CaMKII-dependent phosphorylation of GluK5 mediates plasticity of kainate receptors

EMBO Journal

Volumn 32, Issue 4, 2013, Pages 496-510

  Carta, Mario ^a   Opazo, Patrizio ^a   Veran, Julien ^a   Athané, Axel ^a   Choquet, Daniel ^a   Coussen, Françoise ^a   Mulle, Christophe ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

CaMKII; glutamate receptors; hippocampal mossy fibres; kainate receptors; plasticity

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GLUK5 PROTEIN; KAINIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE LOCUS; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; HUMAN; HUMAN CELL; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CERCOPITHECUS AETHIOPS; COS CELLS; GUANYLATE KINASE; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECEPTORS, KAINIC ACID; SYNAPSES;

EID: 84875210694     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.334     Document Type: Article

References (57)

1. Barberis A, Sachidhanandam S, Mulle C (2008) GluR6/KA2 kainate receptors mediate slow-deactivating currents. J Neurosci 28: 6402-6406
2. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276: 2042-2045
3. Bats C, Groc L, Choquet D (2007) The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53: 719-734
4. Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31: 25-46
5. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2: 315-324
6. Chamberlain SE, Gonzalez-Gonzalez IM, Wilkinson KA, Konopacki FA, Kantamneni S, Henley JM, Mellor JR (2012) SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat Neurosci 15: 845-852
7. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408: 936-943
8. Contractor A, Mulle C, Swanson GT (2011) Kainate receptors coming of age: milestones of two decades of research. Trends Neurosci 34: 154-163
9. Contractor A, Sailer AW, Darstein M, Maron C, Xu J, Swanson GT, Heinemann SF (2003) Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2-/-mice. J Neurosci 23: 422-429
10. Coussen F, Normand E, Marchal C, Costet P, Choquet D, Lambert M, Mege RM, Mulle C (2002) Recruitment of the kainate receptor subunit glutamate receptor 6 by cadherin/catenin complexes. J Neurosci 22: 6426-6436
11. Coussen F, Perrais D, Jaskolski F, Sachidhanandam S, Normand E, Bockaert J, Marin P, Mulle C (2005) Co-assembly of two GluR6 kainate receptor splice variants within a functional protein complex. Neuron 47: 555-566
12. Derkach VA, Oh MC, Guire ES, Soderling TR (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8: 101-113
13. Fernandes HB, Catches JS, Petralia RS, Copits BA, Xu J, Russell TA, Swanson GT, Contractor A (2009) High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 63: 818-829
14. Gallyas Jr. F, Ball SM, Molnar E (2003) Assembly and cell surface expression of KA-2 subunit-containing kainate receptors. J Neurochem 86: 1414-1427
15. Garcia EP, Mehta S, Blair LA, Wells DG, Shang J, Fukushima T, Fallon JR, Garner CC, Marshall J (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21: 727-739
16. Ghetti A, Heinemann SF (2000) NMDA-Dependent modulation of hippocampal kainate receptors by calcineurin and Ca(2\+)/calmodulin-dependent protein kinase. J Neurosci 20: 2766-2773
17. Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, Andreev D, De Zeeuw CI, Elgersma Y (2006) alphaCaMKII is essential for cerebellar LTD and motor learning. Neuron 51: 835-843
18. Hirbec H, Francis JC, Lauri SE, Braithwaite SP, Coussen F, Mulle C, Dev KK, Coutinho V, Meyer G, Isaac JT, Collingridge GL, Henley JM (2003) Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37: 625-638
19. Jaskolski F, Coussen F, Nagarajan N, Normand E, Rosenmund C, Mulle C (2004) Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J Neurosci 24: 2506-2515
20. Jaskolski F, Mayo-Martin B, Jane D, Henley JM (2009) Dynamindependent membrane drift recruits AMPA receptors to dendritic spines. J Biol Chem 284: 12491-12503
21. Jaskolski F, Mulle C, Manzoni OJ (2005) An automated method to quantify and visualize colocalized fluorescent signals. J Neurosci Methods 146: 42-49
22. Kornreich BG, Niu L, Roberson MS, Oswald RE (2007) Identification of C-terminal domain residues involved in protein kinase A-mediated potentiation of kainate receptor subtype 6. Neuroscience 146: 1158-1168
23. Kristensen AS, Jenkins MA, Banke TG, Schousboe A, Makino Y, Johnson RC, Huganir R, Traynelis SF (2011) Mechanism of Ca(2\+)/calmodulin-dependent kinase II regulation of AMPA receptor gating. Nat Neurosci 14: 727-735
24. Kwon HB, Castillo PE (2008) Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron 57: 108-120
25. Lee HK, Takamiya K, He K, Song L, Huganir RL (2010) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103: 479-489
26. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3: 175-190
27. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24: 649-658
28. Makino H, Malinow R (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64: 381-390
29. Mammen AL, Huganir RL, O'Brien RJ (1997) Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci 17: 7351-7358
30. Marchal C, Mulle C (2004) Postnatal maturation of mossy fibre excitatory transmission in mouse CA3 pyramidal cells: a potential role for kainate receptors. J Physiol 561(Part 1): 27-37
31. Martin S, Henley JM (2004) Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways. EMBO J 23: 4749-4759
32. Martin S, Nishimune A, Mellor JR, Henley JM (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447: 321-325
33. Melyan Z, Lancaster B, Wheal HV (2004) Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 24: 4530-4534
34. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392: 601-605
35. Nasu-Nishimura Y, Hurtado D, Braud S, Tang TT, Isaac JT, Roche KW (2006) Identification of an endoplasmic reticulum-retention motif in an intracellular loop of the kainate receptor subunit KA2. J Neurosci 26: 7014-7021
36. Nasu-Nishimura Y, Jaffe H, Isaac JT, Roche KW (2010) Differential regulation of kainate receptor trafficking by phosphorylation of distinct sites on GluR6. J Biol Chem 285: 2847-2856
37. Newton AJ, Kirchhausen T, Murthy VN (2006) Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci USA 103: 17955-17960
38. Nicoll RA, Schmitz D (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6: 863-876
39. O'Brien JA, Lummis SC (2006) Biolistic transfection of neuronal cultures using a hand-held gene gun. Nat Protoc 1: 977-981
40. Opazo P, Choquet D (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46: 1-8
41. 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
42. Park Y, Jo J, Isaac JT, Cho K (2006) Long-term depression of kainate receptor-mediated synaptic transmission. Neuron 49: 95-106
43. Perrais D, Veran J, Mulle C (2010) Gating and permeation of kainate receptors: differences unveiled. Trends Pharmacol Sci 31: 516-522
44. Pinheiro PS, Lanore F, Veran J, Artinian J, Blanchet C, Crepel V, Perrais D, Mulle C (2012) Selective block of postsynaptic kainate receptors reveals their function at hippocampal mossy fiber synapses. Cereb Cortex (advance online publication 17 February 2012; doi: 10.1093/cercor/bhs022
45. Rebola N, Carta M, Lanore F, Blanchet C, Mulle C (2011) NMDA receptor-dependent metaplasticity at hippocampal mossy fiber synapses. Nat Neurosci 14: 691-693
46. Rebola N, Lujan R, Cunha RA, Mulle C (2008) Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron 57: 121-134
47. Rebola N, Sachidhanandam S, Perrais D, Cunha RA, Mulle C (2007) Short-term plasticity of kainate receptor-mediated EPSCs induced by NMDA receptors at hippocampal mossy fiber synapses. J Neurosci 27: 3987-3993
48. Ren Z, Riley NJ, Garcia EP, Sanders JM, Swanson GT, Marshall J (2003) Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 23: 6608-6616
49. Rivera R, Rozas JL, Lerma J (2007) PKC-dependent autoregulation of membrane kainate receptors. EMBO J 26: 4359-4367
50. Ruiz A, Sachidhanandam S, Utvik JK, Coussen F, Mulle C (2005) Distinct subunits in heteromeric kainate receptors mediate ionotropic and metabotropic function at hippocampal mossy fiber synapses. J Neurosci 25: 11710-11718
51. Rumbaugh G, Vicini S (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19: 10603-10610
52. Sachidhanandam S, Blanchet C, Jeantet Y, Cho YH, Mulle C (2009) Kainate receptors act as conditional amplifiers of spike transmission at hippocampal mossy fiber synapses. J Neurosci 29: 5000-5008
53. Selak S, Paternain AV, Aller MI, Pico E, Rivera R, Lerma J (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63: 357-371
54. Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284: 162-166
55. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182
56. Yamagata Y, Kobayashi S, Umeda T, Inoue A, Sakagami H, Fukaya M, Watanabe M, Hatanaka N, Totsuka M, Yagi T, Obata K, Imoto K, Yanagawa Y, Manabe T, Okabe S (2009) Kinase-dead knock-in mouse reveals an essential role of kinase activity of Ca2\+/calmodulin-dependent protein kinase IIalpha in dendritic spine enlargement, long-term potentiation, and learning. J Neurosci 29: 7607-7618
57. Yan JZ, Xu Z, Ren SQ, Hu B, Yao W, Wang SH, Liu SY, Lu W (2011) Protein kinase C promotes N-methyl-D-aspartate (NMDA) receptor trafficking by indirectly triggering calcium/calmodulin-dependent protein kinase II (CaMKII) autophosphorylation. J Biol Chem 286: 25187-25200