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Drosophila Neuropeptide F Signaling Independently Regulates Feeding and Sleep-Wake Behavior.

ABSTRACT: Proper regulation of sleep-wake behavior and feeding is essential for organismal health and survival. While previous studies have isolated discrete neural loci and substrates important for either sleep or feeding, how the brain is organized to coordinate both processes with respect to one another remains poorly understood. Here, we provide evidence that the Drosophila Neuropeptide F (NPF) network forms a critical component of both adult sleep and feeding regulation. Activation of NPF signaling in the brain promotes wakefulness and adult feeding, likely through its cognate receptor NPFR. Flies carrying a loss-of-function NPF allele do not suppress sleep following prolonged starvation conditions, suggesting that NPF acts as a hunger signal to keep the animal awake. NPF-expressing cells, specifically those expressing the circadian photoreceptor cryptochrome, are largely responsible for changes to sleep behavior caused by NPF neuron activation, but not feeding, demonstrating that different NPF neurons separately drive wakefulness and hunger.

SUBMITTER: Chung BY

PROVIDER: S-EPMC5536846 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Drosophila Neuropeptide F Signaling Independently Regulates Feeding and Sleep-Wake Behavior.

Chung Brian Y BY Ro Jennifer J Hutter Sabine A SA Miller Kylie M KM Guduguntla Lakshmi S LS Kondo Shu S Pletcher Scott D SD

Cell reports 20170601 12

Proper regulation of sleep-wake behavior and feeding is essential for organismal health and survival. While previous studies have isolated discrete neural loci and substrates important for either sleep or feeding, how the brain is organized to coordinate both processes with respect to one another remains poorly understood. Here, we provide evidence that the Drosophila Neuropeptide F (NPF) network forms a critical component of both adult sleep and feeding regulation. Activation of NPF signaling i ...[more]

PMID: 28636933

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Project description:Behavior and physiology are orchestrated by neuropeptides acting as central neuromodulators and circulating hormones. An outstanding question is how these neuropeptides function to coordinate complex and competing behaviors. In Drosophila, the neuropeptide leucokinin (LK) modulates diverse functions, but mechanisms underlying these complex interactions remain poorly understood. As a first step towards understanding these mechanisms, we delineated LK circuitry that governs various aspects of post-feeding physiology and behavior. We found that impaired LK signaling in Lk and Lk receptor (Lkr) mutants affects diverse but coordinated processes, including regulation of stress, water homeostasis, feeding, locomotor activity, and metabolic rate. Next, we sought to define the populations of LK neurons that contribute to the different aspects of this physiology. We find that the calcium activity in abdominal ganglia LK neurons (ABLKs), but not in the two sets of brain neurons, increases specifically following water consumption, suggesting that ABLKs regulate water homeostasis and its associated physiology. To identify targets of LK peptide, we mapped the distribution of Lkr expression, mined a brain single-cell transcriptome dataset for genes coexpressed with Lkr, and identified synaptic partners of LK neurons. Lkr expression in the brain insulin-producing cells (IPCs), gut, renal tubules and chemosensory cells, correlates well with regulatory roles detected in the Lk and Lkr mutants. Furthermore, these mutants and flies with targeted knockdown of Lkr in IPCs displayed altered expression of insulin-like peptides (DILPs) and transcripts in IPCs and increased starvation resistance. Thus, some effects of LK signaling appear to occur via DILP action. Collectively, our data suggest that the three sets of LK neurons have different targets, but modulate the establishment of post-prandial homeostasis by regulating distinct physiological processes and behaviors such as diuresis, metabolism, organismal activity and insulin signaling. These findings provide a platform for investigating feeding-related neuroendocrine regulation of vital behavior and physiology.

Project description:BackgroundPrevious studies demonstrated a short-term relationship between infant sleep-wake states and oral feeding performance, with state being an indication of infants' neurobehavioral readiness for feeding. However, the relationship between sleep-wake states and feeding skills has not been evaluated longitudinally during hospitalization.ObjectivesThe purpose of this study was to examine preterm infants' sleep-wake state developmental trajectories and their associations with feeding progression during hospitalization.MethodsThis descriptive and exploratory study was a secondary analysis using data from a longitudinal two-group, randomized controlled trial evaluating the effects of early and late cycled light on health and developmental outcomes among extremely preterm infants who were born ≤28 weeks of gestational age. Sleep-wake states were assessed for two 2-hour interfeeding periods per day (day and night hours), 30 weeks postmenstrual age, and every 3 weeks until discharge. Occurrences of active sleep, quiet sleep, and waking were recorded every 10 seconds. Feeding progression was assessed based on an infant's postmenstrual age at five milestones: first enteral feeding, full enteral feeding, first oral feeding, half oral feeding, and full oral feeding. Trajectory analyses were used to describe developmental changes in sleep-wake states, feeding progression patterns, and associations between feeding progression and sleep-wake trajectories.ResultsActive sleep decreased while waking, and quiet sleep increased during hospitalization. Two distinct feeding groups were identified: typical and delayed feeding progression. In infants with delayed feeding progression, rates of active and quiet sleep development during the day were delayed compared to those with typical feeding progression. We also found that infants with delayed feeding progression were more likely to be awake more often during the night compared to infants with typical feeding progression.DiscussionsFindings suggest that delays in sleep-wake state development may be associated with delays in feeding progression during hospitalization. Infants with delayed feeding skill development may require more environmental protection to further support their sleep development.

Dataset Information

Drosophila Neuropeptide F Signaling Independently Regulates Feeding and Sleep-Wake Behavior.

Publications

Drosophila Neuropeptide F Signaling Independently Regulates Feeding and Sleep-Wake Behavior.

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