Interaction between αCaMKII and GluN2B controls ERK-dependent plasticity

Journal of Neuroscience

Volumn 32, Issue 31, 2012, Pages 10767-10779

  El Gaamouch, Farida ^a,d   Buisson, Alain ^a,c   Moustié, Olivier ^a   Lemieux, Mado ^d   Labrecque, Simon ^d   Bontempi, Bruno ^b   De Koninck, Paul ^d,e   Nicole, Olivier ^a,b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c CHU La Tronche and University   (France)

^d CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; DENDRITIC SPINE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING;

4-AMINOPYRIDINE; ANALYSIS OF VARIANCE; ANIMALS; BICUCULLINE; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; CEREBRAL CORTEX; DENDRITIC SPINES; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; GABA-A RECEPTOR ANTAGONISTS; GUANYLATE KINASE; IMMUNOPRECIPITATION; LUMINESCENT PROTEINS; MALE; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PHOTOBLEACHING; POTASSIUM CHANNEL BLOCKERS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84864437081     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5622-11.2012     Document Type: Article

References (77)

1. Agell N, Bachs O, Rocamora N, Villalonga P (2002) Modulation of the Ras/ Raf/MEK/ERK pathway by Ca(2 +), and calmodulin. Cell Signal 14:649-654.
2. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neu-rosci 1:602-609.
3. Bading H, Greenberg ME (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253:912-914.
4. Bagal AA, Kao JP, Tang CM, Thompson SM (2005) Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc Natl Acad Sci USA 102:14434-14439.
5. Barria A, Malinow R (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289-301.
6. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411:801-805.
7. Bayer KU, LeBel E, McDonald GL, O'Leary H, Schulman H, De Koninck P (2006) Transition from reversible to persistent binding of CaMKII to postsynaptic sites andNR2B. J Neurosci 26:1164-1174.
8. Bellone C, Nicoll RA (2007) Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55:779-785.
9. Chandler LJ, Sutton G, Dorairaj NR, Norwood D (2001) N-methyl D-aspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J Biol Chem 276:2627-2636.
10. Chen Q, He S, Hu XL, Yu J, Zhou Y, Zheng J, Zhang S, Zhang C, Duan WH, Xiong ZQ (2007) Differential roles of NR2A- and NR2B-containing NMDA receptors in activity-dependent brain-derived neurotrophic factor gene regulation and limbic epileptogenesis. J Neurosci 27:542-552.
11. Chwang WB, O'Riordan KJ, Levenson JM, Sweatt JD (2006) ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn Mem 13:322-328.
12. Colbran RJ, Brown AM (2004) Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol 14:318-327.
13. Di Cristo G, Berardi N, Cancedda L, Pizzorusso T, Putignano E, Ratto GM, Maffei L (2001) Requirement of ERK activation for visual cortical plasticity. Science 292:2337-2340.
14. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332.
15. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
16. Foster KA, McLaughlin N, Edbauer D, Phillips M, Bolton A, Constantine-Paton M, Sheng M (2010) Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J Neurosci 30:2676-2685.
17. Fox CJ, Russell KI, Wang YT, Christie BR (2006) Contribution of NR2A and NR2B NMDA subunits to bidirectional synaptic plasticity in the hippocampus in vivo. Hippocampus 16:907-915.
18. Gardoni F, Caputi A, Cimino M, Pastorino L, Cattabeni F, Di Luca M (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J Neuro-chem 71:1733-1741.
19. Gladding CM, Raymond LA (2011) Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci 48:308-320.
20. Gouix E, Leveille F, Nicole O, Melon C, Had-Aissouni L, Buisson A (2009) Reverse glial glutamate uptake triggers neuronal cell death through extra-synaptic NMDA receptor activation. Mol Cell Neurosci 40:463-473.
21. Hardingham GE, Bading H (2002) Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim Biophys Acta 1600:148-153.
22. Harris AZ, Pettit DL (2008) Recruiting extrasynaptic NMDA receptors augments synaptic signaling. J Neurophysiol 99:524-533.
23. 2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J Neurosci 25:6971-6983.
24. Illario M, Cavallo AL, Bayer KU, Di Matola T, Fenzi G, Rossi G, Vitale M (2003) Calcium/calmodulin-dependent protein kinase II binds to Raf-1 and modulates integrin-stimulated ERK activation. J Biol Chem 278:45101-45108.
25. Izumi Y, Auberson YP, Zorumski CF (2006) Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors. J Neurosci 26:7181-7188.
26. Jin SX, Feig LA (2010) Long-term potentiation in the CA1 hippocampus induced by NR2A subunit-containing NMDA glutamate receptors is mediated by Ras-GRF2/Erk map kinase signaling. PloS One 5:e11732.
27. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479.
28. Kim MJ, Dunah AW, Wang YT, Sheng M (2005) Differential roles of NR2A-and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46:745-760.
29. Kirson ED, Yaari Y (1996) Synaptic NMDA receptors in developing mouse hippocampal neurones: functional properties and sensitivity to ifen-prodil. J Physiol 497:437-455.
30. Köhr G (2006) NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 326:439-446.
31. 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 Ras-GRF1. Neuron 40:775-784.
32. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458:299-304.
33. Legendre P, Westbrook GL (1991) Ifenprodil blocks N-methyl-D-aspartate receptors by a two-component mechanism. Mol Pharmacol 40:289-298.
34. Leonard AS, Lim IA, Hemsworth DE, Horne MC, Hell JW (1999) Calcium/ calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. Proc Natl Acad Sci USA 96:3239-3244.
35. Leveille F, El Gaamouch F, Gouix E, Lecocq M, Lobner D, Nicole O, Buisson A (2008) Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 22:4258-4271.
36. Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54:583-597.
37. Li N, Wang C, Wu Y, Liu X, Cao X (2009) Ca(2 +)/calmodulin-dependent protein kinase II promotes cell cycle progression by directly activating MEK1 and subsequently modulating p27 phosphorylation. J Biol Chem 284:3021-3027.
38. Lin YC, Redmond L (2008) CaMKIIbeta binding to stable F-actin in vivo regulates F-actin filament stability. Proc Natl Acad Sci USA 105:15791-15796.
39. Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169-182.
40. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021-1024.
41. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24:7821-7828.
42. Neyton J, Paoletti P (2006) Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 26:1331-1333.
43. Okamoto K, Narayanan R, Lee SH, Murata K, Hayashi Y (2007) The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure. Proc Natl Acad Sci USA 104:6418-6423.
44. Okamoto K, Bosch M, Hayashi Y (2009) The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag? Physiology (Bethesda) 24:357-366.
45. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67:239-252.
46. Otmakhov N, Tao-Cheng JH, Carpenter S, Asrican B, Dosemeci A, Reese TS, Lisman J (2004) Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J Neurosci 24:9324-9331.
47. Pacchioni AM, Vallone J, Worley PF, Kalivas PW (2009) Neuronal pentrax-ins modulate cocaine-induced neuroadaptations. J Pharmacol Exp Ther 328:183-192.
48. Patterson MA, Szatmari EM, Yasuda R (2010) AMPA receptors are exocy-tosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc Natl Acad Sci USA 107:15951-15956.
49. Pi Hj, Otmakhov N, El Gaamouch F, Lemelin D, De Koninck P, Lisman J (2010) CaMKII control of spine size and synaptic strength: role of phosphorylation states and non enzymatic action. Proc Natl Acad Sci USA 107:14437-14442.
50. Rose K, Goldberg MP, Choi DW (1993) Cytotoxicity in murine neocortical cell culture. Methods Toxicol 1:15.
51. Sanhueza M, Fernandez-Villalobos G, Stein IS, Kasumova G, Zhang P, Bayer KU, Otmakhov N, Hell JW, Lisman J (2011) Role of the CaMKII/ NMDA receptor complex in the maintenance of synaptic strength. J Neurosci 31:9170-9178.
52. Schmitt JM, Wayman GA, Nozaki N, Soderling TR (2004) Calcium activation of ERK mediated by calmodulin kinase I. J Biol Chem 279:24064-24072.
53. Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162-166.
54. +] signaling in individual hippocampal dendritic spines. J Neurosci 25:6037-6046.
55. Steward O, Huang F, Guzowski JF (2007) A form of perforant path LTP can occur without ERK1/2 phosphorylation or immediate early gene induction. Learn Mem 14:433-445.
56. Strack S, Colbran RJ (1998) Autophosphorylation-dependent targeting of calcium/ calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 273:20689-20692.
57. Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neuro-chem 76:1-10.
58. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317.
59. Sweatt JD (2009) Experience-dependent epigenetic modifications in the central nervous system. Biol Psychiatry 65:191-197.
60. Thomas CG, Miller AJ, Westbrook GL (2006) Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J Neurophysiol 95:1727-1734.
61. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183.
62. Tolias KF, Duman JG, Um K (2011) Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog Neurobiol 94:133-148.
63. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
64. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
65. Vest RS, Davies KD, O'Leary H, Port JD, Bayer KU (2007) Dual mechanism of a natural CaMKII inhibitor. Mol Biol Cell 18:5024-5033.
66. von Engelhardt J, Doganci B, Jensen V, Hvalby Ø, Göngrich C, Taylor A, Barkus C, Sanderson DJ, Rawlins JN, Seeburg PH, Bannerman DM, Monyer H (2008) Contribution of hippocampal and extra-hippo-campal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 60:846-860.
67. Wang CC, Held RG, Chang SC, Yang L, Delpire E, Ghosh A, Hall BJ (2011) A critical role for GluN2B-containing NMDA receptors in cortical development and function. Neuron 72:789-805.
68. Wang JQ, Tang Q, Parelkar NK, Liu Z, Samdani S, Choe ES, Yang L, Mao L (2004) Glutamate signaling to Ras-MAPK in striatal neurons: mechanisms for inducible gene expression and plasticity. Mol Neurobiol 29:1-14.
69. Wang XB, Zhou Q (2010) Spine remodeling and synaptic modification. Mol Neurobiol 41:29-41.
70. Wayman GA, Lee YS, Tokumitsu H, Silva AJ, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59:914-931.
71. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
72. Xiao L, Hu C, Feng C, Chen Y (2011) Switching of N-methyl-D-aspartate (NMDA) receptor-favorite intracellular signal pathways from ERK1/2 protein to p38 mitogen-activated protein kinase leads to developmental changes in NMDA neurotoxicity. J Biol Chem 286:20175-20193.
73. Yoshimura Y, Shinkawa T, Taoka M, Kobayashi K, Isobe T, Yamauchi T (2002) Identification of protein substrates of Ca(2 +)/calmodulin-dependent protein kinase II in the postsynaptic density by protein sequencing and mass spectrometry. Biochem Biophys Res Commun 290:948-954.
74. Yoshimura Y, Ohmura T, Komatsu Y (2003) Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex. J Neurosci 23:6557-6566.
75. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M (2005) Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47:859-872.
76. Zhou Y, Takahashi E, Li W, Halt A, Wiltgen B, Ehninger D, Li GD, Hell JW, Kennedy MB, Silva AJ (2007) Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 27:13843-13853.
77. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R (2002) Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110:443-455.