Insulin signalling in mushroom body neurons regulates feeding behaviour in drosophila larvae

Journal of Experimental Biology

Volumn 215, Issue 15, 2012, Pages 2696-2702

  Zhao, Xiao Li ^a   Campos, Ana Regina ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Drosophila; Fat body; Feeding; Growth; Insulin

Indexed keywords

INSULIN;

ANIMAL; ARTICLE; CELL PROLIFERATION; CYTOLOGY; DROSOPHILA MELANOGASTER; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; INNERVATION; LARVA; METABOLISM; MUSHROOM BODY; NERVE CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; FEEDING BEHAVIOR; INSULIN; LARVA; MUSHROOM BODIES; NEURONS; SIGNAL TRANSDUCTION;

BASIDIOMYCOTA;

EID: 84863923115     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.066969     Document Type: Article

References (65)

1. Acebes, A., Martin-Pena, A., Chevalier, V. and Ferrus, A. (2011). Synapse loss in olfactory local interneurons modifies perception. J. Neurosci. 31, 2734-2745.
2. Al-Anzi, B., Sapin, V., Waters, C., Zinn, K., Wyman, R. J. and Benzer, S. (2009). Obesity-blocking neurons in Drosophila. Neuron 63, 329-341.
3. Atabakhsh, E., Bryce, D. M., Lefebvre, K. J. and Schild-Poulter, C. (2009). RanBPM has proapoptotic activities that regulate cell death pathways in response to DNA damage. Mol. Cancer Res.7, 1962-1972.
4. Bai, D., Chen, H. and Huang, B. R. (2003). RanBPM is a novel binding protein for p75NTR. Biochem. Biophys. Res. Commun. 309, 552-557.
5. Belgacem, Y. H. and Martin, J. R. (2002). Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila. Proc. Natl. Acad. Sci. USA 99, 15154-15158.
6. Belgacem, Y. H. and Martin, J. R. (2006). Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. J. Neurobiol. 66, 19-32.
7. Bosco, D., Fava, A., Plastino, M., Montalcini, T. and Pujia, A. (2011). Possible implications of insulin resistance and glucose metabolism in Alzheimer's disease pathogenesis. J. Cell. Mol. Med. 15, 1807-1821.
8. Britton, J. S. and Edgar, B. A. (1998). Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125, 2149-2158.
9. Britton, J. S., Lockwood, W. K., Li, L., Cohen, S. M. and Edgar, B. A. (2002). Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2, 239-249.
10. Broughton, S. J., Piper, M. D., Ikeya, T., Bass, T. M., Jacobson, J., Driege, Y., Martinez, P., Hafen, E., Withers, D. J., Leevers, S. J. et al. (2005). Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad. Sci. USA 102, 3105-3110.
11. Brunkhorst, A., Karlén, M., Shi, J., Mikolajczyk, M., Nelson, M. A., Metsis, M. and Hermanson, O. (2005). A specific role for the TFIID subunit TAF4 and RanBPM in neural progenitor differentiation. Mol. Cell. Neurosci. 29, 250-258.
12. Busto, G. U., Cervantes-Sandoval, I. and Davis, R. L. (2010). Olfactory learning in Drosophila. Physiology (Bethesda) 25, 338-346.
13. Chang, Y., Paramasivam, M., Girgenti, M. J., Walikonis, R. S., Bianchi, E. and LoTurco, J. J. (2010). RanBPM regulates the progression of neuronal precursors through M-phase at the surface of the neocortical ventricular zone. Dev. Neurobiol. 70, 1-15.
14. Chell, J. M. and Brand, A. H. (2010). Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143, 1161-1173.
15. 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.
16. Chiu, S. L. and Cline, H. T. (2010). Insulin receptor signaling in the development of neuronal structure and function. Neural Dev. 5, 7.
17. Chiu, S. L., Chen, C. M. and Cline, H. T. (2008). Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58, 708-719.
18. Connolly, J. B., Roberts, I. J., Armstrong, J. D., Kaiser, K., Forte, M., Tully, T. and O'Kane, C. J. (1996). Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104-2107.
19. Corl, A. B., Rodan, A. R. and Heberlein, U. (2005). Insulin signaling in the nervous system regulates ethanol intoxication in Drosophila melanogaster. Nat. Neurosci. 8, 18-19.
