Glutamate receptor δ2 associates with metabotropic glutamate receptor 1 (mGluR1), protein kinase Cγ, and canonical transient receptor potential 3 and regulates mGluR1-mediated synaptic transmission in cerebellar Purkinje neurons

Journal of Neuroscience

Volumn 32, Issue 44, 2012, Pages 15296-15308

  Kato, Akihiko S ^a   Knierman, Michael D ^a   Siuda, Edward R ^a   Isaac, John T R ^a   Nisenbaum, Eric S ^a   Bredt, David S ^a  

^a ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; GLUTAMATE RECEPTOR 2; METABOTROPIC RECEPTOR 1; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE C GAMMA; SYNAPTOPHYSIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3;

ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MASS SPECTROMETRY; MOTOR COORDINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PROTEIN KINASE C; PURKINJE CELLS; RECEPTORS, CELL SURFACE; RECEPTORS, GLUTAMATE; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SOLUBILITY; SUBCELLULAR FRACTIONS; SYNAPTIC TRANSMISSION; TRPC CATION CHANNELS;

EID: 84868156534     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0705-12.2012     Document Type: Article

References (77)

1. 2 homeostasis. J Biol Chem 283:19854-19863.
2. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
3. Araki K, Meguro H, Kushiya E, Takayama C, Inoue Y, Mishina M (1993) Selective expression of the glutamate receptor channel delta 2 subunit in cerebellar Purkinje cells. Biochem Biophys Res Commun 197:1267-1276.
4. Armstrong CL, Duffin CA, McFarland R, Vogel MW (2011) Mechanisms of compartmental Purkinje cell death and survival in the lurcher mutant mouse. Cerebellum 10:504-514.
5. Batchelor AM, Garthwaite J (1993) Novel synaptic potentials in cerebellar Purkinje cells: probable mediation by metabotropic glutamate receptors. Neuropharmacology 32:11-20.
6. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63:911-915.
7. Becker EB, Oliver PL, Glitsch MD, Banks GT, Achilli F, Hardy A, Nolan PM, Fisher EM, Davies KE (2009) A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci U S A 106:6706-6711.
8. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, Hashimoto K, Thompson RF, Tonegawa S (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice. Cell 83:1233-1242.
9. Ciruela F, Soloviev MM, McIlhinney RA (1999) Cell surface expression of the metabotropic glutamate receptor type 1alpha is regulated by the C-terminal tail. FEBS Lett 448:91-94.
10. Coesmans M, Smitt PA, Linden DJ, Shigemoto R, Hirano T, Yamakawa Y, van Alphen AM, Luo C, van der Geest JN, Kros JM, Gaillard CA, Frens MA, de Zeeuw CI (2003) Mechanisms underlying cerebellar motor deficits due to mGluR1-autoantibodies. Ann Neurol 53:325-336.
11. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, Collingridge GL, Crépel F (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237-243.
12. Ehrengruber MU, Kato A, Inokuchi K, Hennou S (2004) Homer/Vesl proteins and their roles in CNS neurons. Mol Neurobiol 29:213-227.
13. Fukuoka T, Takeda H, Ohe Y, Deguchi I, Takahashi Y, Tanahashi N (2012) Anti-glutamate receptor delta2 antibody-positive migrating focal encephalitis. Clin Neurol Neurosurg. Advance online publication. Retrieved September 17, 2012.
14. Glitsch MD (2010) Activation of native TRPC3 cation channels by phospholipase D. FASEB J 24:318-325.
15. Hale JE, Butler JP, Gelfanova V, You JS, Knierman MD (2004) A simplified procedure for the reduction and alkylation of cysteine residues in proteins prior to proteolytic digestion and mass spectral analysis. Anal Biochem 333:174-181.
16. Hartmann J, Konnerth A (2009) Mechanisms of metabotropic glutamate receptor-mediated synaptic signaling in cerebellar Purkinje cells. Acta Physiol (Oxf) 195:79-90.
17. Hartmann J, Blum R, Kovalchuk Y, Adelsberger H, Kuner R, Durand GM, Miyata M, Kano M, Offermanns S, Konnerth A (2004) Distinct roles of G q and G 11 for Purkinje cell signaling and motor behavior. J Neurosci 24:5119-5130.
18. Hartmann J, Dragicevic E, Adelsberger H, Henning HA, Sumser M, Abramowitz J, Blum R, Dietrich A, Freichel M, Flockerzi V, Birnbaumer L, Konnerth A (2008) TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 59:392-398.
19. Hashimoto K, Miyata M, Watanabe M, Kano M (2001a) Roles of phospholipase Cbeta4 in synapse elimination and plasticity in developing and mature cerebellum. Mol Neurobiol 23:69-82.
20. Hashimoto K, Ichikawa R, Takechi H, Inoue Y, Aiba A, Sakimura K, Mishina M, Hashikawa T, Konnerth A, Watanabe M, Kano M (2001b) Roles of glutamate receptor 2 subunit (GluR 2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development. J Neurosci 21:9701-9712.
