Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression

Neuron

Volumn 49, Issue 6, 2006, Pages 845-860

  Steinberg, Jordan P ^a   Takamiya, Kogo ^a   Shen, Ying ^a   Xia, Jun ^b   Rubio, Maria E ^c   Yu, Sandy ^a   Jin, Wenying ^b   Thomas, Gareth M ^a   Linden, David J ^a   Huganir, Richard L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 2; MUTANT PROTEIN; PDZ PROTEIN; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C; PROTEIN SUBUNIT;

ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CEREBELLUM CORTEX; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE MUTATION; GENETIC TRANSFECTION; KNOCKOUT MOUSE; LONG TERM DEPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; TISSUE CULTURE; WILD TYPE;

AGE FACTORS; ALANINE; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CARRIER PROTEINS; CELLS, CULTURED; CEREBELLUM; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIPIDS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; LYSINE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICROSCOPY, IMMUNOELECTRON; MUTAGENESIS; MUTATION; NEURONS; NUCLEAR PROTEINS; PATCH-CLAMP TECHNIQUES; PHORBOL ESTERS; RECEPTORS, AMPA; TRANSFECTION;

EID: 33644872978     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.02.025     Document Type: Article

References (42)

1. A. Aiba, M. Kano, C. Chen, M.E. Stanton, G.D. Fox, K. Herrup, T.A. Zwingman, and S. Tonegawa Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice Cell 79 1994 377 388
2. A. Baude, E. Molnar, D. Latawiec, R.A. McIlhinney, and P. Somogyi Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum J. Neurosci. 14 1994 2830 2843
3. M.F. Bear, and D.J. Linden The mechanisms and meaning of long-term synaptic depression in the mammalian brain W.M. Cowan K. Davies The Synapse 2000 Johns Hopkins University Press Baltimore, MD 455 517
4. T.A. Blanpied, D.B. Scott, and M.D. Ehlers Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines Neuron 36 2002 435 449
5. E.S. Boyden, A. Katoh, and J.L. Raymond Cerebellum-dependent learning: the role of multiple plasticity mechanisms Annu. Rev. Neurosci. 27 2004 581 609
6. H.J. Chung, J. Xia, R.H. Scannevin, X. Zhang, and R.L. Huganir Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins J. Neurosci. 20 2000 7258 7267
7. H.J. Chung, J.P. Steinberg, R.L. Huganir, and D.J. Linden Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression Science 300 2003 1751 1755
8. C.I. De Zeeuw, C. Hansel, F. Bian, S.K. Koekkoek, A.M. van Alphen, D.J. Linden, and J. Oberdick Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex Neuron 20 1998 495 508
9. K.K. Dev, A. Nishimune, J.M. Henley, and S. Nakanishi The protein kinase C alpha binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits Neuropharmacology 38 1999 635 644
10. R. Feil, J. Hartmann, C. Luo, W. Wolfsgruber, K. Schilling, S. Feil, J.J. Barski, M. Meyer, A. Konnerth, C.I. De Zeeuw, and F. Hofmann Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I J. Cell Biol. 163 2003 295 302
11. S.M. Gardner, K. Takamiya, J. Xia, J.G. Suh, R. Johnson, S. Yu, and R.L. Huganir Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF Neuron 45 2005 903 915
12. B. Habermann The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5 2004 250 255
13. M. Ito The molecular organization of cerebellar long-term depression Nat. Rev. Neurosci. 3 2002 896 902
14. N. Kashiwabuchi, K. Ikeda, K. Araki, T. Hirano, K. Shibuki, C. Takayama, Y. Inoue, T. Kutsuwada, T. Yagi, and Y. Kang Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice Cell 81 1995 245 252
15. B.E. Kemp, and R.B. Pearson Protein kinase recognition sequence motifs Trends Biochem. Sci. 15 1990 342 346
16. Y. Kishimoto, S. Kawahara, M. Suzuki, H. Mori, M. Mishina, and Y. Kirino Classical eyeblink conditioning in glutamate receptor subunit delta 2 mutant mice is impaired in the delay paradigm but not in the trace paradigm Eur. J. Neurosci. 13 2001 1249 1253
