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

Author

Listed:
  • 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)

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.

Suggested Citation

  • 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 & W, 2023. "The non-redundant functions of PIWI family proteins in gametogenesis in golden hamsters," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40650-x
    DOI: 10.1038/s41467-023-40650-x
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    References listed on IDEAS

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    1. Angélique Girard & Ravi Sachidanandam & Gregory J. Hannon & Michelle A. Carmell, 2006. "A germline-specific class of small RNAs binds mammalian Piwi proteins," Nature, Nature, vol. 442(7099), pages 199-202, July.
    2. Tianxiong Yu & Kaili Fan & Deniz M. Özata & Gen Zhang & Yu Fu & William E. Theurkauf & Phillip D. Zamore & Zhiping Weng, 2021. "Long first exons and epigenetic marks distinguish conserved pachytene piRNA clusters from other mammalian genes," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Toshiaki Watanabe & Yasushi Totoki & Atsushi Toyoda & Masahiro Kaneda & Satomi Kuramochi-Miyagawa & Yayoi Obata & Hatsune Chiba & Yuji Kohara & Tomohiro Kono & Toru Nakano & M. Azim Surani & Yoshiyuki, 2008. "Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes," Nature, Nature, vol. 453(7194), pages 539-543, May.
    4. Christel Rouget & Catherine Papin & Anthony Boureux & Anne-Cécile Meunier & Bénédicte Franco & Nicolas Robine & Eric C. Lai & Alain Pelisson & Martine Simonelig, 2010. "Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo," Nature, Nature, vol. 467(7319), pages 1128-1132, October.
    5. Oliver H. Tam & Alexei A. Aravin & Paula Stein & Angelique Girard & Elizabeth P. Murchison & Sihem Cheloufi & Emily Hodges & Martin Anger & Ravi Sachidanandam & Richard M. Schultz & Gregory J. Hannon, 2008. "Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes," Nature, Nature, vol. 453(7194), pages 534-538, May.
    6. Qiyuan Yang & Ronghong Li & Qifeng Lyu & Li Hou & Zhen Liu & Qiang Sun & Miao Liu & Huijuan Shi & Beiying Xu & Mingru Yin & Zhiguang Yan & Ying Huang & Mofang Liu & Yiping Li & Ligang Wu, 2019. "Single-cell CAS-seq reveals a class of short PIWI-interacting RNAs in human oocytes," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Alexei Aravin & Dimos Gaidatzis & Sébastien Pfeffer & Mariana Lagos-Quintana & Pablo Landgraf & Nicola Iovino & Patricia Morris & Michael J. Brownstein & Satomi Kuramochi-Miyagawa & Toru Nakano & Minc, 2006. "A novel class of small RNAs bind to MILI protein in mouse testes," Nature, Nature, vol. 442(7099), pages 203-207, July.
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