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The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress

Author

Listed:
  • Olga Kubrak

    (University of Copenhagen)

  • Takashi Koyama

    (University of Copenhagen)

  • Nadja Ahrentløv

    (University of Copenhagen)

  • Line Jensen

    (University of Copenhagen)

  • Alina Malita

    (University of Copenhagen)

  • Muhammad T. Naseem

    (University of Copenhagen)

  • Mette Lassen

    (University of Copenhagen)

  • Stanislav Nagy

    (University of Copenhagen)

  • Michael J. Texada

    (University of Copenhagen)

  • Kenneth V. Halberg

    (University of Copenhagen)

  • Kim Rewitz

    (University of Copenhagen)

Abstract

The intestine is a central regulator of metabolic homeostasis. Dietary inputs are absorbed through the gut, which senses their nutritional value and relays hormonal information to other organs to coordinate systemic energy balance. However, the gut-derived hormones affecting metabolic and behavioral responses are poorly defined. Here we show that the endocrine cells of the Drosophila gut sense nutrient stress through a mechanism that involves the TOR pathway and in response secrete the peptide hormone allatostatin C, a Drosophila somatostatin homolog. Gut-derived allatostatin C induces secretion of glucagon-like adipokinetic hormone to coordinate food intake and energy mobilization. Loss of gut Allatostatin C or its receptor in the adipokinetic-hormone-producing cells impairs lipid and sugar mobilization during fasting, leading to hypoglycemia. Our findings illustrate a nutrient-responsive endocrine mechanism that maintains energy homeostasis under nutrient-stress conditions, a function that is essential to health and whose failure can lead to metabolic disorders.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28268-x
    DOI: 10.1038/s41467-022-28268-x
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    References listed on IDEAS

    as
    1. Alejo Efeyan & William C. Comb & David M. Sabatini, 2015. "Nutrient-sensing mechanisms and pathways," Nature, Nature, vol. 517(7534), pages 302-310, January.
    2. Yuto Yoshinari & Hina Kosakamoto & Takumi Kamiyama & Ryo Hoshino & Rena Matsuoka & Shu Kondo & Hiromu Tanimoto & Akira Nakamura & Fumiaki Obata & Ryusuke Niwa, 2021. "The sugar-responsive enteroendocrine neuropeptide F regulates lipid metabolism through glucagon-like and insulin-like hormones in Drosophila melanogaster," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    3. 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.
    4. Georg Dietzl & Doris Chen & Frank Schnorrer & Kuan-Chung Su & Yulia Barinova & Michaela Fellner & Beate Gasser & Kaolin Kinsey & Silvia Oppel & Susanne Scheiblauer & Africa Couto & Vincent Marra & Kry, 2007. "A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila," Nature, Nature, vol. 448(7150), pages 151-156, July.
    5. Kenneth A. Halberg & Selim Terhzaz & Pablo Cabrero & Shireen A. Davies & Julian A. T. Dow, 2015. "Tracing the evolutionary origins of insect renal function," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    6. Seung K. Kim & Eric J. Rulifson, 2004. "Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells," Nature, Nature, vol. 431(7006), pages 316-320, September.
    7. Fumika N. Hamada & Mark Rosenzweig & Kyeongjin Kang & Stefan R. Pulver & Alfredo Ghezzi & Timothy J. Jegla & Paul A. Garrity, 2008. "An internal thermal sensor controlling temperature preference in Drosophila," Nature, Nature, vol. 454(7201), pages 217-220, July.
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    1. Chen Zhang & Anmo J. Kim & Crisalesandra Rivera-Perez & Fernando G. Noriega & Young-Joon Kim, 2022. "The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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