17. S.K. Koekkoek, H.C. Hulscher, B.R. Dortland, R.A. Hensbroek, Y. Elgersma, T.J. Ruigrok, and C.I. De Zeeuw Cerebellar LTD and learning-dependent timing of conditioned eyelid responses Science 301 2003 1736 1739
18. M. Leitges, J. Kovac, M. Plomann, and D.J. Linden A unique PDZ ligand in PKCalpha confers induction of cerebellar long-term synaptic depression Neuron 44 2004 585 594
19. D.J. Linden The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance Proc. Natl. Acad. Sci. USA 98 2001 14066 14071
20. D.J. Linden Neuroscience. From molecules to memory in the cerebellum Science 301 2003 1682 1685
21. D.J. Linden, and J.A. Connor Participation of postsynaptic PKC in cerebellar long-term depression in culture Science 254 1991 1656 1659
22. S.Q. Liu, and S.G. Cull-Candy Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype Nature 405 2000 454 458
23. 2+ permeability of AMPARs at cerebellar synapses Nat. Neurosci. 8 2005 768 775
24. W. Lu, and E.B. Ziff PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking Neuron 47 2005 407 421
25. S. Matsuda, S. Mikawa, and H. Hirai Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein J. Neurochem. 73 1999 1765 1768
26. S. Matsuda, T. Launey, S. Mikawa, and H. Hirai Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons EMBO J. 19 2000 2765 2774
27. K. Matsui, C.E. Jahr, and M.E. Rubio High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release J. Neurosci. 25 2005 7538 7547
28. J.L. Perez, L. Khatri, C. Chang, S. Srivastava, P. Osten, and E.B. Ziff PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2 J. Neurosci. 21 2001 5417 5428
29. B.J. Peter, H.M. Kent, I.G. Mills, Y. Vallis, P.J. Butler, P.R. Evans, and H.T. McMahon BAR domains as sensors of membrane curvature: the amphiphysin BAR structure Science 303 2004 495 499
30. B. Racz, T.A. Blanpied, M.D. Ehlers, and R.J. Weinberg Lateral organization of endocytic machinery in dendritic spines Nat. Neurosci. 7 2004 917 918
31. M.E. Rubio, and F. Soto Distinct Localization of P2X receptors at excitatory postsynaptic specializations J. Neurosci. 21 2001 641 653
32. G. Rumbaugh, G.M. Sia, C.C. Garner, and R.L. Huganir Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons J. Neurosci. 23 2003 4567 4576
33. K.J. Seidenman, J.P. Steinberg, R. Huganir, and R. Malinow Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells J. Neurosci. 23 2003 9220 9228
34. K. Shibuki, H. Gomi, L. Chen, S. Bao, J.J. Kim, H. Wakatsuki, T. Fujisaki, K. Fujimoto, A. Katoh, and T. Ikeda Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice Neuron 16 1996 587 599
35. Z. Songyang, A.S. Fanning, C. Fu, J. Xu, S.M. Marfatia, A.H. Chishti, A. Crompton, A.C. Chan, J.M. Anderson, and L.C. Cantley Recognition of unique carboxyl-terminal motifs by distinct PDZ domains Science 275 1997 73 77
36. J. Staudinger, J. Zhou, R. Burgess, S.J. Elledge, and E.N. Olson PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system J. Cell Biol. 128 1995 263 271
37. J. Staudinger, J. Lu, and E.N. Olson Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha J. Biol. Chem. 272 1997 32019 32024
38. J.P. Steinberg, R.L. Huganir, and D.J. Linden N-ethylmaleimide-sensitive factor is required for the synaptic incorporation and removal of AMPA receptors during cerebellar long-term depression Proc. Natl. Acad. Sci. USA 101 2004 18212 18216
39. C. Tarricone, B. Xiao, N. Justin, P.A. Walker, K. Rittinger, S.J. Gamblin, and S.J. Smerdon The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways Nature 411 2001 215 219
40. Y.T. Wang, and D.J. Linden Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis Neuron 25 2000 635 647
41. J. Xia, X. Zhang, J. Staudinger, and R.L. Huganir Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1 Neuron 22 1999 179 187
42. J. Xia, H.J. Chung, C. Wihler, R.L. Huganir, and D.J. Linden Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins Neuron 28 2000 499 510