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Drosophila insulin-like peptide 2 mediates dietary regulation of sleep intensity

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  • Elizabeth B Brown
  • Kreesha D Shah
  • Richard Faville
  • Benjamin Kottler
  • Alex C Keene

Abstract

Sleep is a nearly universal behavior that is regulated by diverse environmental stimuli and physiological states. A defining feature of sleep is a homeostatic rebound following deprivation, where animals compensate for lost sleep by increasing sleep duration and/or sleep depth. The fruit fly, Drosophila melanogaster, exhibits robust recovery sleep following deprivation and represents a powerful model to study neural circuits regulating sleep homeostasis. Numerous neuronal populations have been identified in modulating sleep homeostasis as well as depth, raising the possibility that the duration and quality of recovery sleep is dependent on the environmental or physiological processes that induce sleep deprivation. Here, we find that unlike most pharmacological and environmental manipulations commonly used to restrict sleep, starvation potently induces sleep loss without a subsequent rebound in sleep duration or depth. Both starvation and a sucrose-only diet result in increased sleep depth, suggesting that dietary protein is essential for normal sleep depth and homeostasis. Finally, we find that Drosophila insulin like peptide 2 (Dilp2) is acutely required for starvation-induced changes in sleep depth without regulating the duration of sleep. Flies lacking Dilp2 exhibit a compensatory sleep rebound following starvation-induced sleep deprivation, suggesting Dilp2 promotes resiliency to sleep loss. Together, these findings reveal innate resilience to starvation-induced sleep loss and identify distinct mechanisms that underlie starvation-induced changes in sleep duration and depth.Author summary: Sleep is nearly universal throughout the animal kingdom and homeostatic regulation represents a defining feature of sleep, where animals compensate for lost sleep by increasing sleep over subsequent time periods. Despite the robustness of this feature, the neural mechanisms regulating recovery from different types of sleep deprivation are not fully understood. Fruit flies provide a powerful model for investigating the genetic regulation of sleep, and like mammals, display robust recovery sleep following deprivation. Here, we find that unlike most stimuli that suppress sleep, sleep deprivation by starvation does not require a homeostatic rebound. These findings are likely due to flies engaging in deeper sleep during the period of partial sleep deprivation, suggesting a natural resilience to starvation-induced sleep loss. This unique resilience to starvation-induced sleep loss is dependent on Drosophila insulin-like peptide 2, revealing a critical role for insulin signaling in regulating interactions between diet and sleep homeostasis.

Suggested Citation

  • Elizabeth B Brown & Kreesha D Shah & Richard Faville & Benjamin Kottler & Alex C Keene, 2020. "Drosophila insulin-like peptide 2 mediates dietary regulation of sleep intensity," PLOS Genetics, Public Library of Science, vol. 16(3), pages 1-26, March.
  • Handle: RePEc:plo:pgen00:1008270
    DOI: 10.1371/journal.pgen.1008270
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    References listed on IDEAS

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    1. Gang Liu & Holger Seiler & Ai Wen & Troy Zars & Kei Ito & Reinhard Wolf & Martin Heisenberg & Li Liu, 2006. "Distinct memory traces for two visual features in the Drosophila brain," Nature, Nature, vol. 439(7076), pages 551-556, February.
    2. Melvyn H. W. Yap & Martyna J. Grabowska & Chelsie Rohrscheib & Rhiannon Jeans & Michael Troup & Angelique C. Paulk & Bart Alphen & Paul J. Shaw & Bruno van Swinderen, 2017. "Oscillatory brain activity in spontaneous and induced sleep stages in flies," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    3. Diogo Pimentel & Jeffrey M. Donlea & Clifford B. Talbot & Seoho M. Song & Alexander J. F. Thurston & Gero Miesenböck, 2016. "Operation of a homeostatic sleep switch," Nature, Nature, vol. 536(7616), pages 333-337, August.
    4. Maria E Yurgel & Priyanka Kakad & Meet Zandawala & Dick R Nässel & Tanja A Godenschwege & Alex C Keene, 2019. "A single pair of leucokinin neurons are modulated by feeding state and regulate sleep–metabolism interactions," PLOS Biology, Public Library of Science, vol. 17(2), pages 1-26, February.
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