20. de Belle, J. S. and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695.
21. Dou, J. T., Chen, M., Dufour, F., Alkon, D. L. and Zhao, W. Q. (2005). Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn. Mem. 12, 646-655.
22. Géminard, C., Rulifson, E. J. and Léopold, P. (2009). Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 10, 199-207.
23. Gong, X., Ye, W., Zhou, H., Ren, X., Li, Z., Zhou, W., Wu, J., Gong, Y., Ouyang, Q., Zhao, X. et al. (2009). RanBPM is an acetylcholinesterase- interacting protein that translocates into the nucleus during apoptosis. Acta Biochim. Biophys. Sin. 41, 883- 891.
24. Haase, A., Nordmann, C., Sedehizade, F., Borrmann, C. and Reiser, G. (2008). RanBPM, a novel interaction partner of the brain-specific protein p42(IP4)/centaurin alpha-1. J. Neurochem. 105, 2237-2248.
25. Hafizi, S., Gustafsson, A., Stenhoff, J. and Dahlbäck, B. (2005). The Ran binding protein RanBPM interacts with Axl and Sky receptor tyrosine kinases. Int. J. Biochem. Cell Biol. 37, 2344-2356.
26. Hassan, J., Iyengar, B., Scantlebury, N., Rodriguez Moncalvo, V. and Campos, A. R. (2005). Photic input pathways that mediate the Drosophila larval response to light and circadian rhythmicity are developmentally related but functionally distinct. J. Comp. Neurol. 481, 266-275.
27. Heisenberg, M., Borst, A., Wagner, S. and Byers, D. (1985). Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1-30.
28. Hong, S. T., Bang, S., Hyun, S., Kang, J., Jeong, K., Paik, D., Chung, J. and Kim, J. (2008). cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila. Nature 454, 771-775.
29. Honjo, K. and Furukubo-Tokunaga, K. (2005). Induction of cAMP response elementbinding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae. J. Neurosci. 25, 7905-7913.
30. Honjo, K. and Furukubo-Tokunaga, K. (2009). Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. J. Neurosci. 29, 852-862.
31. Iijima, K., Zhao, L., Shenton, C. and Iijima-Ando, K. (2009). Regulation of energy stores and feeding by neuronal and peripheral CREB activity in Drosophila. PLoS ONE 4, e8498.
32. Ikeya, T., Galic, M., Belawat, P., Nairz, K. and Hafen, E. (2002). Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12, 1293-1300.
33. Johard, H. A., Enell, L. E., Gustafsson, E., Trifilieff, P., Veenstra, J. A. and Nässel, D. R. (2008). Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J. Comp. Neurol. 507, 1479-1496.
34. Joiner, W. J., Crocker, A., White, B. H. and Sehgal, A. (2006). Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757-760.
35. Jones, M. A., Gargano, J. W., Rhodenizer, D., Martin, I., Bhandari, P. and Grotewiel, M. (2009). A forward genetic screen in Drosophila implicates insulin signaling in age-related locomotor impairment. Exp. Gerontol. 44, 532-540.
36. Kapogiannis, D. and Mattson, M. P. (2011). Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neurol. 10, 187-198.
37. Karcavich, R. and Doe, C. Q. (2005). Drosophila neuroblast 7-3 cell lineage: a model system for studying programmed cell death, Notch/Numb signaling, and sequential specification of ganglion mother cell identity. J. Comp. Neurol. 481, 240-251.
38. Kim, T., Kim, S., Yun, H. M., Chung, K. C., Han, Y. S., Shin, H. S. and Rhim, H. (2009). Modulation of Ca(v)3.1 T-type Ca2+ channels by the ran binding protein RanBPM. Biochem. Biophys. Res. Commun. 378, 15-20.
39. Kitamoto, T. (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92.
40. Kramer, J. M., Davidge, J. T., Lockyer, J. M. and Staveley, B. E. (2003). Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev. Biol. 3, 5.
41. Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D. and Waddell, S. (2009). A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-427.
