Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search

Cell

Volumn 145, Issue 1, 2011, Pages 133-144

  Root, Cory M ^a   Ko, Kang I ^a   Jafari, Amir ^a   Wang, Jing W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR; SHORT NEUROPEPTIDE F; SHORT NEUROPEPTIDE F RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CONTROL; CONTROLLED STUDY; DROSOPHILA; FACILITATION; FEMALE; FOOD DEPRIVATION; FOOD SEARCH BEHAVIOR; HORMONAL REGULATION; NEUROMODULATION; NONHUMAN; ODOR; OLFACTORY NERVE; OLFACTORY RECEPTOR; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SYNTHESIS INHIBITION; SATIETY; SIGNAL TRANSDUCTION;

EID: 79953276547     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.02.008     Document Type: Article

References (66)

1. A. Arcaro, and M.P. Wymann Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses Biochem. J. 296 1993 297 301 (Pubitemid 23350826)
2. G.S. Barsh, and M.W. Schwartz Genetic approaches to studying energy balance: perception and integration Nat. Rev. Genet. 3 2002 589 600 (Pubitemid 34827133)
3. H.R. Berthoud Multiple neural systems controlling food intake and body weight Neurosci. Biobehav. Rev. 26 2002 393 428
4. M.R. Brown, J.W. Crim, R.C. Arata, H.N. Cai, C. Chun, and P. Shen Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family Peptides 20 1999 1035 1042 (Pubitemid 29424209)
5. M.A. Carlsson, M. Diesner, J. Schachtner, and D.R. Nassel Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits J. Comp. Neurol. 518 2010 3359 3380
6. S.H. Chalasani, S. Kato, D.R. Albrecht, T. Nakagawa, L.F. Abbott, and C.I. Bargmann Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons Nat. Neurosci. 13 2010 615 621
7. P.J. Clyne, C.G. Warr, M.R. Freeman, D. Lessing, J. Kim, and J.R. Carlson A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila Neuron 22 1999 327 338 (Pubitemid 29109666)
8. M.A. Cowley, N. Pronchuk, W. Fan, D.M. Dinulescu, W.F. Colmers, and R.D. Cone Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: Evidence of a cellular basis for the adipostat Neuron 24 1999 155 163 (Pubitemid 29466155)
9. A.M. Dacks, D.S. Green, C.M. Root, A.J. Nighorn, and J.W. Wang Serotonin modulates olfactory processing in the antennal lobe of Drosophila J. Neurogenet. 23 2009 366 377
10. A. Destexhe, and E. Marder Plasticity in single neuron and circuit computations Nature 431 2004 789 795 (Pubitemid 39434068)
11. V.G. Dethier The Hungry Fly: A Physiological Study of the Behavior Associated with Feeding 1976 Harvard University Press Cambridge, MA
12. P.G. Distler, and J. Boeckh Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons J. Comp. Neurol. 383 1997 529 540 (Pubitemid 27290839)
13. B.A. Edgar How flies get their size: genetics meets physiology Nat. Rev. Genet. 7 2006 907 916 (Pubitemid 44871394)
14. G. Feng, V. Reale, H. Chatwin, K. Kennedy, R. Venard, C. Ericsson, K. Yu, P.D. Evans, and L.M. Hall Functional characterization of a neuropeptide F-like receptor from Drosophila melanogaster Eur. J. Neurosci. 18 2003 227 238 (Pubitemid 36999929)
15. A. Gelperin Regulation of feeding Annu. Rev. Entomol. 16 1971 365 378
16. C. Geminard, E.J. Rulifson, and P. Leopold Remote control of insulin secretion by fat cells in Drosophila Cell Metab. 10 2009 199 207
17. K. Gerozissis Brain insulin: regulation, mechanisms of action and functions Cell. Mol. Neurobiol. 23 2003 1 25
18. D.E. Hansel, B.A. Eipper, and G.V. Ronnett Neuropeptide Y functions as a neuroproliferative factor Nature 410 2001 940 944 (Pubitemid 32335840)
19. R.S. Hewes, and P.H. Taghert Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome Genome Res. 11 2001 1126 1142 (Pubitemid 32834556)
20. R. Ignell, C.M. Root, R.T. Birse, J.W. Wang, D.R. Nassel, and A.M. Winther Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila Proc. Natl. Acad. Sci. USA 106 2009 13070 13075
