A new signalling pathway for parallel fibre presynaptic type 4 metabotropic glutamate receptors (mGluR4) in the rat cerebellar cortex

Journal of Physiology

Volumn 590, Issue 13, 2012, Pages 2977-2994

  Abitbol, Karine ^a   Mclean, Heather ^a   Bessiron, Thomas ^a   Daniel, Hervé ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GUANYLATE CYCLASE; METABOTROPIC RECEPTOR 4; MITOGEN ACTIVATED PROTEIN KINASE; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE C; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CEREBELLUM CORTEX; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; MALE; NERVE ENDING; NERVE FIBER; NEUROMODULATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CEREBELLAR CORTEX; MALE; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TYPE C PHOSPHOLIPASES;

EID: 84862998111     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.232074     Document Type: Article

References (66)

1. Abitbol K, Acher F & Daniel H (2008). Depression of excitatory transmission at PF-PC synapse by group III metabotropic glutamate receptors is provided exclusively by mGluR4 in the rodent cerebellar cortex. J Neurochem 105, 2069-2079.
2. Alessi DR, Cuenda A, Cohen P, Dudley DT & Saltiel AR (1995). PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 270, 27 489-27 494.
3. Aller MI, Veale EL, Linden AM, Sandu C, Schwaninger M, Evans LJ, Korpi ER, Mathie A, Wisden W & Brickley SG (2005). Modifying the subunit composition of TASK channels alters the modulation of a leak conductance in cerebellar granule neurons. J Neurosci 25, 11455-11467.
4. Atluri P & Regehr WG (1996). Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J Neurosci 16, 5661-5671.
5. + channels. Mol Interv 3, 205-219.
6. 3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351, 751-754.
7. Brown SP, Safo PK & Regehr WG (2004). Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24, 5623-5631.
8. 2P2.1 is dependant on C-terminal dephosphorylation. Mol Cell Neurosci 37, 32-39.
9. Capogna M (2004). Distinct properties of presynaptic group II and III metabotropic glutamate receptor-mediated inhibition of perforant pathway-CA1 EPSCs. Eur J Neurosci 19, 2847-2858.
10. Chavis P, Mollard P, Bockaert J & Manzoni O (1998). Visualization of cyclic AMP-regulated presynaptic activity at cerebellar granule cells. Neuron 20, 773-781.
11. Chen C & Regher WG (1997). The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J Neurosci 17, 8687-8694
12. + channels. Ann N Y Acad Sci 868, 233-285.
13. Conn PJ & Pin JP (1997). Pharmacology and functions of metabotropic glutamate receptors. Ann Rev Pharmacol Toxicol 37, 205-237.
14. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, Collingridge L & Crepel F (1994). Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237-243.
15. + channels. J Physiol 537, 793-800.
16. 2+ influx at parallel fibre synapses of the rat cerebellum. J Physiol 557, 159-174.
17. Endo S & Thomas Launey T (2003). ERKs regulate PKC-dependent synaptic depression and declustering of glutamate receptors in cerebellar Purkinje cells. Neuropharmacology 45, 863-872.
18. Evans DI, Jones RS & Woodhall G (2001). Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex. J Neurophysiol 85, 571-579.
19. Flor PJ, Lukic S, Ruegg D, Leonhardt T, Knopfel T & Kuhn R (1995). Molecular cloning, functional expression and pharmacological characterization of the human metabotropic glutamate receptor type 4. Neuropharmacology 34, 149-155.
20. Gille A, Lushington GH, Mou TC, Doughty MB, Johnson RA & Seifert R (2004). Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides. J Biol Chem 279, 19955-19969.
21. Goldstein SN, Bockenhauer D, O'Kelly I & Zilberberg N (2001). Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2, 175-184.
