A G-protein-coupled Neuropeptide Y-like Receptor Suppresses Behavioral and Sensory Response to Multiple Stressful Stimuli in Drosophila

Overview

Journal J Neurosci

Specialty Neurology

Date 2010 Feb 19

PMID 20164335

Citations 23

Authors

Jie Xu

Mo Li

Ping Shen

Affiliations

Soon will be listed here.

Abstract

Recent studies suggest that human neuropeptide Y (NPY) plays a prominent role in management of stress response and emotion, and higher NPY levels observed in combat-exposed veterans may help coping with posttraumatic stress. Neuropeptide F (NPF), the counterpart of NPY in Drosophila melanogaster, also displays parallel activities, including promotion of resilience to diverse stressors and prevention of uncontrolled aggressive behavior. However, it remains unclear how NPY family peptides modulate physical and emotional responses to various stressors. Here we show that NPFR1, a G-protein-coupled NPF receptor, exerts an inhibitory effect on larval aversion to diverse stressful stimuli mediated by different subtypes of fly and mammalian transient receptor potential (TRP) family channels. Imaging analysis in larval sensory neurons and cultured human cells showed that NPFR1 attenuates Ca(2+) influx mediated by fly TRPA and rat TRPV1 channels. Our findings suggest that suppression of TRP channel-mediated neural excitation by the conserved NPF/NPFR1 system may be a major mechanism for attaining its broad anti-stress function.

Citing Articles

Exposure to Environmental Pollutants and Risk of Diarrhea: A Systematic Review.

Nwanaforo E, Obasi C, Frazzoli C, Bede-Ojimadu O, Orisakwe O Environ Health Insights. 2024; 18:11786302241304539.

PMID: 39619770 PMC: 11608449. DOI: 10.1177/11786302241304539.

Failure to mate enhances investment in behaviors that may promote mating reward and impairs the ability to cope with stressors via a subpopulation of Neuropeptide F receptor neurons.

Ryvkin J, Omesi L, Kim Y, Levi M, Pozeilov H, Barak-Buchris L PLoS Genet. 2024; 20(1):e1011054.

PMID: 38236837 PMC: 10795991. DOI: 10.1371/journal.pgen.1011054.

Transcriptomic comparison between populations selected for higher and lower mobility in the red flour beetle Tribolium castaneum.

Matsumura K, Onuma T, Kondo S, Noguchi H, Uchiyama H, Yajima S Sci Rep. 2024; 14(1):67.

PMID: 38167631 PMC: 10762016. DOI: 10.1038/s41598-023-50923-6.

Descending control of nociception in insects?.

Gibbons M, Sarlak S, Chittka L Proc Biol Sci. 2022; 289(1978):20220599.

PMID: 35858073 PMC: 9257290. DOI: 10.1098/rspb.2022.0599.

The short neuropeptide F regulates appetitive but not aversive responsiveness in a social insect.

Bestea L, Paoli M, Arrufat P, Ronsin B, Carcaud J, Sandoz J iScience. 2022; 25(1):103619.

PMID: 35005557 PMC: 8719019. DOI: 10.1016/j.isci.2021.103619.

References

Thorsell A, Heilig M . Diverse functions of neuropeptide Y revealed using genetically modified animals. Neuropeptides. 2002; 36(2-3):182-93. DOI: 10.1054/npep.2002.0897. View

Mostany R, Diaz A, Valdizan E, Rodriguez-Munoz M, Garzon J, Hurle M . Supersensitivity to mu-opioid receptor-mediated inhibition of the adenylyl cyclase pathway involves pertussis toxin-resistant Galpha protein subunits. Neuropharmacology. 2008; 54(6):989-97. DOI: 10.1016/j.neuropharm.2008.02.004. View

Moran M, Xu H, Clapham D . TRP ion channels in the nervous system. Curr Opin Neurobiol. 2004; 14(3):362-9. DOI: 10.1016/j.conb.2004.05.003. View

