Altered agonist sensitivity and desensitization of neuronal mGluR1 responses in knock-in mice by a single amino acid substitution at the PKC phosphorylation site

European Journal of Neuroscience

Volumn 20, Issue 4, 2004, Pages 947-955

  Sato, Masaaki ^a   Tabata, Toshihide ^b   Hashimoto, Kouichi ^b   Nakamura, Kenji ^c   Nakao, Kazuki ^d   Katsuki, Motoya ^e   Kitano, Jun ^a   Moriyoshi, Koki ^a   Kano, Masanobu ^b   Nakanishi, Shigetada ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

^c MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^d RIKEN   (Japan)

^e NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Agonist response; Amino acid mutation; Calcium oscillation; Cerebellar Purkinje cell; Metabotropic glutamate receptor

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; ASPARTIC ACID; CALCIUM ION; CATION CHANNEL; INOSITOL TRISPHOSPHATE; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR AGONIST; PROTEIN KINASE C; THREONINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONCENTRATION (PARAMETERS); DESENSITIZATION; FEMALE; FLUOROMETRY; GENE MUTATION; GENE SEQUENCE; MALE; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; STIMULATION; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CHIMERA; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLYCINE; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASE C; RECEPTORS, METABOTROPIC GLUTAMATE; RESORCINOLS;

EID: 4344701963     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03552.x     Document Type: Article

References (44)