22. Goossens J, Daniel H, Rancillac A, van der Steen J, Oberdick J, Crépel F, De Zeeuw CI & Frens MA (2001). Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J Neurosci 21, 5813-5823.
23. 2+ channels in rat sympathetic neurons. Mol Pharmacol 67, 1840-1851.
24. Harris DN, Asaad MM, Phillips MB, Goldenberg HJ & Antonaccio MJ (1979). Inhibition of adenylyl cylase in human blood platelets by 9-substituted adenine derivatives. J Cyclic Nucleotide Res 5, 125-134.
25. 2P channels: focus on TREK1. Nat Neurosci 8, 251-261.
26. Iacovelli L, Bruno V, Salvatore L, Melchiorri D, Gradini R, Caricasole A, Barletta E, De Blasi A & Nicoletti F (2002). Native group-III metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/phosphatidylinositol-3-kinase pathways. J Neurochem 82, 216-223.
27. Jackson C, Welch HC & Bellamy TC (2010). Control of cerebellar long-term potentiation by P-Rex-family guanine-nucleotide exchange factors and phosphoinositide 3-kinase. PLoS ONE 5, e11962.
28. + channels. Biochemistry 37, 13291-13299.
29. Kase H, Iwahashi K, Nakanishi S, Matsuda Y, Yamada K, Takahashi M, Murakata C, Sato A & Kaneko M (1987). K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun 142, 436-440.
30. Kennard LE, Chumbley JR, Ranatunga KM, Armstrong SJ, Veale EL & Mathie A (2005). Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br J Pharmacol 144, 821-829.
31. Kreitzer AC & Regehr WG (2002). Retrograde signalling by endocannabinoids. Curr Opin Neurobiol 12, 324-330.
32. Krieger P, Buschges A & el Manira A (1999). Calcium channels involved in synaptic transmission from reticulospinal axons in lamprey. J Neurophysiol 81, 1699-1705.
33. Kristensen P, Suzdak PD & Thomsen C (1993). Expression pattern and pharmacology of the rat type IV metabotropic glutamate receptor. Neurosci Lett 155, 159-162.
34. Lavialle-Defaix C, Gautier H, Defaix A, Lapied B & Grolleau F (2006). Differential regulation of two distinct voltage-dependent sodium currents by group III metabotropic glutamate receptor activation in insect pacemaker neurons. J Neurophysiol 96, 2437-2450.
35. Levenes C, Daniel H & Crepel F (2001). Retrograde modulation of transmitter release by postsynaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum. J Physiol 537, 125-140.
36. Llano I, Marty A, Armstrong C & Konnerth A (1991). Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol 434, 183-213.
37. Lorez M, Humbel U, Pflimlin MC & Kew JN (2003). Group III metabotropic glutamate receptors as autoreceptors in the cerebellar cortex. Br J Pharmacol 138, 614-625.
38. Mateos JM, Elezgarai I, Benitez R, Osorio A, Bilbao A, Azkue JJ, Kuhn R, Knöpfel T & Grandes P (1999). Clustering of the group III metabotropic glutamate receptor 4a at parallel fiber synaptic terminals in the rat cerebellar molecular layer. Neurosci Res 35, 71-74.
39. Mathie A (2007). Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors. J Physiol 578, 377-385.
40. 2+ channels in single nerve terminals. J Biol Chem 277, 47796-47803.
41. Miniaci MC, Bonsi P, Tempia F, Strata P & Pisani A (2001). Presynaptic modulation by group III metabotropic glutamate receptors (mGluRs) of the excitatory postsynaptic potential mediated by mGluR1 in rat cerebellar Purkinje cells. Neurosci Lett 310, 61-65.
42. Mintz IM, Sabatini BL & Regehr WG (1995). Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675-688.
43. Morreale A, Mallon B, Beale G, Watson J & Rumsby M (1997). Ro31-8220 inhibits protein kinase C to block the phorbol ester-stimulated release of choline- and ethanolamin-metabolites from CG glioma cells: p70 S6 kinase and MAPKAP kinase-1β do not function downstream of PKC in activating PLD. FEBS Lett 417, 38-42.
