A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila

Journal of Neuroscience

Volumn 30, Issue 7, 2010, Pages 2504-2512

  Xu, Jie ^a   Li, Mo ^a   Shen, Ping ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CAPSAICIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; NEUROPEPTIDE; NEUROPEPTIDE F; PROTEIN NPFR1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ARTICLE; AVERSION; CALCIUM TRANSPORT; CELL CULTURE; CELL STRAIN HEK293; CONTROLLED STUDY; DROSOPHILA; HUMAN; HUMAN CELL; LARVA; NEUROIMAGING; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SENSORY NERVE CELL; STRESS;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CALCIUM; CAPSAICIN; CARBOHYDRATES; CELL LINE, TRANSFORMED; CYCLIC GMP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LARVA; LOCOMOTION; LUMINESCENT PROTEINS; NEURONS; NEUROPEPTIDES; PAIN MEASUREMENT; PHYSICAL STIMULATION; RECEPTORS, NEUROPEPTIDE; RECEPTORS, NEUROPEPTIDE Y; SENSATION; SENSORY SYSTEM AGENTS; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; STRESS, PHYSIOLOGICAL; THIONUCLEOTIDES; TIME FACTORS; TRANSFECTION; TRPV CATION CHANNELS;

EID: 77249145891     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3262-09.2010     Document Type: Article

References (49)