1. Aiba, A., Kano, M., Chen, C., Stanton, M.E., Fox, G.D., Herrup, K., Zwingman, T.A. & Tonegawa, S. (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell, 79, 377-388.
2. Ango, F., Prézeau, L., Muller, T., Tu, J.C., Xiao, B., Worley, P.F., Pin, J.P., Bockaert, J. & Fagni, L. (2001) Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer. Nature, 411, 962-965.
3. Batchelor, A.M. & Garthwaite, J. (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature, 385, 74-77.
4. Baude, A., Nusser, Z., Roberts, J.D.B., Mulvihill, E., McIlhinney, R.A.J. & Somogyi, P. (1993) The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron, 11, 771-787.
5. Bliss, T.V.P. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
6. Catania, M.V., Bellomo, M., Di Giorgi-Gerevini, V., Seminara, G., Giuffrida, R., Romeo, R., De Blasi, A. & Nicoletti, F. (2001) Endogenous activation of group-I metabotropic glutamate receptors is required for differentiation and survival of cerebellar Purkinje cells. J. Neurosci., 21, 7664-7673.
7. Choi, D.W. & Rothman, S.M. (1990) The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci., 13, 171-182.
8. 2+ oscillations and waves by oscillating translocation and activation of protein kinase C. Curr. Bio., 11, 1089-1097.
9. Dale, L.B., Babwah, A.V., Bhattacharya, M., Kelvin, D.J. & Ferguson, S.S.G. (2001) Spatial-temporal patterning of metabotropic glutamate receptor-mediated inositol 1,4,5-triphosphate, calcium, and protein kinase C oscillations: protein kinase C-dependent receptor phosphorylation is not required. J. Biol. Chem., 276, 35900-35908.
10. Dale, L.B., Bhattacharya, M., Anborgh, P.H., Murdoch, B., Bhatia, M., Nakanishi, S. & Ferguson, S.S.G. (2000) G-protein-coupled receptor-kinase-mediated desensitization of metabotropic glutamate receptor 1A protects against cell death. J. Biol. Chem., 275, 38213-38220.
11. Flint, A.C., Dammerman, R.S. & Kriegstein, A.R. (1999) Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc. Natl Acad. Sci. USA, 96, 12144-12149.
12. Freedman, N.J. & Lefkowitz, R.J. (1996) Desensitization of G protein-coupled receptors. Recent Prog. Horm Res., 51, 319-351.
13. Gereau, R.W., IV, & Heinemann, S.F. (1998) Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5. Neuron, 20, 143-151.
14. Hashimoto, K. & Kano, M. (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron, 38, 785-796.
15. Hirono, M., Konishi, S. & Yoshioka, T. (1998) Phospholipase C-independent group I metabotropic glutamate receptor-mediated inward current in mouse purkinje cells. Biochem. Biophys. Res. Commun., 251, 753-758.
16. Hollmann, M. & Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci., 17, 31-108.
17. Kadotani, H., Hirano, T., Masugi, M., Nakamura, K., Nakao, K., Katsuki, M. & Nakanishi, S. (1996) Motor discoordination results from combined gene disruption of the NMDA receptor NR2A and NR2C subunits, but not from single disruption of the NR2A or NR2C subunit. J. Neurosci., 16, 7859-7867.
18. Kano, M., Garaschuk, O., Verkhratsky, A. & Konnerth, A. (1995) Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurones. J. Physiol. (Lond), 487, 1-16.
19. Kawabata, S., Kohara, A., Tsutsumi, R., Itahana, H., Hayashibe, S., Yamaguchi, T. & Okada, M. (1998) Diversity of calcium signaling by metabotropic glutamate receptors. J. Biol. Chem., 273, 17381-17385.
20. Kawabata, S., Tsutsumi, R., Kohara, A., Yamaguchi, T., Nakanishi, S. & Okada, M. (1996) Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Nature, 383, 89-92.
21. 2+ pool in cerebellar Purkinje neurons. Biophys. J., 73, 3349-3357.
22. Kitabatake, Y., Hikida, T., Watanabe, D., Pastan, I. & Nakanishi, S. (2003) Impairment of reward-related learning by cholinergic cell ablation in the striatum. Proc. Natl Acad. Sci. USA, 100, 7965-7970.
23. 2+ buffering in Purkinje neurons. Neuron, 24, 989-1002.
24. Martin, L.J., Blackstone, C.D., Huganir, R.L. & Price, D.L. (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron, 9, 259-270.
25. Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R., Takeda, M., Nakamura, K., Nakao, K., Katsuki, M. & Nakanishi, S. (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell, 80, 757-765.
26. Minami, I., Kengaku, M., Smitt, P.S., Shigemoto, R. & Hirano, T. (2003) Long-term potentiation of mGluR1 activity by depolarization-induced Homerla in mouse cerebellar Purkinje neurons. Eur. J. Neurosci., 17, 1023-1032.
27. 2+ homeostasis in hippocampal neurons in vitro. Mol Pharmacol., 35, 671-680.
28. 1-Adrenergic modulation of metabotropic glutamate receptor-induced calcium oscillations and glutamate release in astrocytes. J. Biol. Chem., 276, 46504-46514.
29. Nakahara, K., Okada, M. & Nakanishi, S. (1997) The metabotropic glutamate receptor mGluR5 induces calcium oscillations in cultured astrocytes via protein kinase C phosphorylation. J. Neurochem., 69, 1467-1475.
30. Nakanishi, S. & Masu, M. (1994) Molecular diversity and functions of glutamate receptors. Annu. Rev. Biophys. Biomol. Struct., 23, 319-348.
31. Nakanishi, S., Nakajima, Y., Masu, M., Ueda, Y., Nakahara, K., Watanabe, D., Yamaguchi, S., Kawabata, S. & Okada, M. (1998) Glutamate receptors: brain function and signal transduction. Brain Res. Brain Res. Rev., 26, 230-235.
32. 2+ and inositol 1,4,5-trispbosphate oscillation frequency. Receptor density versus agonist concentration. J. Biol. Chem., 277, 35947-35960.
33. Pin, J.P. & Duvoisin, R. (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology, 34, 1-26.
34. Prézeau, L., Gomeza, J., Ahern, S., Mary, S., Galvez, T., Bockaert, J. & Pin, J.P. (1996) Changes in the carboxyl-terminal domain of metabotropic glutamate receptor 1 by alternative splicing generate receptors with differing agonist-independent activity. Mol. Pharmacol., 49, 422-429.
35. 2+ signaling in rat hippocampal neurons. J. Neurosci., 20, 8628-8636.
36. Reichelt, W. & Knöpfel, T. (2002) Glutamate uptake controls expression of a slow postsynaptic current mediated by mGluRs in cerebellar Purkinje cells. J. Neurophysiol., 87, 1974-1980.
37. Rothstein, J.D., Martin, L., Levey, A.I., Dykes-Hoberg, M., Jin, L., Wu, D., Nash, N. & Kuncl R.W. (1994) Localization of neuronal and glial glutamate transporters. Neuron, 13, 713-725.
38. Sato, M., Suzuki, K. & Nakanishi, S. (2001) NMDA receptor stimulation and brain-derived neurotrophic factor upregulate Homer 1a mRNA via the mitogen-activated protein kinase cascade in cultured cerebellar granule cells. J. Neurosci., 21, 3797-3805.
39. Shigemoto, R., Nakanishi, S. & Mizuno, N. (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J. Comp. Neurol., 322, 121-135.
40. Tabata, T., Aiba, A. & Kano, M. (2002) Extracellular calcium controls the dynamic range of neuronal metabotropic glutamate receptor responses. Mol. Cell. Neurosci., 20, 56-68.
41. Tabata, T., Sawada, S., Araki, K., Bono, Y., Furuya, S. & Kano, M. (2000) A reliable method for culture of dissociated mouse cerebellar cells enriched for Purkinje neurons. J. Neurosci. Meth., 104, 45-53.
42. Tempia, F., Miniaci, M.C., Anchisi, D. & Strata, P. (1998) Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J. Neurophysiol., 80, 520-528.
43. Watanabe, D., Inokawa, H., Hashimoto, K., Suzuki, N., Kano, M., Shigemoto, R., Hirano, T., Toyama, K., Kaneko, S., Yokoi, M., Moriyoshi, K., Suzuki, M., Kobayashi, K., Nagatsu, T., Kreitman, R.J., Pastan, I. & Nakanishi, S. (1998) Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination. Cell, 95, 17-27.
44. Yamamoto, M., Wada, N., Kitabatake, Y., Watanabe, D., Anzai, M., Yokoyama, M., Teranishi, Y. & Nakanishi, S. (2003) Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J. Neurosci., 23, 6759-6767.