The Insulin/PI 3-Kinase Pathway Regulates Salt Chemotaxis Learning in Caenorhabditis elegans

Neuron

Volumn 51, Issue 5, 2006, Pages 613-625

  Tomioka, Masahiro ^a   Adachi, Takeshi ^a   Suzuki, Hiroshi ^b   Kunitomo, Hirofumi ^a   Schafer, William R ^b   Iino, Yuichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

MOLNEURO; SIGNALING; SYSNEURO

Indexed keywords

CHEMOATTRACTANT; INSULIN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SODIUM CHLORIDE; SOMATOMEDIN C RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CAENORHABDITIS ELEGANS; CHEMOTAXIS; CONTROLLED STUDY; INTERNEURON; LEARNING; MUTANT; NERVE CELL; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; REGULATORY MECHANISM; SENSORY NERVE CELL; SEQUENCE HOMOLOGY; STARVATION; SYNAPSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHEMOTAXIS; IMMUNOHISTOCHEMISTRY; INSULIN; INTERNEURONS; LEARNING; MUTATION; NEURONS, AFFERENT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

EID: 33748068817     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.07.024     Document Type: Article

References (57)

1. Abbott M.A., Wells D.G., and Fallon J.R. The insulin receptor tyrosine kinase substrate p58/53 and the insulin receptor are components of CNS synapses. J. Neurosci. 19 (1999) 7300-7308
2. Adler C.E., Fetter R.D., and Bargmann C.I. UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat. Neurosci. 9 (2006) 511-518
3. Apfeld J., and Kenyon C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell 95 (1998) 199-210
4. Bargmann C.I., and Mori I. Chemotaxis and thermotaxis. In: Riddle D.L., Blumenthal T., Meyer B.J., and Priess J.R. (Eds). C. elegans II (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 717-738
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
6. Chang S., Johnston Jr. R.J., and Hobert O. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17 (2003) 2123-2137
7. Chang C., Adler C.E., Krause M., Clark S.G., Gertler F.B., Tessier-Lavigne M., and Bargmann C.I. MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin. Curr. Biol. 16 (2006) 854-862
8. Chuang C.F., and Bargmann C.I. A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev. 19 (2005) 270-281
9. Colbert H.A., and Bargmann C.I. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14 (1995) 803-812
10. Colbert H.A., Smith T.L., and Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17 (1997) 8259-8269
11. Devaskar S.U., Giddings S.J., Rajakumar P.A., Carnaghi L.R., Menon R.K., and Zahm D.S. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J. Biol. Chem. 269 (1994) 8445-8454
12. Faumont S., Miller A.C., and Lockery S.R. Chemosensory behavior of semi-restrained Caenorhabditis elegans. J. Neurobiol. 65 (2005) 171-178
13. Hawasli A.H., Saifee O., Liu C., Nonet M.L., and Crowder C.M. Resistance to volatile anesthetics by mutations enhancing excitatory neurotransmitter release in Caenorhabditis elegans. Genetics 168 (2004) 831-843
14. Hilliard M.A., Apicella A.J., Kerr R., Suzuki H., Bazzicalupo P., and Schafer W.R. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J. 24 (2005) 63-72
15. Hirotsu T., Saeki S., Yamamoto M., and Iino Y. The Ras-MAPK pathway is important for olfaction in Caenorhabditis elegans. Nature 404 (2000) 289-293
16. Hobert O. Behavioral plasticity in C. elegans: paradigms, circuits, genes. J. Neurobiol. 54 (2003) 203-223
17. Hukema R.K., Rademakers S., Dekkers M.P., Burghoorn J., and Jansen G. Antagonistic sensory cues generate gustatory plasticity in Caenorhabditis elegans. EMBO J. 25 (2006) 312-322
18. Ishihara T., Iino Y., Mohri A., Mori I., Gengyo-Ando K., Mitani S., and Katsura I. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109 (2002) 639-649
19. Jansen G., Weinkove D., and Plasterk R.H. The G-protein gamma subunit gpc-1 of the nematode C.elegans is involved in taste adaptation. EMBO J. 21 (2002) 986-994
20. 2+ pool and of neuropeptide secretion. Nature 385 (1997) 343-346
21. Kaba H., Hayashi Y., Higuchi T., and Nakanishi S. Induction of an olfactory memory by the activation of a metabotropic glutamate receptor. Science 265 (1994) 262-264
22. Kass J., Jacob T.C., Kim P., and Kaplan J.M. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J. Neurosci. 21 (2001) 9265-9272
23. Kerr R., Lev-Ram V., Baird G., Vincent P., Tsien R.Y., and Schafer W.R. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26 (2000) 583-594
24. Kimura K.D., Tissenbaum H.A., Liu Y., and Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277 (1997) 942-946
25. L'Etoile N.D., Coburn C.M., Eastham J., Kistler A., Gallegos G., and Bargmann C.I. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36 (2002) 1079-1089
26. Lackner M.R., Nurrish S.J., and Kaplan J.M. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24 (1999) 335-346