1. Al-Anzi B, TraceyWDJr, Benzer S (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ ANKTM1. Curr Biol 16:1034-1040.
2. Alyokhin A, Mille C, Messing R, Duan J (2001) Selection of pupation habitats by oriental fruit fly larvae in the laboratory. J Insect Behav 14:57-67.
3. Ashburner M (1989) Drosophila: a laboratory handbook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
4. Bannon AW, Seda J, Carmouche M, Francis JM, Norman MH, Karbon B, McCaleb ML (2000) Behavioral characterization of neuropeptide Y knockout mice. Brain Res 868:79-87.
5. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW 4th (2002) cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35:721-731.
6. Broder J, Majumder A, Porter E, Srinivasamoorthy G, Keith C, Lauderdale J, Sornborger A (2007) Estimating weak ratiometric signals in imaging data. I. Dual-channel data. J Opt Soc Am A Opt Image Sci Vis 24:2921-2931.
7. Brumovsky P, Shi TS, Landry M, Villar MJ, Hökfelt T (2007) Neuropeptide tyrosine and pain. Trends Pharmacol Sci 28:93-102.
8. Caterina MJ, Julius D (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24:487-517.
9. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
10. Chiang HC, Hodson AC (1950) An analytical study of population growth in Drosophila melanogaster. Ecol Monogr 20:173-206.
11. Demuth DG, Molleman A (2006) Cannabinoid signalling. Life Sci 78:549-563.
12. Díaz-Laviada I, Ruiz-Llorente L (2005) Signal transduction activated by cannabinoid receptors. Mini Rev Med Chem 5:619-630.
13. Diversé-Pierluissi M, Goldsmith PK, Dunlap K (1995) Transmitter-mediated inhibition of N-type calcium channels in sensory neurons involves multiple GTP-binding proteins and subunits. Neuron 14:191-200.
14. Endres-Becker J, Heppenstall PA, Mousa SA, Labuz D, Oksche A, Schäfer M, Stein C, Zöllner C (2007) Mu-opioid receptor activation modulates transient receptor potential vanilloid 1 (TRPV1) currents in sensory neurons in a model of inflammatory pain. Mol Pharmacol 71:12-18.
15. Flood JF, Morley JE (1991) Increased food intake by neuropeptide Y is due to an increased motivation to eat. Peptides 12:1329-1332.
16. Garczynski SF, Brown MR, Shen P, Murray TF, Crim JW (2002) Characterization of a functional neuropeptide F receptor from Drosophila melanogaster. Peptides 23:773-780.
17. Gibbs JL, Hargreaves KM (2008) Neuropeptide Y Y1 receptor effects on pulpal nociceptors. J Dent Res 87:948-952.
18. Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61:373-384.
19. Hu SJ, Song XJ, Greenquist KW, Zhang JM, LaMotte RH (2001) Protein kinase A modulates spontaneous activity in chronically compressed dorsal root ganglion neurons in the rat. Pain 94:39-46.
20. 4+ neuron-specific mechanism. J Neurosci 25:6119-6126.
21. Jewett DC, Cleary J, Levine AS, Schaal DW, Thompson T (1995) Effects of neuropeptide Y, insulin, 2-deoxyglucose, and food deprivation on foodmotivated behavior. Psychopharmacology (Berl) 120:267-271.
22. Kiger JA Jr, Eklund JL, Younger SH, O'Kane CJ (1999) Transgenic inhibitors identify two roles for protein kinase A in Drosophila development. Genetics 152:281-290.
23. Lingo PR, Zhao Z, Shen P (2007) Co-regulation of cold-resistant food acquisition by insulin- and neuropeptide Y-like systems in Drosophila melanogaster. Neuroscience 148:371-374.
24. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285-295.
25. 2+ measurements using improved cameleons. Proc Natl Acad Sci U S A 96:2135-2140.
26. Montell C (2005) Drosophila TRP channels. Pflugers Arch 451:19-28.
27. Montell C, Birnbaumer L, Flockerzi V (2002) The TRP channels, a remarkably functional family. Cell 108:595-598.
28. Moran MM, Xu H, Clapham DE (2004) TRP ion channels in the nervous system. Curr Opin Neurobiol 14:362-369.
29. Mostany R, Díaz A, Valdizán EM, Rodríguez- MuñozM, Garzón J, Hurlé MA (2008) Supersensitivity to mu-opioid receptor-mediated inhibition of the adenylyl cyclase pathway involves pertussis toxin-resistant Galpha protein subunits. Neuropharmacology 54:989-997.
30. Mukhopadhyay S, Shim JY, Assi AA, Norford D, Howlett AC (2002) CB1 cannabinoid receptor-G protein association: a possible mechanism for differential signaling. Chem Phys Lipids 121:91-109.
31. Pertwee RG (2001) Cannabinoid receptors and pain. Prog Neurobiol 63:569-611.
32. Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619-647.
33. Shen P, Cai HN (2001) Drosophila neuropeptide F mediates integration of chemosensory stimulation and conditioning of the nervous system by food. J Neurobiol 47:16-25.
34. Song XJ, Wang ZB, Gan Q, Walters ET (2006) cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression. J Neurophysiol 95:479-492.
35. Thomas D (1995) Predation on the soil inhabiting stages of the Mexican fruit fly. Southwest Entomol 20:61-71.
36. Thomson D (1982) Spectrum estimation and harmonic analysis. Proc IEEE 70:1055-1096.
37. Thorsell A, Heilig M (2002) Diverse functions of neuropeptide Y revealed using genetically modified animals. Neuropeptides 36:182-193.
38. Thorsell A, Michalkiewicz M, Dumont Y, Quirion R, Caberlotto L, Rimondini R, Mathé AA, Heilig M (2000) Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc Natl Acad Sci U S A 97:12852-12857.
39. Tracey WD Jr, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila gene essential for nociception. Cell 113:261-273.
40. Vetter I, Cheng W, Peiris M, Wyse BD, Roberts-Thomson SJ, Zheng J, Monteith GR, Cabot PJ (2008) Rapid, opioid-sensitive mechanisms involved in transient receptor potential vanilloid 1 sensitization. J Biol Chem 283:19540-19550.
41. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
42. Wen T, Parrish CA, Xu D, Wu Q, Shen P (2005) Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci U S A 102:2141-2146.
43. Wu Q, Wen T, Lee G, Park JH, Cai HN, Shen P (2003) Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39:147-161.
44. Wu Q, Zhao Z, Shen P (2005a) Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems. Nat Neurosci 8:1350-1355.
45. Wu Q, Zhang Y, Xu J, Shen P (2005b) Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad SciU S A 102:13289-13294.
46. Xu J, Sornborger AT, Lee JK, Shen P (2008) Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat Neurosci 11:676-682.
47. ATP channel. J Biol Chem 283:5306-5316.
48. Zhou Z, Zhu G, Hariri AR, Enoch MA, Scott D, Sinha R, Virkkunen M, Mash DC, Lipsky RH, Hu XZ, Hodgkinson CA, Xu K, Buzas B, Yuan Q, Shen PH, Ferrell RE, Manuck SB, Brown SM, Hauger RL, Stohler CS, Zubieta JK, Goldman D (2008) Genetic variation in human NPY expression affects stress response and emotion. Nature 452:997-1001.
49. Zhu W, Xu P, Cuascut FX, Hall AK, Oxford GS (2007) Activin acutely sensitizes dorsal root ganglion neurons and induces hyperalgesia via PKCmediated potentiation of transient receptor potential vanilloid I. J Neurosci 27:13770-13780.