21. M.J. Krashes, S. DasGupta, A. Vreede, B. White, J.D. Armstrong, and S. Waddell A neural circuit mechanism integrating motivational state with memory expression in Drosophila Cell 139 2009 416 427
22. K.S. Lee, K.H. You, J.K. Choo, Y.M. Han, and K. Yu Drosophila short neuropeptide F regulates food intake and body size J. Biol. Chem. 279 2004 50781 50789 (Pubitemid 40017816)
23. K.S. Lee, O.Y. Kwon, J.H. Lee, K. Kwon, K.J. Min, S.A. Jung, A.K. Kim, K.H. You, M. Tatar, and K. Yu Drosophila short neuropeptide F signalling regulates growth by ERK-mediated insulin signalling Nat. Cell Biol. 10 2008 468 475
24. S.J. Leevers, D. Weinkove, L.K. MacDougall, E. Hafen, and M.D. Waterfield The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth EMBO J. 15 1996 6584 6594 (Pubitemid 26413791)
25. E.Z. Macosko, N. Pokala, E.H. Feinberg, S.H. Chalasani, R.A. Butcher, J. Clardy, and C.I. Bargmann A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans Nature 458 2009 1171 1175
26. M. Mathieu, G. Tagliafierro, F. Bruzzone, and M. Vallarino Neuropeptide tyrosine-like immunoreactive system in the brain, olfactory organ and retina of the zebrafish, Danio rerio, during development Brain Res. Dev. Brain Res. 139 2002 255 265 (Pubitemid 35453912)
27. C.M. Mayer, and D.D. Belsham Insulin directly regulates NPY and AgRP gene expression via the MAPK MEK/ERK signal transduction pathway in mHypoE-46 hypothalamic neurons Mol. Cell. Endocrinol. 307 2009 99 108
28. A. Mousley, G. Polese, N.J. Marks, and H.L. Eisthen Terminal nerve-derived neuropeptide y modulates physiological responses in the olfactory epithelium of hungry axolotls (Ambystoma mexicanum) J. Neurosci. 26 2006 7707 7717 (Pubitemid 44315190)
29. M. Murakami, H. Kashiwadani, Y. Kirino, and K. Mori State-dependent sensory gating in olfactory cortex Neuron 46 2005 285 296 (Pubitemid 40545783)
30. D.R. Nassel, L.E. Enell, J.G. Santos, C. Wegener, and H.A. Johard A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions BMC Neurosci. 9 2008 90
31. M.N. Nitabach, Y. Wu, V. Sheeba, W.C. Lemon, J. Strumbos, P.K. Zelensky, B.H. White, and T.C. Holmes Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods J. Neurosci. 26 2006 479 489 (Pubitemid 43237112)
32. S.R. Olsen, and R.I. Wilson Lateral presynaptic inhibition mediates gain control in an olfactory circuit Nature 452 2008 956 960 (Pubitemid 351589620)
33. S.R. Olsen, V. Bhandawat, and R.I. Wilson Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe Neuron 54 2007 89 103 (Pubitemid 46498691)
34. C.M. Root, K. Masuyama, D.S. Green, L.E. Enell, D.R. Nassel, C.H. Lee, and J.W. Wang A presynaptic gain control mechanism fine-tunes olfactory behavior Neuron 59 2008 311 321 (Pubitemid 352033691)
35. C.M. Root, J.L. Semmelhack, A.M. Wong, J. Flores, and J.W. Wang Propagation of olfactory information in Drosophila Proc. Natl. Acad. Sci. USA 104 2007 11826 11831 (Pubitemid 47175097)
36. E.J. Rulifson, S.K. Kim, and R. Nusse Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes Science 296 2002 1118 1120 (Pubitemid 34517128)
37. S. Sachse, and C.G. Galizia Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study J. Neurophysiol. 87 2002 1106 1117 (Pubitemid 34670872)
38. M.W. Schwartz, A.J. Sipols, J.L. Marks, G. Sanacora, J.D. White, A. Scheurink, S.E. Kahn, D.G. Baskin, S.C. Woods, and D.P. Figlewicz Inhibition of hypothalamic neuropeptide Y gene expression by insulin Endocrinology 130 1992 3608 3616
39. J.L. Semmelhack, and J.W. Wang Select Drosophila glomeruli mediate innate olfactory attraction and aversion Nature 459 2009 218 223
40. Y. Shang, A. Claridge-Chang, L. Sjulson, M. Pypaert, and G. Miesenbock Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe Cell 128 2007 601 612 (Pubitemid 46198891)
41. R.F. Stocker, M.C. Lienhard, A. Borst, and K.F. Fischbach Neuronal architecture of the antennal lobe in Drosophila melanogaster Cell Tissue Res. 262 1990 9 34 (Pubitemid 20308096)
