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

Michał Brouze, Agnieszka Czarnocka-Cieciura, Olga Gewartowska, Monika Kusio-Kobiałka, Kamil Jachacy, Marcin Szpila, Bartosz Tarkowski, Jakub Gruchota, Paweł Krawczyk, Seweryn Mroczek, Ewa Borsuk and Andrzej Dziembowski ()
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Michał Brouze: International Institute of Molecular and Cell Biology
Agnieszka Czarnocka-Cieciura: International Institute of Molecular and Cell Biology
Olga Gewartowska: International Institute of Molecular and Cell Biology
Monika Kusio-Kobiałka: International Institute of Molecular and Cell Biology
Kamil Jachacy: International Institute of Molecular and Cell Biology
Marcin Szpila: International Institute of Molecular and Cell Biology
Bartosz Tarkowski: International Institute of Molecular and Cell Biology
Jakub Gruchota: International Institute of Molecular and Cell Biology
Paweł Krawczyk: International Institute of Molecular and Cell Biology
Seweryn Mroczek: International Institute of Molecular and Cell Biology
Ewa Borsuk: International Institute of Molecular and Cell Biology
Andrzej Dziembowski: International Institute of Molecular and Cell Biology

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-49479-4

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