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TENT5-mediated polyadenylation of mRNAs encoding secreted proteins is essential for gametogenesis in mice

Author

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  • Michał Brouze

    (International Institute of Molecular and Cell Biology
    Polish Academy of Sciences)

  • Agnieszka Czarnocka-Cieciura

    (International Institute of Molecular and Cell Biology)

  • Olga Gewartowska

    (International Institute of Molecular and Cell Biology
    International Institute of Molecular and Cell Biology
    University of Warsaw)

  • Monika Kusio-Kobiałka

    (International Institute of Molecular and Cell Biology)

  • Kamil Jachacy

    (International Institute of Molecular and Cell Biology
    University of Warsaw)

  • Marcin Szpila

    (International Institute of Molecular and Cell Biology
    University of Warsaw)

  • Bartosz Tarkowski

    (International Institute of Molecular and Cell Biology
    Polish Academy of Sciences)

  • Jakub Gruchota

    (International Institute of Molecular and Cell Biology
    Polish Academy of Sciences)

  • Paweł Krawczyk

    (International Institute of Molecular and Cell Biology
    Polish Academy of Sciences)

  • Seweryn Mroczek

    (International Institute of Molecular and Cell Biology
    University of Warsaw)

  • Ewa Borsuk

    (International Institute of Molecular and Cell Biology
    University of Warsaw)

  • Andrzej Dziembowski

    (International Institute of Molecular and Cell Biology
    Polish Academy of Sciences
    University of Warsaw
    University of Warsaw)

Abstract

Cytoplasmic polyadenylation plays a vital role in gametogenesis; however, the participating enzymes and substrates in mammals remain unclear. Using knockout and knock-in mouse models, we describe the essential role of four TENT5 poly(A) polymerases in mouse fertility and gametogenesis. TENT5B and TENT5C play crucial yet redundant roles in oogenesis, with the double knockout of both genes leading to oocyte degeneration. Additionally, TENT5B-GFP knock-in females display a gain-of-function infertility effect, with multiple chromosomal aberrations in ovulated oocytes. TENT5C and TENT5D both regulate different stages of spermatogenesis, as shown by the sterility in males following the knockout of either gene. Finally, Tent5a knockout substantially lowers fertility, although the underlying mechanism is not directly related to gametogenesis. Through direct RNA sequencing, we discovered that TENT5s polyadenylate mRNAs encoding endoplasmic reticulum-targeted proteins essential for gametogenesis. Sequence motif analysis and reporter mRNA assays reveal that the presence of an endoplasmic reticulum-leader sequence represents the primary determinant of TENT5-mediated regulation.

Suggested Citation

  • Michał Brouze & Agnieszka Czarnocka-Cieciura & Olga Gewartowska & Monika Kusio-Kobiałka & Kamil Jachacy & Marcin Szpila & Bartosz Tarkowski & Jakub Gruchota & Paweł Krawczyk & Seweryn Mroczek & Ewa Bo, 2024. "TENT5-mediated polyadenylation of mRNAs encoding secreted proteins is essential for gametogenesis in mice," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49479-4
    DOI: 10.1038/s41467-024-49479-4
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    References listed on IDEAS

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    1. Seweryn Mroczek & Justyna Chlebowska & Tomasz M. Kuliński & Olga Gewartowska & Jakub Gruchota & Dominik Cysewski & Vladyslava Liudkovska & Ewa Borsuk & Dominika Nowis & Andrzej Dziembowski, 2017. "The non-canonical poly(A) polymerase FAM46C acts as an onco-suppressor in multiple myeloma," Nature Communications, Nature, vol. 8(1), pages 1-17, December.
    2. Liaoteng Wang & Christian R. Eckmann & Lisa C. Kadyk & Marvin Wickens & Judith Kimble, 2002. "A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans," Nature, Nature, vol. 419(6904), pages 312-316, September.
    3. Matthias Kettwig & Katharina Ternka & Kristin Wendland & Dennis Manfred Krüger & Silvia Zampar & Charlotte Schob & Jonas Franz & Abhishek Aich & Anne Winkler & M. Sadman Sakib & Lalit Kaurani & Robert, 2021. "Interferon-driven brain phenotype in a mouse model of RNaseT2 deficient leukoencephalopathy," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
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