A fat-derived metabolite regulates a peptidergic feeding circuit in Drosophila

Kim, Dohyoung; Shin, Min-Gyoung; Jung, Sunghwan; Kim, Youngjoon; Jones, Walton D.

doi:10.1371/journal.pbio.2000532

Cited by 26 publications

(23 citation statements)

References 48 publications

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“…Hormonal signals also play important roles in mediating hunger control in the fruit fly Drosophila ; these include insulin-like peptides, the two homologs of mammalian NPY (Neuropeptide F, NPF, and short Neuropeptide F, sNPF), the homolog of mammalian leptin (Unpaired 2, Upd2), the insect analog of glucagon (adipokinetic hormone, AKH), and a handful of other neuropeptides and metabolites ( Dus et al, 2015 ; Inagaki et al, 2014 ; Jourjine et al, 2016 ; Kim et al, 2017 ; Lee et al, 2004 ; Pool and Scott, 2014 ; Rajan and Perrimon, 2012 ; Root et al, 2011 ; Sun et al, 2017 ; Wu et al, 2005 ; Yu et al, 2016 ). These hormonal signals and neuromodulators are regulated by starvation and have been shown to modulate neural circuit functions in both the periphery ( Farhan et al, 2013 ; Inagaki et al, 2014 ; 2012 ; Ko et al, 2015 ; LeDue et al, 2016 ; Root et al, 2011 ) and the brain ( Beshel et al, 2017 ; Beshel and Zhong, 2013 ; Schlegel et al, 2016 ; Wang et al, 2013 ; Yu et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

Tsao

Chen

Lin

et al. 2018

eLife

167

192

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The fruit fly can evaluate its energy state and decide whether to pursue food-related cues. Here, we reveal that the mushroom body (MB) integrates hunger and satiety signals to control food-seeking behavior. We have discovered five pathways in the MB essential for hungry flies to locate and approach food. Blocking the MB-intrinsic Kenyon cells (KCs) and the MB output neurons (MBONs) in these pathways impairs food-seeking behavior. Starvation bi-directionally modulates MBON responses to a food odor, suggesting that hunger and satiety controls occur at the KC-to-MBON synapses. These controls are mediated by six types of dopaminergic neurons (DANs). By manipulating these DANs, we could inhibit food-seeking behavior in hungry flies or promote food seeking in fed flies. Finally, we show that the DANs potentially receive multiple inputs of hunger and satiety signals. This work demonstrates an information-rich central circuit in the fly brain that controls hunger-driven food-seeking behavior.

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Section: Introductionmentioning

confidence: 99%

Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

Tsao

Chen

Lin

et al. 2018

eLife

167

192

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“…NPF neurons are intensively studied multifunctional neurons including courtship, aggression, feeding, and sleep behaviors (Chung et al, ; Dierick & Greenspan, ; Kim, Shin, Jung, Kim, & Jones, ; Kim, Jan, & Jan, ). However, there have been no studies characterized biological functions of the specific subsets of the NPF neurons.…”

Section: Discussionmentioning

confidence: 99%

A cyclic nucleotide‐gated channel in the brain regulates olfactory modulation through neuropeptide F in fruit fly Drosophila melanogaster

Lee

Jones

Kim

2019

Arch Insect Biochem Physiol

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Olfactory sensing and its modulation are important for the insects in recognizing diverse odors from the environment and in making correct decisions to survive. Identifying new genes involved in olfactory modulation and unveiling their mechanisms may lead us to understand decision making processes in the central nervous system. Here, we report a novel olfactory function of the cyclic nucleotide-gated (CNG) channel CG42260 in modulating ab3A olfactory sensory neurons, which specifically respond to food-derived odors in fruit fly Drosophila melanogaster. We found that two independent CG42260 mutants show reduced responses in the ab3A neurons. Unlike mammalian CNGs, CG42260 is not expressed in the odorant sensory neurons but broadly in the central nervous system including neuropeptide-producing cells. By using molecular genetic tools, we identified CG42260 expression in one pair of neuropeptide F (NPF) positive L1-l cells known to modulate food odor responsiveness. Knockdown of CG42260 in the NPF neurons reduced production of NPF in Ll-1 cells, which in turn, led to reduction of neuronal responses of the ab3A neurons. Our findings show the novel biological function of CG42260 in modulating olfactory responses to food odor through NPF. K E Y W O R D S

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“…To our knowledge, this study represents the first genetic screen for Drosophila sleep regulators that specifically examine the role of non-neuronal tissue in sleep regulation. The fat body is critical for regulating energy storage in Drosophila and has been implicated in many behaviors including sleep regulation, courtship, circadian rhythms, and feeding ( Lazareva et al 2007 ; Xu et al 2011 ; Kim et al 2017 ; Thimgan et al 2010 ). While the genetic examination of many behaviors, including sleep, have predominantly focused on investigating the neural regulation of behavior, the contribution of the fat body to behavioral regulation is less understood ( Iijima et al 2009 ; Xu et al 2011 ; Sassu et al 2012 ).…”

Section: Discussionmentioning

confidence: 99%

“…The GAL4 / UAS system, in combination with genome-wide RNAi libraries, allow for selectively decreasing gene expression in the fly fat body and then measuring the effects on sleep ( Brand and Perrimon 1993 ; Dietzl et al 2007 ). Growing evidence suggests that the fat body regulates complex behaviors including sleep ( Lazareva et al 2007 ; Kim et al 2017 ; Umezaki et al 2018 ), yet the molecular basis through which the fat body regulates sleep remains poorly understood.…”

mentioning

confidence: 99%

Ade2 Functions in the Drosophila Fat Body To Promote Sleep

Yurgel

Shah

Brown

et al. 2018

G3 Genes|Genomes|Genetics

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Metabolic state is a potent modulator of sleep and circadian behavior, and animals acutely modulate their sleep in accordance with internal energy stores and food availability. Across phyla, hormones secreted from adipose tissue act in the brain to control neural physiology and behavior to modulate sleep and metabolic state. Growing evidence suggests the fat body is a critical regulator of complex behaviors, but little is known about the genes that function within the fat body to regulate sleep. To identify molecular factors functioning in non-neuronal tissues to regulate sleep, we performed an RNAi screen selectively knocking down genes in the fat body. We found that knockdown of Phosphoribosylformylglycinamidine synthase/Pfas (Ade2), a highly conserved gene involved the biosynthesis of purines, sleep regulation and energy stores. Flies heterozygous for multiple Ade2 mutations are also short sleepers and this effect is partially rescued by restoring Ade2 to the Drosophila fat body. Targeted knockdown of Ade2 in the fat body does not alter arousal threshold or the homeostatic response to sleep deprivation, suggesting a specific role in modulating baseline sleep duration. Together, these findings suggest Ade2 functions within the fat body to promote both sleep and energy storage, providing a functional link between these processes.

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A fat-derived metabolite regulates a peptidergic feeding circuit in Drosophila

Cited by 26 publications

References 48 publications

Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

A cyclic nucleotide‐gated channel in the brain regulates olfactory modulation through neuropeptide F in fruit fly Drosophila melanogaster

Ade2 Functions in the Drosophila Fat Body To Promote Sleep

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