A nucleostemin family GTPase, NS3, acts in serotonergic neurons to regulate insulin signaling and control body size

Genes and Development

Volumn 22, Issue 14, 2008, Pages 1877-1893

  Kaplan, Daniel D ^a,b   Zimmermann, Gregor ^a   Suyama, Kaye ^a   Meyer, Tobias ^b   Scott, Matthew P ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Growth; Insulin; Neurons; Nucleostemin; Serotonin; Size

Indexed keywords

GUANOSINE TRIPHOSPHATASE; INSULIN; NUCLEOSTEMIN 3; NUCLEOSTEMIN FAMILY GUANOSINE TRIPHOSPHATASE; SEROTONIN;

ARTICLE; BODY SIZE; CELL SIZE; DROSOPHILA; GROWTH DISORDER; GROWTH REGULATION; INSULIN RELEASE; LARVAL DEVELOPMENT; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY SIZE; CELL COMMUNICATION; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOBLOTTING; IN SITU HYBRIDIZATION, FLUORESCENCE; INSULIN; MALE; MICROINJECTIONS; MUTATION; NEURONS; NUCLEAR PROTEINS; RECEPTOR, INSULIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTONIN; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 47549108079     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1670508     Document Type: Article

References (64)

1. Arquier, N., Geminard, C., Bourouis, M., Jarretou, G., Honegger, B., Paix, A., and Leopold, P. 2008. Drosophila ALS regulates growth and metabolism through functional interaction with insulin-like peptides. Cell Metab. 7: 333-338.
2. Ashburner, M. and Thompson Jr., J.N. 1978. The laboratory culture of Drosophila. In The genetics and biology of Drosophila (eds. M. Ashburner and T.R.F. Wright), Vol. 2a, pp. 1-109. Academic Press, Inc., New York.
3. Baker, K.D. and Thummel, C.S. 2007. Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab. 6: 257-266.
4. Bohni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B.F., Beckingham, K., and Hafen, E. 1999. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865-875.
5. Bourne, H.R., Sanders, D.A., and McCormick, F. 1991. The GTPase superfamily: Conserved structure and molecular mechanism. Nature 349: 117-127.
6. Brand, A.H. and Perrimon, N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phe-notypes. Development 118: 401-415.
7. Chen, C., Jack, J., and Garofalo, R.S. 1996. The Drosophila insulin receptor is required for normal growth. Endocrinology 137: 846-856.
8. Cherbas, L., Hu, X., Zhimulev, I., Belyaeva, E., and Cherbas, P. 2003. EcR isoforms in Drosophila: Testing tissue-specific requirements by targeted blockade and rescue. Development 130: 271-284.
9. Cole, S.H., Carney, G.E., McClung, C.A., Willard, S.S., Taylor, B.J., and Hirsh, J. 2005. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: Distinct roles for neural tyramine and octopamine in female fertility. J. Biol. Chem. 280: 14948-14955.
10. Colombani, J., Raisin, S., Pantalacci, S., Radimerski, T., Montagne, J., and Leopold, P. 2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
11. Conlon, I. and Raff, M. 1999. Size control in animal development. Cell 96: 235-244.
12. Dieguez, C. and Casanueva, F.F. 1995. Influence of metabolic substrates and obesity on growth hormone secretion. Trends Endocrinol. Metab. 6: 55-59.
13. Dietzl, G., Chen, D., Schnorrer, F., Su, K.C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
14. Edgar, B.A. 2006. How flies get their size: Genetics meets physiology. Nat. Rev. Genet. 7: 907-916.
15. Feldman, J.M. and Lebovitz, H.E. 1970. Serotonin inhibition of in vitro insulin release from golden hamster pancreas. Endocrinology 86: 66-70.
16. Friggi-Grelin, F., Coulom, H., Meller, M., Gomez, D., Hirsh, J., and Birman, S. 2003. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54: 618-627.
17. Gagliardino, J.J., Zieher, L.M., Iturriza, F.C., Hernandez, R.E., and Rodriguez, R.R. 1971. Insulin release and glucose changes induced by serotonin. Horm. Metab. Res. 3: 145-150.
18. Galloni, M. and Edgar, B.A. 1999. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster. Development 126: 2365-2375.
19. Golic, K.G. and Lindquist, S. 1989. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59: 499-509.
20. Hedges, J., West, M., and Johnson, A.W. 2005. Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 24: 567-579.
21. Huang, X., Suyama, K., Buchanan, J., Zhu, A.J., and Scott, M.P. 2005. A Drosophila model of the Niemann-Pick type C lysosome storage disease: dnpc1a is required for molting and sterol homeostasis. Development 132: 5115-5124.
22. 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.
23. Kallstrom, G., Hedges, J., and Johnson, A. 2003. The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 23: 4344-4355.
24. Kenyon, C., Chang, J., Gensch, E., Rudner, A., and Tabtiang, R. 1993. A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
25. Kim, S.K. and Rulifson, E.J. 2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora car-diaca cells. Nature 431: 316-320.
26. Kosman, D., Mizutani, C.M., Lemons, D., Cox, W.G., McGinnis, W., and Bier, E. 2004. Multiplex detection of RNA expression in Drosophila embryos. Science 305: 846. doi: 10.1126/science.1099247.
27. Lambertsson, A. 1998. The minute genes in Drosophila and their molecular functions. Adv. Genet. 38: 69-134.
28. 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.
29. Li, H., Chaney, S., Roberts, I.J., Forte, M., and Hirsh, J. 2000. Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr. Biol. 10: 211-214.
30. Melcher, C. and Pankratz, M.J. 2005. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol. 3: e305. doi: 10.1371/journal.pbio.0030305.
