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A GREB1-steroid receptor feedforward mechanism governs differential GREB1 action in endometrial function and endometriosis

Author

Listed:
  • Sangappa B. Chadchan

    (Baylor College of Medicine, One Baylor Plaza)

  • Pooja Popli

    (Baylor College of Medicine, One Baylor Plaza)

  • Zian Liao

    (Baylor College of Medicine, One Baylor Plaza)

  • Eryk Andreas

    (Washington University School of Medicine)

  • Michelle Dias

    (Baylor College of Medicine, One Baylor Plaza)

  • Tianyuan Wang

    (Integrative Bioinformatics, National Institute of Environmental Health Sciences)

  • Stephanie J. Gunderson

    (Washington University School of Medicine)

  • Patricia T. Jimenez

    (Washington University School of Medicine)

  • Denise G. Lanza

    (Baylor College of Medicine, One Baylor Plaza)

  • Rainer B. Lanz

    (Baylor College of Medicine, One Baylor Plaza)

  • Charles E. Foulds

    (Lester and Sue Smith Breast Center, Baylor College of Medicine, One Baylor Plaza)

  • Diana Monsivais

    (Baylor College of Medicine, One Baylor Plaza)

  • Francesco J. DeMayo

    (Reproductive and Developmental Biology Laboratory, National Institute of Environmental Health Sciences)

  • Hari Krishna Yalamanchili

    (Baylor College of Medicine, One Baylor Plaza
    USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, One Baylor Plaza
    Jan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital)

  • Emily S. Jungheim

    (Washington University School of Medicine
    Fienberg School of Medicine)

  • Jason D. Heaney

    (Baylor College of Medicine, One Baylor Plaza)

  • John P. Lydon

    (Baylor College of Medicine, One Baylor Plaza)

  • Kelle H. Moley

    (Washington University School of Medicine)

  • Bert W. O’Malley

    (Baylor College of Medicine, One Baylor Plaza)

  • Ramakrishna Kommagani

    (Baylor College of Medicine, One Baylor Plaza
    Baylor College of Medicine, One Baylor Plaza)

Abstract

Cellular responses to the steroid hormones, estrogen (E2), and progesterone (P4) are governed by their cognate receptor’s transcriptional output. However, the feed-forward mechanisms that shape cell-type-specific transcriptional fulcrums for steroid receptors are unidentified. Herein, we found that a common feed-forward mechanism between GREB1 and steroid receptors regulates the differential effect of GREB1 on steroid hormones in a physiological or pathological context. In physiological (receptive) endometrium, GREB1 controls P4-responses in uterine stroma, affecting endometrial receptivity and decidualization, while not affecting E2-mediated epithelial proliferation. Of mechanism, progesterone-induced GREB1 physically interacts with the progesterone receptor, acting as a cofactor in a positive feedback mechanism to regulate P4-responsive genes. Conversely, in endometrial pathology (endometriosis), E2-induced GREB1 modulates E2-dependent gene expression to promote the growth of endometriotic lesions in mice. This differential action of GREB1 exerted by a common feed-forward mechanism with steroid receptors advances our understanding of mechanisms that underlie cell- and tissue-specific steroid hormone actions.

Suggested Citation

  • Sangappa B. Chadchan & Pooja Popli & Zian Liao & Eryk Andreas & Michelle Dias & Tianyuan Wang & Stephanie J. Gunderson & Patricia T. Jimenez & Denise G. Lanza & Rainer B. Lanz & Charles E. Foulds & Di, 2024. "A GREB1-steroid receptor feedforward mechanism governs differential GREB1 action in endometrial function and endometriosis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46180-4
    DOI: 10.1038/s41467-024-46180-4
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    References listed on IDEAS

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    1. Andrew M. Kelleher & Jessica Milano-Foster & Susanta K. Behura & Thomas E. Spencer, 2018. "Uterine glands coordinate on-time embryo implantation and impact endometrial decidualization for pregnancy success," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Xiaoqiu Wang & Xilong Li & Tianyuan Wang & San-Pin Wu & Jae-Wook Jeong & Tae Hoon Kim & Steven L. Young & Bruce A. Lessey & Rainer B. Lanz & John P. Lydon & Francesco J. DeMayo, 2018. "SOX17 regulates uterine epithelial–stromal cross-talk acting via a distal enhancer upstream of Ihh," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    3. Jia Yuan & Shizu Aikawa & Wenbo Deng & Amanda Bartos & Gerd Walz & Florian Grahammer & Tobias B. Huber & Xiaofei Sun & Sudhansu K. Dey, 2019. "Primary decidual zone formation requires Scribble for pregnancy success in mice," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Rong Li & Tianyuan Wang & Ryan M. Marquardt & John P. Lydon & San-Pin Wu & Francesco J. DeMayo, 2023. "TRIM28 modulates nuclear receptor signaling to regulate uterine function," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Jia Yuan & Wenbo Deng & Jeeyeon Cha & Xiaofei Sun & Jean-Paul Borg & Sudhansu. K. Dey, 2018. "Tridimensional visualization reveals direct communication between the embryo and glands critical for implantation," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
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