Group I metabotropic glutamate receptor signaling via Gαq/Gα11 secures the induction of long-term potentiation in the hippocampal area CA1

Journal of Neuroscience

Volumn 22, Issue 19, 2002, Pages 8379-8390

  Miura, Masami ^a,f   Watanabe, Masahiko ^b   Offermanns, Stefan ^c   Simon, Melvin I ^d   Kano, Masanobu ^a,e  

^a KANAZAWA UNIV SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^e KANAZAWA UNIVERSITY   (Japan)

^f TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

Author keywords

G protein; Hippocampus; Long term potentiation; Metabotropic glutamate receptor; Mouse; Protein kinase C

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA11; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHAQ; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MUSCARINIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; GENE MUTATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WILD TYPE;

EID: 0036813653     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-19-08379.2002     Document Type: Article

References (71)

1. 2+ signal transduction. J Biol Chem 267:13361-13368.
2. Abeliovich A, Chen C, Goda Y, Silvia AJ, Stevens CF, Tonegawa S (1993) Modified hippocampal long-term potentiation in PKCγ mutant mice. Cell 75:1253-1262.
3. Abraham WC, Bear MF (1996) Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
4. Auerbach JM, Segal M (1994) A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72:2034-2040.
5. Balschun D, Manahan-Vaughan D, Wagner T, Behnisch T, Reymann KG, Wetzel W (1999) A specific role for group I mGluRs in hippocampal LTP and hippocampus-dependent spatial learning. Learn Mem 6:138-152.
6. Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving AJ, Seal AJ, Henley JM, Jane DE, Watkins JC, Collingridge GL (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363:347-350.
7. Bear MF, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19:437-462.
8. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
9. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
10. Bortolotto ZA, Collingridge GL (1992) Activation of glutamate metabotropic receptors induces long-term potentiation. Eur J Pharmacol 214:297-298.
11. Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368:740-743.
12. Chinestra P, Aniksztejn L, Diabira D, Ben-Ari Y (1993) (RS)-alpha-methyl-4-carboxyphenylglycine neither prevents induction of LTP nor antagonizes metabotropic glutamate receptors in CA1 hippocampal neurons. J Neurophysiol 70:2684-2689.
13. Cohen AS, Abraham WC (1996) Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors. J Neurophysiol 76:953-962.
14. Cohen AS, Raymond CR, Abraham WC (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8:160-170.
15. Conn PJ, Pin J-P (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
16. 2+ stores in rat sympathetic neurons. Proc Natl Acad Sci USA 95:7151-7156.
17. Delmas P, Wanaverbecq N, Abogadie FC, Mistry M, Brown DA (2002) Signaling microdomains define the specificity of receptor-mediated InsP3 pathways in neurons. Neuron 24:209-220.
18. Docherty JR (1998) Subtypes of functional alpha1- and alpha2-adrenoceptors. Eur J Pharmacol 361:1-15.
19. Exton JH (1996) Regulation of phosphoinositide phospholipases by hormones, neurotransmitters, and other agonists linked to G-proteins. Annu Rev Pharmacol Toxicol 36:481-509.
20. Frey U, Schroeder H, Matthies H (1990) Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 522:69-75.
21. Friberg IK, Young AB, Standaert DG (1998) Differential localization of the mRNAs for the pertussis toxin insensitive G-protein alpha subunits Gq, G11, and Gz in the rat brain, and regulation of their expression after striatal deafferentation. Brain Res Mol Brain Res 54:298-310.
22. Goh JW, Pennefather PS (1989) A pertussis toxin-sensitive G protein in hippocampal long-term potentiation. Science 244:980-983.
23. Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Wu D, Simon MI, Kano M (2000) Climbing fiber synapse elimination during postnatal cerebellar development requires signal transduction involving Gαq and phospholipase C β4. Prog Brain Res 124:31-48.
24. Hoyer D, Martin GR (1997) 5-HT receptor classification and nomenclature: Towards a harmonization with the human genome. Neuropharmacology 36:419-428.
25. Jouvenceau A, Billard JM, Lamour Y, Dutar P (1996) Persistence of CA1 hippocampal LTP after selective cholinergic denervation. Neuro-Report 7:948-952.
26. Kaneko S, Maeda T, Satoh M (1997) Cognitive enhancers and hippocampal long-term potentiation in vitro. Behav Brain Res 83:45-49.
27. Katsuki H, Kaneko S, Satoh M (1992) Involvement of postsynaptic G proteins in hippocampal long-term potentiation. Brain Res 581:108-114.
28. Katsuki H, Izumi Y, Zorumski CF (1997) Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 77:3013-3020.
29. Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M (1998) Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor ε1 subunit. J Neurosci 18:6704-6712.
30. Klann E, Chen SJ, Sweatt JD (1993) Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a selective peptide substrate. Proc Natl Acad Sci USA 90:8337-8341.
31. Kleppisch T, Voigt V, Allmann R, Offermanns S (2001) Gαq-deficient mice lack metabotropic glutamate receptor-dependent long-term depression but show normal long-term potentiation in the hippocampal CA1 region. J Neurosci 21:4943-4948.
32. Liu M, Simon MI (1996) Regulation by cAMP-dependent protein kinase of a G-protein-mediated phospholipase C. Nature 382:83-87.
33. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196-5205.