Zhu W, Xu P, Cuascut F, Hall A, Oxford G . Activin acutely sensitizes dorsal root ganglion neurons and induces hyperalgesia via PKC-mediated potentiation of transient receptor potential vanilloid I. J Neurosci. 2007; 27(50):13770-80. PMC: 6673610. DOI: 10.1523/JNEUROSCI.3822-07.2007. View

Lingo P, Zhao Z, Shen P . Co-regulation of cold-resistant food acquisition by insulin- and neuropeptide Y-like systems in Drosophila melanogaster. Neuroscience. 2007; 148(2):371-4. PMC: 2837932. DOI: 10.1016/j.neuroscience.2007.06.010. View

Gibbs J, Hargreaves K . Neuropeptide Y Y1 receptor effects on pulpal nociceptors. J Dent Res. 2008; 87(10):948-52. PMC: 2576745. DOI: 10.1177/154405910808701008. View

Bhave G, Zhu W, Wang H, Brasier D, Oxford G, Gereau 4th R . cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron. 2002; 35(4):721-31. DOI: 10.1016/s0896-6273(02)00802-4. View

Montell C, Birnbaumer L, Flockerzi V . The TRP channels, a remarkably functional family. Cell. 2002; 108(5):595-8. DOI: 10.1016/s0092-8674(02)00670-0. View

Gordon M, Scott K . Motor control in a Drosophila taste circuit. Neuron. 2009; 61(3):373-84. PMC: 2650400. DOI: 10.1016/j.neuron.2008.12.033. View

10.

Montell C . Drosophila TRP channels. Pflugers Arch. 2005; 451(1):19-28. DOI: 10.1007/s00424-005-1426-2. View

11.

Wang J, Wong A, Flores J, Vosshall L, Axel R . Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell. 2003; 112(2):271-82. DOI: 10.1016/s0092-8674(03)00004-7. View

12.

Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K . Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron. 2006; 49(2):285-95. DOI: 10.1016/j.neuron.2005.11.037. View

13.

Hucho T, Dina O, Levine J . Epac mediates a cAMP-to-PKC signaling in inflammatory pain: an isolectin B4(+) neuron-specific mechanism. J Neurosci. 2005; 25(26):6119-26. PMC: 6725047. DOI: 10.1523/JNEUROSCI.0285-05.2005. View

14.

Garczynski S, Brown M, Shen P, Murray T, Crim J . Characterization of a functional neuropeptide F receptor from Drosophila melanogaster. Peptides. 2002; 23(4):773-80. DOI: 10.1016/s0196-9781(01)00647-7. View

15.

Jewett D, Cleary J, Levine A, Schaal D, Thompson T . Effects of neuropeptide Y, insulin, 2-deoxyglucose, and food deprivation on food-motivated behavior. Psychopharmacology (Berl). 1995; 120(3):267-71. DOI: 10.1007/BF02311173. View

16.

Demuth D, Molleman A . Cannabinoid signalling. Life Sci. 2005; 78(6):549-63. DOI: 10.1016/j.lfs.2005.05.055. View

17.

Ramsey I, Delling M, Clapham D . An introduction to TRP channels. Annu Rev Physiol. 2006; 68:619-47. DOI: 10.1146/annurev.physiol.68.040204.100431. View

18.

Zhou Z, Zhu G, Hariri A, Enoch M, Scott D, Sinha R . Genetic variation in human NPY expression affects stress response and emotion. Nature. 2008; 452(7190):997-1001. PMC: 2715959. DOI: 10.1038/nature06858. View

19.

Tracey Jr W, Wilson R, Laurent G, Benzer S . painless, a Drosophila gene essential for nociception. Cell. 2003; 113(2):261-73. DOI: 10.1016/s0092-8674(03)00272-1. View

20.

FLOOD J, Morley J . Increased food intake by neuropeptide Y is due to an increased motivation to eat. Peptides. 1991; 12(6):1329-32. DOI: 10.1016/0196-9781(91)90215-b. View