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Somatic cell fate maintenance in mouse fetal testes via autocrine/paracrine action of AMH and activin B

Author

Listed:
  • Karina F. Rodriguez

    (National Institute of Environmental Health Sciences)

  • Paula R. Brown

    (National Institute of Environmental Health Sciences)

  • Ciro M. Amato

    (National Institute of Environmental Health Sciences)

  • Barbara Nicol

    (National Institute of Environmental Health Sciences)

  • Chia-Feng Liu

    (Cleveland Clinic)

  • Xin Xu

    (National Institute of Environmental Health Sciences)

  • Humphrey Hung-Chang Yao

    (National Institute of Environmental Health Sciences)

Abstract

Fate determination and maintenance of fetal testes in most mammals occur cell autonomously as a result of the action of key transcription factors in Sertoli cells. However, the cases of freemartin, where an XX twin develops testis structures under the influence of an XY twin, imply that hormonal factor(s) from the XY embryo contribute to sex reversal of the XX twin. Here we show that in mouse XY embryos, Sertoli cell-derived anti-Mullerian hormone (AMH) and activin B together maintain Sertoli cell identity. Sertoli cells in the gonadal poles of XY embryos lacking both AMH and activin B transdifferentiate into their female counterpart granulosa cells, leading to ovotestis formation. The ovotestes remain to adulthood and produce both sperm and oocytes, although there are few of the former and the latter fail to mature. Finally, the ability of XY mice to masculinize ovaries is lost in the absence of these two factors. These results provide insight into fate maintenance of fetal testes through the action of putative freemartin factors.

Suggested Citation

  • Karina F. Rodriguez & Paula R. Brown & Ciro M. Amato & Barbara Nicol & Chia-Feng Liu & Xin Xu & Humphrey Hung-Chang Yao, 2022. "Somatic cell fate maintenance in mouse fetal testes via autocrine/paracrine action of AMH and activin B," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31486-y
    DOI: 10.1038/s41467-022-31486-y
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    References listed on IDEAS

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    1. 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.
    2. Jonathan A. Griffiths & Arianne C. Richard & Karsten Bach & Aaron T. L. Lun & John C. Marioni, 2018. "Detection and removal of barcode swapping in single-cell RNA-seq data," Nature Communications, Nature, vol. 9(1), pages 1-6, December.
    3. 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.
    4. 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.
    5. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
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