42. Lee, K. S., You, K. H., Choo, J. K., Han, Y. M. and Yu, K. (2004). Drosophila short neuropeptide F regulates food intake and body size. J. Biol. Chem. 279, 50781-50789.
43. Leevers, S. J., Weinkove, D., MacDougall, L. K., Hafen, E. and Waterfield, M. D. (1996). The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15, 6584-6594.
44. Margulies, C., Tully, T. and Dubnau, J. (2005). Deconstructing memory in Drosophila. Curr. Biol. 15, R700-R713.
45. Martin, J. R., Ernst, R. and Heisenberg, M. (1998). Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn. Mem. 5, 179-191.
46. Menon, R. P., Gibson, T. J. and Pastore, A. (2004). The C terminus of fragile X mental retardation protein interacts with the multi-domain Ran-binding protein in the microtubule-organising centre. J. Mol. Biol. 343, 43-53.
47. Mikolajczyk, M., Shi, J., Vaillancourt, R. R., Sachs, N. A. and Nelson, M. (2003). The cyclin-dependent kinase 11(p46) isoform interacts with RanBPM. Biochem. Biophys. Res. Commun. 310, 14-18.
48. Murrin, L. C. and Talbot, J. N. (2007). RanBPM, a scaffolding protein in the immune and nervous systems. J. Neuroimmune Pharmacol. 2, 290-295.
49. Nässel, D. R. and Winther, A. M. (2010). Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92, 42-104.
50. Oda, S., Tomioka, M. and Iino, Y. (2011). Neuronal plasticity regulated by the insulinlike signaling pathway underlies salt chemotaxis learning in Caenorhabditis elegans. J. Neurophysiol. 106, 301-308.
51. Pauls, D., Selcho, M., Gendre, N., Stocker, R. F. and Thum, A. S. (2010). Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J. Neurosci. 30, 10655-10666.
52. Rodriguez Moncalvo, V. G. and Campos, A. R. (2009). Role of serotonergic neurons in the Drosophila larval response to light. BMC Neurosci. 10, 66.
53. Root, C. M., Ko, K. I., Jafari, A. and Wang, J. W. (2011). Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145, 133-144.
54. Rulifson, E. J., Kim, S. K. and Nusse, R. (2002). Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296, 1118-1120.
55. Scantlebury, N., Zhao, X. L., Rodriguez Moncalvo, V. G., Camiletti, A., Zahanova, S., Dineen, A., Xin, J. H. and Campos, A. R. (2010). The Drosophila gene RanBPM functions in the mushroom body to regulate larval behavior. PLoS ONE 5, e10652.
56. Serway, C. N., Kaufman, R. R., Strauss, R. and de Belle, J. S. (2009). Mushroom bodies enhance initial motor activity in Drosophila. J. Neurogenet. 23, 173-184.
57. Sousa-Nunes, R., Yee, L. L. and Gould, A. P. (2011). Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471, 508-512.
58. Spéder, P., Liu, J. and Brand, A. H. (2011). Nutrient control of neural stem cells. Curr. Opin. Cell Biol. 23, 724-729.
59. Teleman, A. A. (2010). Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem. J. 425, 13-26.
60. White, B., Osterwalder, T. and Keshishian, H. (2001). Molecular genetic approaches to the targeted suppression of neuronal activity. Curr. Biol. 11, R1041-R1053.
61. Wu, Q., Zhao, Z. and Shen, P. (2005a). Regulation of aversion to noxious food by Drosophila neuropeptide Y-and insulin-like systems. Nat. Neurosci. 8, 1350-1355.
62. Wu, Q., Zhang, Y., Xu, J. and Shen, P. (2005b). Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc. Natl. Acad. Sci. USA 102, 13289-13294.
63. Yin, Y. X., Sun, Z. P., Huang, S. H., Zhao, L., Geng, Z. and Chen, Z. Y. (2010). RanBPM contributes to TrkB signaling and regulates brain-derived neurotrophic factor-induced neuronal morphogenesis and survival. J. Neurochem. 114, 110-121.
64. Zars, T., Fischer, M., Schulz, R. and Heisenberg, M. (2000). Localization of a shortterm memory in Drosophila. Science 288, 672-675.
65. Zinke, I., Kirchner, C., Chao, L. C., Tetzlaff, M. T. and Pankratz, M. J. (1999). Suppression of food intake and growth by amino acids in Drosophila: The role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 126, 5275-5284.