34. Luján R, Nusser Z, Roberts JDB, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488-1500.
35. Luján R, Roberts JDB, Shigemoto R, Ohishi H, Somogyi P (1997) Differential plasma membrane distribution of metabotropic glutamate receptor mGluR1α, mGluR2 and mGluR5, relative to neurotransmitter release sites. J Chem Neuroanat 13:219-241.
36. Mailleux P, Mitchell F, Vanderhaeghen JJ, Milligan G, Erneux C (1992) Immunohistochemical distribution of neurons containing the G-proteins Gq alpha/G11 alpha in the adult rat brain. Neuroscience 51:311-316.
37. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA (1993) Modulation of synaptic transmission and long-term potentiation: Effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70:1451-1459.
38. Manzoni OJ, Weisskopf MG, Nicoll RA (1994) MCPG antagonizes metabotropic glutamate receptors but not long-term potentiation in the hippocampus. Eur J Neurosci 6:1050-1054.
39. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765.
40. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
41. Milligan G (1993) Regional distribution and quantitative measurement of the phosphoinositidase C-linked guanine nucleotide binding proteins G11 alpha and Gq alpha in rat brain. J Neurochem 61:845-851.
42. Nakanishi S (1994) Metabotropic glutamate receptors: Synaptic transmission, modulation, and plasticity. Neuron 13:1031-1037.
43. Nicoll RA, Malenka RC (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
44. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
45. Nusser Z, Mulvihill E, Streit P, Somogyi P (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427.
46. Offermanns S, Simon MI (1998) Genetic analysis of mammalian G-protein signalling. Oncogene 17:1375-1381.
47. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Gαq. Proc Natl Acad Sci USA 94:14089-14094.
48. Offermanns S, Zhao LP, Gohla A, Sarosi I, Simon MI, Wilkie TM (1998) Embryonic cardiomyocyte hypoplasia and craniofacial defects in G alpha q/G alpha 11-mutant mice. EMBO J 17:4304-4312.
49. Ramakers GM, McNamara RK, Lenox RH, De Graan PN (1999) Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanine-rich C kinase substrate and growth-associated protein-43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J Neurochem 73:2175-2183.
50. Richter-Levin G, Errington ML, Maegawa H, Bliss TVP (1994) Activation of metabotropic glutamate receptors is necessary for long-term potentiation in the dentate gyrus and for spatial learning. Neuropharmacology 33:853-857.
51. Riedel G, Reymann KG (1993) An antagonist of the metabotropic glutamate receptor prevents LTP in the dentate gyrus of freely moving rats. Neuropharmacology 32:929-931.
52. Riedel G, Wetzel W, Reymann KG (1996) Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 20:761-789.
53. Sakimura K, Kutsuwada T, Ito I, Manabe T, Takayama C, Kushiya E, Yagi T, Aizawa S, Inoue Y, Sugiyama H, Mishina M (1995) Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature 373:151-155.
54. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93:13304-13309.
55. Selig DK, Lee HK, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075-1082.
56. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503-7522.
57. Simon MI, Strathmann MP, Gautam N (1991) Diversity of G proteins in signal transduction. Science 252:802-808.
58. Stanton PK, Sarvey JM (1985) Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J Neurosci 5:2169-2176.
59. Staubli U, Otaky N (1994) Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptor-mediated responses. Brain Res 643:10-16.
60. Strathmann MP, Simon MI (1990) G protein diversity: A distinct class of a subunits is present in vertebrates and invertebrates. Proc Natl Acad Sci USA 87:9113-9117.
61. Tanaka J, Nakagawa S, Kushiya E, Yamasaki M, Fukaya M, Iwanaga T, Simon MI, Sakimura K, Kano M, Watanabe M (2000) Gq protein a subunits Gαq and Gα11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12:781-792.
62. Tecott LH, Logue SF, Wehner JM, Kauer JA (1998) Perturbed dentate gyrus function in serotonin 5-HT2C receptor mutant mice. Proc Natl Acad Sci USA 95:15026-15031.
63. 2+ signalling in K562 human erythroleukaemia cells: Effect of dimethyl sulphoxide and role of G-proteins in thrombin- and thromboxane A2-activated pathways. Biochem J 312:151-158.
64. Tsubokawa H, Ross WN (1997) Muscarinic modulation of spike back-propagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 17:5782-5791.
65. Tsubokawa H, Offermanns S, Simon MI, Kano M (2000) Calcium-dependent persistent facilitation of spike backpropagation in the CA1 pyramidal neurons. J Neurosci 20:4878-4884.
66. Wang JH, Feng DP (1992) Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region. Proc Natl Acad Sci USA 89:2576-2580.
67. Wang RY, Arvanov VL (1998) M100907, a highly selective 5-HT2A receptor antagonist and a potential atypical antipsychotic drug, facilitates induction of long-term potentiation in area CA1 of the rat hippocampal slice. Brain Res 779:309-313.
68. Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10:478-487.
69. Wess J, Blin N, Mutschler E, Bluml K (1995) Muscarinic acetylcholine receptors: Structural basis of ligand binding and G protein coupling. Life Sci 56:915-922.
70. Wilsch VW, Behnisch T, Jager T, Reymann KG, Balschun D (1998) When are class I metabotropic glutamate receptors necessary for long-term potentiation? J Neurosci 18:6071-6080.
71. Yamada K, Fukaya M, Shimizu H, Sakimura K, Watanabe M (2001) NMDA receptor subunits GluRε1, GluRε3, and GluRζ1 are enriched at the mossy fiber-granule cell synapse in the adult mouse cerebellum. Eur J Neurosci 13:2025-2036.