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TRIM28-dependent SUMOylation protects the adult ovary from activation of the testicular pathway

Author

Listed:
  • Moïra Rossitto

    (CNRS UMR9002 University of Montpellier
    Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286)

  • Stephanie Déjardin

    (CNRS UMR9002 University of Montpellier)

  • Chris M. Rands

    (University of Geneva CMU, lab E09.2750.B 1)

  • Stephanie Gras

    (GenomEast platform, IGBMC, 1, rue Laurent Fries)

  • Roberta Migale

    (The Francis Crick Institute)

  • Mahmoud-Reza Rafiee

    (The Francis Crick Institute)

  • Yasmine Neirijnck

    (University of Geneva CMU, lab E09.2750.B 1)

  • Alain Pruvost

    (Université Paris Saclay, CEA, INRAE, Département Médicaments et Technologies pour la Santé (DMTS), SPI)

  • Anvi Laetitia Nguyen

    (Université Paris Saclay, CEA, INRAE, Département Médicaments et Technologies pour la Santé (DMTS), SPI)

  • Guillaume Bossis

    (University of Montpellier, CNRS)

  • Florence Cammas

    (Institut de Recherche en Cancérologie de Montpellier, IRCM, INSERM U1194, Université de Montpellier, Institut régional du Cancer de Montpellier)

  • Lionel Gallic

    (CNRS UMR9002 University of Montpellier)

  • Dagmar Wilhelm

    (University of Melbourne)

  • Robin Lovell-Badge

    (The Francis Crick Institute)

  • Brigitte Boizet-Bonhoure

    (CNRS UMR9002 University of Montpellier)

  • Serge Nef

    (University of Geneva CMU, lab E09.2750.B 1)

  • Francis Poulat

    (CNRS UMR9002 University of Montpellier)

Abstract

Gonadal sexual fate in mammals is determined during embryonic development and must be actively maintained in adulthood. In the mouse ovary, oestrogen receptors and FOXL2 protect ovarian granulosa cells from transdifferentiation into Sertoli cells, their testicular counterpart. However, the mechanism underlying their protective effect is unknown. Here, we show that TRIM28 is required to prevent female-to-male sex reversal of the mouse ovary after birth. We found that upon loss of Trim28, ovarian granulosa cells transdifferentiate to Sertoli cells through an intermediate cell type, different from gonadal embryonic progenitors. TRIM28 is recruited on chromatin in the proximity of FOXL2 to maintain the ovarian pathway and to repress testicular-specific genes. The role of TRIM28 in ovarian maintenance depends on its E3-SUMO ligase activity that regulates the sex-specific SUMOylation profile of ovarian-specific genes. Our study identifies TRIM28 as a key factor in protecting the adult ovary from the testicular pathway.

Suggested Citation

  • Moïra Rossitto & Stephanie Déjardin & Chris M. Rands & Stephanie Gras & Roberta Migale & Mahmoud-Reza Rafiee & Yasmine Neirijnck & Alain Pruvost & Anvi Laetitia Nguyen & Guillaume Bossis & Florence Ca, 2022. "TRIM28-dependent SUMOylation protects the adult ovary from activation of the testicular pathway," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32061-1
    DOI: 10.1038/s41467-022-32061-1
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    1. X. Fan & M. Bialecka & I. Moustakas & E. Lam & V. Torrens-Juaneda & N. V. Borggreven & L. Trouw & L. A. Louwe & G. S. K. Pilgram & H. Mei & L. Westerlaken & S. M. Chuva de Sousa Lopes, 2019. "Single-cell reconstruction of follicular remodeling in the human adult ovary," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Fu-Ping Zhang & Marjo Malinen & Arfa Mehmood & Tiina Lehtiniemi & Tiina Jääskeläinen & Einari A. Niskanen & Hanna Korhonen & Asta Laiho & Laura L. Elo & Claes Ohlsson & Noora Kotaja & Matti Poutanen &, 2019. "Lack of androgen receptor SUMOylation results in male infertility due to epididymal dysfunction," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Barbara Nicol & Sara A. Grimm & Frédéric Chalmel & Estelle Lecluze & Maëlle Pannetier & Eric Pailhoux & Elodie Dupin-De-Beyssat & Yann Guiguen & Blanche Capel & Humphrey H.-C. Yao, 2019. "RUNX1 maintains the identity of the fetal ovary through an interplay with FOXL2," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Clinton K. Matson & Mark W. Murphy & Aaron L. Sarver & Michael D. Griswold & Vivian J. Bardwell & David Zarkower, 2011. "Erratum: DMRT1 prevents female reprogramming in the postnatal mammalian testis," Nature, Nature, vol. 477(7363), pages 238-238, September.
    5. Magdalena Wagner & Masahito Yoshihara & Iyadh Douagi & Anastasios Damdimopoulos & Sarita Panula & Sophie Petropoulos & Haojiang Lu & Karin Pettersson & Kerstin Palm & Shintaro Katayama & Outi Hovatta , 2020. "Single-cell analysis of human ovarian cortex identifies distinct cell populations but no oogonial stem cells," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    6. Christina Ernst & Nils Eling & Celia P. Martinez-Jimenez & John C. Marioni & Duncan T. Odom, 2019. "Staged developmental mapping and X chromosome transcriptional dynamics during mouse spermatogenesis," Nature Communications, Nature, vol. 10(1), pages 1-20, December.
    7. Clinton K. Matson & Mark W. Murphy & Aaron L. Sarver & Michael D. Griswold & Vivian J. Bardwell & David Zarkower, 2011. "DMRT1 prevents female reprogramming in the postnatal mammalian testis," Nature, Nature, vol. 476(7358), pages 101-104, August.
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    1. Damien Dufour & Typhanie Dumontet & Isabelle Sahut-Barnola & Aude Carusi & Méline Onzon & Eric Pussard & James Jr Wilmouth & Julie Olabe & Cécily Lucas & Adrien Levasseur & Christelle Damon-Soubeyrand, 2022. "Loss of SUMO-specific protease 2 causes isolated glucocorticoid deficiency by blocking adrenal cortex zonal transdifferentiation in mice," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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