31. Melcher, C., Bader, R., and Pankratz, M.J. 2007. Amino acids, taste circuits, and feeding behavior in Drosophila: Towards understanding the psychology of feeding in flies and man. J. Endocrinol. 192: 467-472.
32. Monastirioti, M. 1999. Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc. Res. Tech. 45: 106-121.
33. Morton, G.J., Cummings, D.E., Baskin, D.G., Barsh, G.S., and Schwartz, M.W. 2006. Central nervous system control of food intake and body weight. Nature 443: 289-295.
34. Neckameyer, W.S., Coleman, C.M., Eadie, S., and Goodwin, S.F. 2007. Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster. Genes Brain Behav. 6: 756-769.
35. Ng, M., Roorda, R.D., Lima, S.Q., Zemelman, B.V., Morcillo, P., and Miesenbock, G. 2002. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36: 463-474.
36. Oldham, S. and Hafen, E. 2003. Insulin/IGF and target of rapamycin signaling: A TOR de force in growth control. Trends Cell Biol. 13: 79-85.
37. Orosco, M., Rouch, C., and Gerozissis, K. 2000. Activation of hypothalamic insulin by serotonin is the primary event of the insulin-serotonin interaction involved in the control of feeding. Brain Res. 872: 64-70.
38. Peschke, E., Peschke, D., Hammer, T., and Csernus, V. 1997. Influence of melatonin and serotonin on glucose-stimulated insulin release from perifused rat pancreatic islets in vitro. J. Pineal Res. 23: 156-163.
39. Reiling, J.H. and Hafen, E. 2004. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes & Dev. 18: 2879-2892.
40. Reynaud, E.G., Andrade, M.A., Bonneau, F., Ly, T.B., Knop, M., Scheffzek, K., and Pepperkok, R. 2005. Human Lsg1 defines a family of essential GTPases that correlates with the evolution of compartmentalization. BMC Biol. 3: 21. doi: 10.1186/ 1741-7007-3-21.
41. 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.
42. Salvaterra, P.M. and Kitamoto, T. 2001. Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res. Gene Expr. Patterns 1: 73-82.
43. Sanders-Bush, E. and Mayer, S.E. 2001. 5-Hydroxytryptamine (serotonin) receptor agonists and antagonists. In Goodman Gilman's: The pharmacological basis of therapeutics, 10th Ed., pp 281-284. McGraw-Hill, New York.
44. Sarbassov, D.D., Guertin, D.A., Ali, S.M., and Sabatini, D.M. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
45. Schaeffer, H.J. and Sirotkin, A.V. 1997. Melatonin and serotonin regulate the release of insulin-like growth factor-I, oxytocin and progesterone by cultured human granulosa cells. Exp. Clin. Endocrinol. Diabetes 105: 109-112.
46. Schwartz, M.W., Woods, S.C., Porte Jr., D., Seeley, R.J., and Baskin, D.G. 2000. Central nervous system control of food intake. Nature 404: 661-671.
47. Siegmund, T. and Korge, G. 2001. Innervation of the ring gland of Drosophila melanogaster. J. Comp. Neurol. 431: 481-491.
48. Sink, H., Rehm, E.J., Richstone, L., Bulls, Y.M., and Goodman, C.S. 2001. sidestep encodes a target-derived attractant essential for motor axon guidance in Drosophila. Cell 105: 57-67.
49. Sykes, P.A. and Condron, B.G. 2005. Development and sensitivity to serotonin of Drosophila serotonergic varicosities in the central nervous system. Dev. Biol. 286: 207-216.
50. Sze, J.Y., Victor, M., Loer, C., Shi, Y., and Ruvkun, G. 2000. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564.
51. Tabata, T., Schwartz, C., Gustavson, E., Ali, Z., and Kornberg, T.B. 1995. Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 121: 3359-3369.
52. Taghert, P.H., Hewes, R.S., Park, J.H., O'Brien, M.A., Han, M., and Peck, M.E. 2001. Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J. Neurosci. 21: 6673-6686.
53. Telib, M., Raptis, S., Schroder, K.E., and Pfeiffer, E.F. 1968. Serotonin and insulin release in vitro. Diabetologia 4: 253-256.
54. Timmons, L., Becker, J., Barthmaier, P., Fyrberg, C, Shearn, A., and Fyrberg, E. 1997. Green fluorescent protein/β-galactosidase double reporters for visualizing Drosophila gene expression patterns. Dev. Genet. 20: 338-347.
55. Tsai, R.Y. and McKay, R.D. 2002. A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes & Dev. 16: 2991-3003.
56. Valles, A.M. and White, K. 1986. Development of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin. J. Neurosci. 6: 1482-1491.
57. Valles, A.M. and White, K. 1988. Serotonin-containing neurons in Drosophila melanogaster: Development and distribution. J. Comp. Neurol. 268: 414-428.
58. Verdu, J., Buratovich, M.A., Wilder, E.L., and Birnbaum, M.J. 1999. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1: 500-506.
59. Wimberly, B.T., Brodersen, D.E., Clemons Jr., W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C, Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal sub-unit. Nature 407: 327-339.
60. Wu, Q., Wen, T., Lee, G., Park, J.H., Cai, H.N., and Shen, P. 2003. Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39: 147-161.
61. Xiong, W.C., Okano, H., Patel, N.H., Blendy, J.A., and Montell, C. 1994. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes & Dev. 8: 981-994.
62. Zhang, H., Stallock, J.P., Ng, J.C., Reinhard, C, and Neufeld, T.P. 2000. Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes & Dev. 14: 2712-2724.
63. Zimmermann, G., Furlong, E.E., Suyama, K., and Scott, M.P. 2006. Mes2, a MADF-containing transcription factor essential for Drosophila development. Dev. Dyn. 235: 3387-3395.
64. 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.