42. R.F. Stocker, G. Heimbeck, N. Gendre, and J.S. de Belle Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons J. Neurobiol. 32 1997 443 456 (Pubitemid 27172931)
43. C.J. Vlahos, W.F. Matter, K.Y. Hui, and R.F. Brown A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4- one (LY294002) J. Biol. Chem. 269 1994 5241 5248
44. L.B. Vosshall, and R.F. Stocker Molecular architecture of smell and taste in Drosophila Annu. Rev. Neurosci. 30 2007 505 533 (Pubitemid 47218766)
45. L.B. Vosshall, H. Amrein, P.S. Morozov, A. Rzhetsky, and R. Axel A spatial map of olfactory receptor expression in the Drosophila antenna Cell 96 1999 725 736 (Pubitemid 29122814)
46. L.B. Vosshall, A.M. Wong, and R. Axel An olfactory sensory map in the fly brain Cell 102 2000 147 159
47. J.W. Wang, A.M. Wong, J. Flores, L.B. Vosshall, and R. Axel Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain Cell 112 2003 271 282 (Pubitemid 36144115)
48. D. Weinkove, T.P. Neufeld, T. Twardzik, M.D. Waterfield, and S.J. Leevers Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor Curr. Biol. 9 1999 1019 1029 (Pubitemid 29456170)
49. S.C. Woods, R.J. Seeley, D. Porte Jr.; and M.W. Schwartz Signals that regulate food intake and energy homeostasis Science 280 1998 1378 1383 (Pubitemid 28264819)
50. Q. Wu, T. Wen, G. Lee, J.H. Park, H.N. Cai, and P. Shen Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system Neuron 39 2003 147 161 (Pubitemid 36830955)
51. Q. Wu, Z. Zhao, and P. Shen Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems Nat. Neurosci. 8 2005 1350 1355 (Pubitemid 41630423)
52. Chiang, H.C.; Wang, L.; Xie, Z.; Yau, A.; and Zhong, Y. (2010). PI3 kinase signaling is involved in Abeta-induced memory loss in Drosophila. Proc. Natl. Acad. Sci. USA 107, 7060-7065.
53. Couto, A.; Alenius, M.; and Dickson, B.J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547. (Pubitemid 41219592)
54. DiAngelo, J.R.; and Birnbaum, M.J. (2009). Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol. Cell. Biol. 29, 6341-6352.
55. DiAngelo, J.R.; Bland, M.L.; Bambina, S.; Cherry, S.; and Birnbaum, M.J. (2009). The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc. Natl. Acad. Sci. USA 106, 20853-20858.
56. Fishilevich, E.; and Vosshall, L.B. (2005). Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553. (Pubitemid 41219593)
57. Kreher, S.A.; Kwon, J.Y.; and Carlson, J.R. (2005). The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445-456. (Pubitemid 40616888)
58. Lai, S.L.; and Lee, T. (2006). Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703-709. (Pubitemid 44012270)
59. Lai, S.L.; Awasaki, T.; Ito, K.; and Lee, T. (2008). Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135, 2883-2893.
60. Lee, K.S.; Kwon, O.Y.; Lee, J.H.; Kwon, K.; Min, K.J.; Jung, S.A.; Kim, A.K.; You, K.H.; Tatar, M.; and Yu, K. (2008). Drosophila short neuropeptide F signaling regulates growth by ERK-mediated insulin signaling. Nat. Cell Biol. 10, 468-475.
61. Longo, N.; Shuster, R.C.; Griffin, L.D.; Langley, S.D.; and Elsas, L.J. (1992). Activation of insulin receptor signaling by a single amino acid substitution in the transmembrane domain. J. Biol. Chem. 267, 12416-12419.
62. Nitabach, M.N.; Wu, Y.; Sheeba, V.; Lemon, W.C.; Strumbos, J.; Zelensky, P.K.; White, B.H.; and Holmes, T.C. (2006). Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26, 479-489. (Pubitemid 43237112)
63. Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
64. Root, C.M.; Masuyama, K.; Green, D.S.; Enell, L.E.; Nassel, D.R.; Lee, C.H.; and Wang, J.W. (2008). A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311-321. (Pubitemid 352033691)
65. Stocker, R.F.; Heimbeck, G.; Gendre, N.; and de Belle, J.S. (1997). Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443-456. (Pubitemid 27172931)
66. Wang, J.W.; Wong, A.M.; Flores, J.; Vosshall, L.B.; and Axel, R. (2003). Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282. (Pubitemid 36144115)