianmin Li: Nanjing Medical University
Ligang Wu: University of Chinese Academy of Sciences

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The piRNA pathway is essential for female fertility in golden hamsters and likely humans, but not in mice. However, the role of individual PIWIs in mammalian reproduction remains poorly understood outside of mice. Here, we describe the expression profiles, subcellular localization, and knockout-associated reproductive defects for all four PIWIs in golden hamsters. In female golden hamsters, PIWIL1 and PIWIL3 are highly expressed throughout oogenesis and early embryogenesis, while knockout of PIWIL1 leads to sterility, and PIWIL3 deficiency results in subfertility with lagging zygotic development. PIWIL1 can partially compensate for TE silencing in PIWIL3 knockout females, but not vice versa. PIWIL1 and PIWIL4 are the predominant PIWIs expressed in adult and postnatal testes, respectively, while PIWIL2 is present at both stages. Loss of any PIWI expressed in testes leads to sterility and severe but distinct spermatogenesis disorders. These findings illustrate the non-redundant regulatory functions of PIWI-piRNAs in gametogenesis and early embryogenesis in golden hamsters, facilitating study of their role in human fertility.

Date: 2023
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DOI: 10.1038/s41467-023-40650-x

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