mGluR1/5 subtype-specific calcium signalling and induction of long-term potentiation in rat hippocampal oriens/alveus interneurones

Journal of Physiology

Volumn 575, Issue 1, 2006, Pages 115-131

  Topolnik, Lisa ^a   Azzi, Mounia ^a   Morin, France ^a   Kougioumoutzakis, André ^a   Lacaille, Jean Claude ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL; METABOTROPIC RECEPTOR 1ALPHA; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITE; GENE ACTIVATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INTERNEURON; INTRACELLULAR RECORDING; LONG TERM POTENTIATION; MOLECULAR IMAGING; MOLECULAR MECHANICS; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; WESTERN BLOTTING; DENDRITIC CELL; ENZYME ACTIVATION; HIPPOCAMPAL ALVEUS INTERNEURON; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL ORIENS INTERNEURON; IMMUNOHISTOCHEMISTRY; NERVE CELL NETWORK; NERVE EXCITABILITY; POSTSYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP;

EID: 33746821798     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.112896     Document Type: Article

References (64)

1. Alle H, Jonas P & Geiger JR (2001). PTP and LTP at a hippocampal mossy fiber-interneuron synapse. Proc Natl Acad Sci U S A 98, 14708-14713.
2. Atsumi S, Wakabayashi K, Titani K, Fujii Y & Kawate T (1993). Neuronal pp60c-src(+) in the developing chick spinal cord as revealed with anti-hexapeptide antibody. J Neurocytol 22, 244-258.
3. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA & Somogyi P (1993). The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
4. Berkeley JL & Levey AI (2003). Cell-specific extracellular signal-regulated kinase activation by multiple G protein-coupled receptor families in hippocampus. Mol Pharmacol 63, 128-135.
5. Bonni A, Brunet A, West AE, Datta SR, Takasu MA & Greenberg ME (1999). Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 28, 1358-1362.
6. Bortolotto ZA & Collingridge GL (1993). Characterization of LTP induced by the activation of glutamate metabotropic receptors in area CA1 of the hippocampus. Neuropharmacology 32, 1-9.
7. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL & Worley PF (1997). Homer: A protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
8. Cao W, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL & Worley PF (2000). Direct binding of activated c-Src to the β3-adrenergic receptor is required for MAP kinase activation. J Biol Chem 275, 38131-38134.
9. Clapham DE (2003). TRP channels as cellular sensors. Nature 426, 517-524.
10. Congar P, Leinekugel X, Ben-Ari Y & Crepel V (1997). A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17, 5366-5379.
11. Emptage NG (1999). Calcium on the up: Supralinear calcium signaling in central neurons. Neuron 24, 495-497.
12. English JD & Sweatt JD (1996). Activation of p42 mitogen-activated protein kinase in hippocampal long-term potentiation. J Biol Chem 271, 24329-24332.
13. Ferraguti F, Baldani-Guerra B, Corsi M, Nakanishi S & Corti C (1999). Activation of the extracellular signal-regulated kinase 2 by metabotropic glutamate receptors. Eur J Neurosci 11, 2073-2082.
14. Fotuhi M, Sharp AH, Glatt CE, Hwang PM, von Krosigk M, Snyder SH & Dawson TM (1993). Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain. J Neurosci 13, 2001-2013.
15. Freund TS & Buzsaki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
16. Gee CE, Benquet P & Gerber U (2003). Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol 546, 655-664.
17. Grewal SS, York RD & Stork PJ (1999). Extracellular-signal-regulated kinase signalling in neurons. Current Opin Neurobiol 9, 544-553.
18. Hermans E & Challiss R (2001). Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors: Prototypic family C G-protein-coupled receptors. Biochem J 359, 465-484.
19. Heuss C, Scanziani M, Gahwiler BH & Gerber U (1999). G-protein-independent signaling mediated by metabotropic glutamate receptors. Nature Neurosci 2, 1070-1077.
20. Hisatsune C, Kuroda Y, Nakamura K, Inoue T, Nakamura T, Michikawa T, Mizutani A & Mikoshiba K (2004). Regulation of TRPC6 channel activity by tyrosine phosphorylation. J Biol Chem 279, 18887-18894.
21. Kelleher R, Govindarajan A, Jung H-Y, Kang H & Tonegawa S (2004). Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467-479.
22. Kim SJ, Kim YuS, Yuan JP, Petralia RS, Worley PF & Linden DJ (2003). Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426, 285-291.
23. Komiyama NH, Watabe AM, Carlisle HJ, Porter K, Charlesworth P, Monti J et al. (2002). SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J Neurosci 22, 9721-9732.
24. Krapivinsky G, Krapivinsky L, Manasian Y, Ivanov A, Tyzio R, Pellegrino C, Ben-Ari Y, Clapham DE & Medina I (2003). The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 40, 775-784.
25. Laezza F, Doherty JJ & Dingledine R (1999). Long-term depression in hippocampal interneurons: Joint requirement for pre- and postsynaptic events. Science 285, 1411-1414.
26. Lamsa K, Heeroma JH & Kullmann D (2005). Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci 8, 916-924.
27. Lapointe V, Morin F, Ratte S, Croce A, Conquet F & Lacaille J-C (2004). Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J Physiol 15, 125-135.
28. Lei S & McBain CJ (2004). Two loci of expression for long-term depression at hippocampal mossy-fiber-interneuron synapses. J Neurosci 24, 2112-2121.
29. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, Sonenberg N & Lawrence JC Jr (1994). PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266, 653-656.
30. Luttrell LM, Ferguson SS, Daaka Y, Miller WE, Maudsley S, Della Rocca GJ et al. (1999). Beta-arrestin-dependent formation of β2 adrenergic receptor-Src protein kinase complexes. Science 283, 655-661.
31. McBain CJ, DiChiara TJ & Kauer JA (1994). Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14, 4433-4445.
32. Maccaferri G, Toth K & McBain CJ (1998). Target-specific expression of presynaptic mossy fiber plasticity. Science 279, 1368-1370.
33. McMahon LL & Kauer JA (1997). Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18, 295-305.
34. Mannaioni G, Marino MJ, Valenti O, Traynelis SF & Conn PJ (2001). Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21, 5925-5934.
35. Mao L, Yang L, Tang Q, Samdani S, Zhang G & Wang JQ (2005). The scaffold protein Homer1b/c links metabotropic glutamate receptor 5 to extracellular signal-regulated protein kinase cascades in neurons. J Neurosci 25, 2741-2752.
36. 2+ stores: ubiquitous partners of surface channels in neurons. News Physiol Sci 17, 144-149.
37. Morin F, Beaulieu C & Lacaille J-C (1998). Selective loss of GABA neurons in area CA1 of the rat hippocampus after intraventricular kainate. Epilepsy Res 32, 363-369.
38. 2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with back-propagating action potentials. Neuron 24, 727-737.
39. Odell A, Scott JL & Van Helden DF (2005). Epidermal growth factor induces tyrosine phosphorylation, membrane insertion, and activation of transient receptor potential channel 4. J Biochem 280, 37974-37987.
40. Parekh AB & Putney JW Jr (2005). Store-operated calcium channels. Physiol Rev 85, 757-810.
41. Peavy RD & Conn PJ (1998). Phosphorylation of mitogen-activated protein kinase in cultured rat cortical glia by stimulation of metabotropic glutamate receptors. J Neurochem 71, 603-612.
42. Pelkey KA, Lavezzari G, Racca C, Roche KW & McBain CJ (2005). mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46, 89-102.
43. Perez Y, Morin F & Lacaille J-C (2001). A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci U S A 98, 9401-9406.
44. Pin J-P & Duvoisin R (1995). The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 1-26.
45. 2+ release and inward currents in hippocampal CA1 pyramidal neurons. Neuropharmacology 46, 1057-1069.
46. Ramsey IS, Delling M & Clapham DE (2006). An introduction to trp channels. Annu Rev Physiol 68, 619-647.
47. Renaud J, Emond M, Meilleur S, Psarropoulou C & Carmant L (2002). AIDA, a class I metabotropic glutamate-receptor antagonist limits kainate-induced hippocampal dysfunction. Epilepsia 43, 1306-1317.
48. Rosen LB, Ginty DD, Weber MJ & Greenberg ME (1994). Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12, 1207-1221.
49. Scanziani M, Gahwiler BH & Charpak S (1998). Target cell-specific modulation of transmitter release at terminals from a single axon. Proc Natl Acad Sci U S A 95, 12004-12009.
50. Strübing C, Krapivinsky G, Krapivinsky L & Clapham DE (2001). TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645-655.
51. Sweatt JD (2004). Mitogen-activated protein kinases in synaptic plasticity and memory. Current Opin Neurobiol 14, 311-317.
52. Tempia F, Alojado ME, Strata P & Knopfel T (2001). Characterization of the mGluR1-mediated electrical and calcium signaling in Purkinje cells of mouse cerebellar slices. J Neurophysiol 86, 1389-1397.
53. Thandi S, Blank JL & Challiss RA (2002). Group-I metabotropic glutamate receptors, mGlu1a and mGlu5a, couple to extracellular signal-regulated kinase (ERK) activation via distinct, but overlapping, signalling pathways. J Neurochem 83, 1139-1153.
54. 2+ signals by pre- and postsynaptic activity in hippocampal interneurons. J Neurosci 25, 990-1001.
55. Toth K & McBain CJ (1998). Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nature Neurosci 1, 572-578.
56. Tozzi A, Bengtson CP, Longone P, Carignani C, Fusco FR, Bernardi G & Mercuri NB (2003). Involvement of transient receptor potential-like channels in responses to mGluR-I activation in midbrain dopamine neurons. Eur J Neurosci 18, 2133-2145.
57. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ & Worley PF (1998). Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21, 717-726.
58. Venkatachalam K, Zheng E & Gill DL (2003). Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 278, 29031-29040.
59. Weiler IJ & Greenough WT (1993). Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc Natl Acad Sci U S A 90, 7168-7171.
60. 2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons. J Neurophysiol 81, 371-382.
61. Xiao B, Tu JC & Worley PF (2000). Homer: A link between neural activity and glutamate receptor function. Curr Opin Neurobiol 10, 370-374.
62. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22, 4860-4868.
63. Yuan J, Lipinski M & Degterev A (2003). Diversity in the mechanisms of neuronal cell death. Neuron 40, 401-413.
64. Zhao W, Bianchi R, Wang M & Wong RK (2004). Extracellular signal-regulated kinase 1/2 is required for the induction of group I metabotropic glutamate receptor-mediated epileptiform discharges. J Neurosci 24, 76-84.