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Enteric neurons increase maternal food intake during reproduction

Author

Listed:
  • Dafni Hadjieconomou

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • George King

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Pedro Gaspar

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Alessandro Mineo

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Laura Blackie

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Tomotsune Ameku

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Chris Studd

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Alex Mendoza

    (The University of Western Australia
    Harry Perkins Institute of Medical Research
    Queen Mary University of London)

  • Fengqiu Diao

    (National Institute of Mental Health, National Institutes of Health)

  • Benjamin H. White

    (National Institute of Mental Health, National Institutes of Health)

  • André E. X. Brown

    (MRC London Institute of Medical Sciences
    Imperial College London)

  • Pierre-Yves Plaçais

    (CNRS, ESPCI Paris, PSL Research University)

  • Thomas Préat

    (CNRS, ESPCI Paris, PSL Research University)

  • Irene Miguel-Aliaga

    (MRC London Institute of Medical Sciences
    Imperial College London)

Abstract

Reproduction induces increased food intake across females of many animal species1–4, providing a physiologically relevant paradigm for the exploration of appetite regulation. Here, by examining the diversity of enteric neurons in Drosophila melanogaster, we identify a key role for gut-innervating neurons with sex- and reproductive state-specific activity in sustaining the increased food intake of mothers during reproduction. Steroid and enteroendocrine hormones functionally remodel these neurons, which leads to the release of their neuropeptide onto the muscles of the crop—a stomach-like organ—after mating. Neuropeptide release changes the dynamics of crop enlargement, resulting in increased food intake, and preventing the post-mating remodelling of enteric neurons reduces both reproductive hyperphagia and reproductive fitness. The plasticity of enteric neurons is therefore key to reproductive success. Our findings provide a mechanism to attain the positive energy balance that sustains gestation, dysregulation of which could contribute to infertility or weight gain.

Suggested Citation

  • Dafni Hadjieconomou & George King & Pedro Gaspar & Alessandro Mineo & Laura Blackie & Tomotsune Ameku & Chris Studd & Alex Mendoza & Fengqiu Diao & Benjamin H. White & André E. X. Brown & Pierre-Yves , 2020. "Enteric neurons increase maternal food intake during reproduction," Nature, Nature, vol. 587(7834), pages 455-459, November.
  • Handle: RePEc:nat:nature:v:587:y:2020:i:7834:d:10.1038_s41586-020-2866-8
    DOI: 10.1038/s41586-020-2866-8
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    Cited by:

    1. Yunpo Zhao & Mohammed A. Khallaf & Emilia Johansson & Najat Dzaki & Shreelatha Bhat & Johannes Alfredsson & Jianli Duan & Bill S. Hansson & Markus Knaden & Mattias Alenius, 2022. "Hedgehog-mediated gut-taste neuron axis controls sweet perception in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Christian F. Christensen & Quentin Laurichesse & Rihab Loudhaief & Julien Colombani & Ditte S. Andersen, 2024. "Drosophila activins adapt gut size to food intake and promote regenerative growth," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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