27. Li W., Kennedy S.G., and Ruvkun G. daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev. 17 (2003) 844-858
28. Libina N., Berman J.R., and Kenyon C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115 (2003) 489-502
29. Lin C.H., Yeh S.H., Lu K.T., Leu T.H., Chang W.C., and Gean P.W. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31 (2001) 841-851
30. Man H.Y., Lin J.W., Ju W.H., Ahmadian G., Liu L., Becker L.E., Sheng M., and Wang Y.T. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25 (2000) 649-662
31. Man H.Y., Wang Q., Lu W.Y., Ju W., Ahmadian G., Liu L., D'Souza S., Wong T.P., Taghibiglou C., Lu J., et al. Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38 (2003) 611-624
32. Miller A.C., Thiele T.R., Faumont S., Moravec M.L., and Lockery S.R. Step-response analysis of chemotaxis in Caenorhabditis elegans. J. Neurosci. 25 (2005) 3369-3378
33. Mori I., and Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376 (1995) 344-348
34. Mohri A., Kodama E., Kimura K.D., Koike M., Mizuno T., and Mori I. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 169 (2005) 1437-1450
35. Murakami H., Bessinger K., Hellmann J., and Murakami S. Aging-dependent and -independent modulation of associative learning behavior by insulin/insulin-like growth factor-1 signal in Caenorhabditis elegans. J. Neurosci. 25 (2005) 10894-10904
36. Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., and Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20 (2002) 87-90
37. Nonet M.L., Saifee O., Zhao H., Rand J.B., and Wei L. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 18 (1998) 70-80
38. Paradis S., Ailion M., Toker A., Thomas J.H., and Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 13 (1999) 1438-1452
39. Pierce S.B., Costa M., Wisotzkey R., Devadhar S., Homburger S.A., Buchman A.R., Ferguson K.C., Heller J., Platt D.M., Pasquinelli A.A., et al. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 15 (2001) 672-686
40. Pierce-Shimomura J.T., Faumont S., Gaston M.R., Pearson B.J., and Lockery S.R. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 410 (2001) 694-698
41. Richmond J.E., Davis W.S., and Jorgensen E.M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2 (1999) 959-964
42. Riddle D.L., and Albert P.S. Genetic and environmental regulation of Dauer larva development. In: Riddle D.L., Blumenthal T., Meyer B.J., and Priess J.R. (Eds). C. elegans II (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 739-768
43. Saeki S., Yamamoto M., and Iino Y. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J. Exp. Biol. 204 (2001) 1757-1764
44. Scott B.A., Avidan M.S., and Crowder C.M. Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science 296 (2002) 2388-2391
45. Shi S.H., Jan L.Y., and Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112 (2003) 63-75
46. Skeberdis V.A., Lan J., Zheng X., Zukin R.S., and Bennett M.V. Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. USA 98 (2001) 3561-3566
47. Solari F., Bourbon-Piffaut A., Masse I., Payrastre B., Chan A.M., and Billaud M. The human tumour suppressor PTEN regulates longevity and dauer formation in Caenorhabditis elegans. Oncogene 24 (2005) 20-27
48. + channels in hypothalamic neurons of lean, but not obese rats. Nat. Neurosci. 3 (2000) 757-758
49. Spehr M., Wetzel C.H., Hatt H., and Ache B.W. 3-phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron 33 (2002) 731-739
50. Suzuki H., Kerr R., Bianchi L., Frokjaer-Jensen C., Slone D., Xue J., Gerstbrein B., Driscoll M., and Schafer W.R. In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39 (2003) 1005-1017
51. Vigh J., Li G.L., Hull C., and von Gersdorff H. Long-Term plasticity mediated by mGluR1 at a retinal reciprocal synapse. Neuron 46 (2005) 469-482
52. Wei L.T., Matsumoto H., and Rhoads D.E. Release of immunoreactive insulin from rat brain synaptosomes under depolarizing conditions. J. Neurochem. 54 (1990) 1661-1665
53. Werner E.D., Lee J., Hansen L., Yuan M., and Shoelson S.E. Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302. J. Biol. Chem. 279 (2004) 35298-35305
54. White J.G., Southgate E., Thomson J.N., and Brenner S. The structure of the nervous system of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314 (1986) 1-340
55. Wu Q., Zhao Z., and Shen P. Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems. Nat. Neurosci. 8 (2005) 1350-1355
56. Zahn T.R., Angleson J.K., MacMorris M.A., Domke E., Hutton J.F., Schwartz C., and Hutton J.C. Dense core vesicle dynamics in Caenorhabditis elegans neurons and the role of kinesin UNC-104. Traffic 5 (2004) 544-559
57. Zhao W.Q., Chen H., Quon M.J., and Alkon D.L. Insulin and the insulin receptor in experimental models of learning and memory. Eur. J. Pharmacol. 490 (2004) 71-81