44. + channel TASK-3 and on the outward current in thalamic neurons. J Physiol 572, 639-657.
45. 2+-dependent release of Munc18-1 from presynaptic mGluRs in short-term facilitation. Proc Natl Acad Sci U S A 106, 18385-18389.
46. Neale SA, Garthwaite J & Batchelor AM (2001). Metabotropic glutamate receptor subtypes modulating neurotransmission at parallel fibre-Purkinje cell synapses in rat cerebellum. Neuropharmacology 41, 42-49.
47. Neil KE, Kendall DA & Alexander SP (1996). Coupling of metabotropic glutamate receptors to phosphoinositide mobilisation and inhibition of cyclic AMP generation in the guinea-pig cerebellum. Br J Pharmacol 118, 311-316.
48. 2+ levels via the phospholipase C transduction pathway in cultured Purkinje neurons. J Neurophysiol 78, 63-75.
49. Niswender CM, Johnson KA, Luo Q, Ayala JE, Kim C, Conn PJ & Weaver CD (2008). A novel assay of Gi/o-linked G protein-coupled receptor coupling to potassium channels provides new insights into the pharmacology of the group III metabotropic glutamate receptors. Mol Pharmacol 73, 1213-1224.
50. Pekhletski R, Gerlai R, Overstreet LS, Huang XP, Agopyan N, Slater NT, Abramow-Newerly W, Roder JC & Hampson DR (1996). Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J Neurosci 16, 6364-6373.
51. Perroy J, Prezeau L, De Waard M, Shigemoto R, Bockaert J & Fagni L (2000). Selective blockade of P/Q-type calcium channels by the metabotropic glutamate receptor type 7 involves a phospholipase C pathway in neurons. J Neurosci 20, 7896-7904.
52. Prézeau L, Carrette J, Helpap B, Curry K, Pin JP & Bockaert J (1994). Pharmacological characterization of metabotropic glutamate receptors in several types of brain cells in primary cultures. Mol Pharmacol 45, 570-577.
53. 2+ current modulation by mGluRs at individual hippocampal synapses. Cereb Cortex 14, 748-758.
54. Sabatini BL & Regehr WG (1997). Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J Neurosci 17, 3425-3435.
55. Salin PA, Malenka RC & Nicoll RA (1996). Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fibre synapses. Neuron 16, 797-803.
56. Saugstad JA & Segerson TP & Westbrook GL (1996). Metabotropic glutamate receptors activate G-protein-coupled inwardly rectifying potassium channels in Xenopus oocytes. J Neurosci 16, 5979-5985.
57. + channel, GIRK, in Xenopus oocytes. J Gen Physiol 109, 477-490.
58. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M & Onodera K (1996). Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274, 594-597.
59. Talley EM, Solorzqno G, Lei Q, Kim D & Bayliss DA (2001). CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21, 7491-7505.
60. Tanabe Y, Nomura A, Masu M, Shigemoto R, Mizuno N & Nakanishi S (1993). Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13, 1372-1378.
61. 2+-ATPase. Proc Natl Acad Sci U S A 87, 2466-2470.
62. Thomsen C, Kristensen P, Mulvihill E, Haldeman B & Suzdak PD (1992). L-2-amino-4-phosphonobutyrate (L-AP4) is an agonist at the type IV metabotropic glutamate receptor which is negatively coupled to adenylyl cyclase. Eur J Pharmacol 227, 361-362.
63. Vlahos CJ, Matter WF, Hui KY & Brown RF (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269, 5241-5248.
64. + current sensitive to muscarinic receptor activation in rat cultured cerebellar granule neurons. J Physiol 491, 401-412.
65. Woodhall GL, Ayman G & Jones RS (2007). Differential control of two forms of glutamate release by group III metabotropic glutamate receptors at rat entorhinal synapses. Neuroscience 148, 7-21.
66. Zhang W & Linden DJ (2009). Neuromodulation at single presynaptic boutons of cerebellar parallel fibres is determined by bouton size and basal action potential-evoked Ca transient amplitude. J Neurosci 29, 15586-15594.