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A nutrient-responsive hormonal circuit mediates an inter-tissue program regulating metabolic homeostasis in adult Drosophila

Author

Listed:
  • Takashi Koyama

    (University of Copenhagen)

  • Selim Terhzaz

    (University of Glasgow
    MRC-University of Glasgow Centre for Virus Research)

  • Muhammad T. Naseem

    (University of Copenhagen)

  • Stanislav Nagy

    (University of Copenhagen)

  • Kim Rewitz

    (University of Copenhagen)

  • Julian A. T. Dow

    (University of Glasgow)

  • Shireen A. Davies

    (University of Glasgow)

  • Kenneth V. Halberg

    (University of Copenhagen)

Abstract

Animals maintain metabolic homeostasis by modulating the activity of specialized organs that adjust internal metabolism to external conditions. However, the hormonal signals coordinating these functions are incompletely characterized. Here we show that six neurosecretory cells in the Drosophila central nervous system respond to circulating nutrient levels by releasing Capa hormones, homologs of mammalian neuromedin U, which activate the Capa receptor (CapaR) in peripheral tissues to control energy homeostasis. Loss of Capa/CapaR signaling causes intestinal hypomotility and impaired nutrient absorption, which gradually deplete internal nutrient stores and reduce organismal lifespan. Conversely, increased Capa/CapaR activity increases fluid and waste excretion. Furthermore, Capa/CapaR inhibits the release of glucagon-like adipokinetic hormone from the corpora cardiaca, which restricts energy mobilization from adipose tissue to avoid harmful hyperglycemia. Our results suggest that the Capa/CapaR circuit occupies a central node in a homeostatic program that facilitates the digestion and absorption of nutrients and regulates systemic energy balance.

Suggested Citation

  • Takashi Koyama & Selim Terhzaz & Muhammad T. Naseem & Stanislav Nagy & Kim Rewitz & Julian A. T. Dow & Shireen A. Davies & Kenneth V. Halberg, 2021. "A nutrient-responsive hormonal circuit mediates an inter-tissue program regulating metabolic homeostasis in adult Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25445-2
    DOI: 10.1038/s41467-021-25445-2
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    Cited by:

    1. Olga Kubrak & Takashi Koyama & Nadja Ahrentløv & Line Jensen & Alina Malita & Muhammad T. Naseem & Mette Lassen & Stanislav Nagy & Michael J. Texada & Kenneth V. Halberg & Kim Rewitz, 2022. "The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Olga Kubrak & Anne F. Jørgensen & Takashi Koyama & Mette Lassen & Stanislav Nagy & Jacob Hald & Gianluca Mazzoni & Dennis Madsen & Jacob B. Hansen & Martin Røssel Larsen & Michael J. Texada & Jakob L., 2024. "LGR signaling mediates muscle-adipose tissue crosstalk and protects against diet-induced insulin resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Alka Singh & Kandahalli Venkataranganayaka Abhilasha & Kathya R. Acharya & Haibo Liu & Niraj K. Nirala & Velayoudame Parthibane & Govind Kunduri & Thiruvaimozhi Abimannan & Jacob Tantalla & Lihua Juli, 2024. "A nutrient responsive lipase mediates gut-brain communication to regulate insulin secretion in Drosophila," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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