21. Hirano T (2012) Glutamate-receptor-like molecule GluRdelta2 involved in synapse formation at parallel fiber-Purkinje neuron synapses. Cerebellum 11:71-77.
22. Hironaka K, Umemori H, Tezuka T, Mishina M, Yamamoto T (2000) The protein-tyrosine phosphatase PTPMEG interacts with glutamate receptor delta 2 and epsilon subunits. J Biol Chem 275:16167-16173.
23. Inoue T, Kato K, Kohda K, Mikoshiba K (1998) Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J Neurosci 18:5366-5373.
24. Jo K, Derin R, Li M, Bredt DS (1999) Characterization of MALS/Velis-1,-2, and-3: a family of mammalian LIN-7 homologs enriched at brain synapses in association with the postsynaptic density-95/NMDA receptor postsynaptic complex. J Neurosci 19:4189-4199.
25. Joo JY, Lee SJ, Uemura T, Yoshida T, Yasumura M, Watanabe M, Mishina M (2011) Differential interactions of cerebellin precursor protein (Cbln) subtypes and neurexin variants for synapse formation of cortical neurons. Biochem Biophys Res Commun 406:627-632.
26. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, Inoue Y, Tonegawa S (1995) Impaired synapse elimination during cerebellar development in PKC gamma mutant mice. Cell 83:1223-1231.
27. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
28. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81: 245-252.
29. Kato AS, Zhou W, Milstein AD, Knierman MD, Siuda ER, Dotzlaf JE, Yu H, Hale JE, Nisenbaum ES, Nicoll RA, Bredt DS (2007) New transmembrane AMPA receptor regulatory protein isoform, γ-7, differentially regulates AMPA receptors. J Neurosci 27:4969-4977.
30. Kato AS, Gill MB, Ho MT, Yu H, Tu Y, Siuda ER, Wang H, Qian YW, Nisenbaum ES, Tomita S, Bredt DS (2010) Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins. Neuron 68:1082-1096.
31. Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ (2003) Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426:285-291.
32. Kinno R, Yamazaki T, Yamamoto M, Takahashi Y, Fukui T, Kinugasa E (2012) Cerebellar symptoms in a case of acute limbic encephalitis associated with autoantibodies to glutamate receptors delta2 and epsilon2. Clin Neurol Neurosurg. Advance online publication. Retrieved September 17, 2012.
33. Knöpfel T, Grandes P (2002) Metabotropic glutamate receptors in the cerebellum with a focus on their function in Purkinje cells. Cerebellum 1:19-26.
34. Kubota M, Takahashi Y (2008) Steroid-responsive chronic cerebellitis with positive glutamate receptor delta 2 antibody. J Child Neurol 23:228-230.
35. Kumpost J, Syrova Z, Kulihova L, Frankova D, Bologna JC, Hlavackova V, Prezeau L, Kralikova M, Hruskova B, Pin JP, Blahos J (2008) Surface expression of metabotropic glutamate receptor variants mGluR1a and mGluR1b in transfected HEK293 cells. Neuropharmacology 55:409-418.
36. Kurihara H, Hashimoto K, Kano M, Takayama C, Sakimura K, Mishina M, Inoue Y, Watanabe M (1997) Impaired parallel fiber3 Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor 2 subunit. J Neurosci 17:9613-9623.
37. Kuroyanagi T, Yokoyama M, Hirano T (2009) Postsynaptic glutamate receptor delta family contributes to presynaptic terminal differentiation and establishment of synaptic transmission. Proc Natl Acad Sci U S A 106:4912-4916.
38. Lalouette A, Lohof A, Sotelo C, Guénet J, Mariani J (2001) Neurobiological effects of a null mutation depend on genetic context: comparison between two hotfoot alleles of the delta-2 ionotropic glutamate receptor. Neuroscience 105:443-455.
39. Lee SJ, Uemura T, Yoshida T, Mishina M (2012) GluR 2 assembles four neurexins into trans-synaptic triad to trigger synapse formation. J Neurosci 32:4688-4701.
40. Levenes C, Daniel H, Crépel F (1998) Long-term depression of synaptic transmission in the cerebellum: cellular and molecular mechanisms revisited. Prog Neurobiol 55:79-91.
41. Lomeli H, Sprengel R, Laurie DJ, Köhr G, Herb A, Seeburg PH, Wisden W (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett 315:318-322.
42. MacLean DM (2009) The 2 glutamate-like receptor undergoes similar conformational changes as other ionotropic glutamate receptors. J Neurosci 29:6767-6768.
43. Mandolesi G, Cesa R, Autuori E, Strata P (2009) An orphan ionotropic glutamate receptor: the delta2 subunit. Neuroscience 158:67-77.
44. Marignier R, Chenevier F, Rogemond V, Sillevis Smitt P, Renoux C, Cavillon G, Androdias G, Vukusic S, Graus F, Honnorat J, Confavreux C (2010) Metabotropic glutamate receptor type 1 autoantibody-associated cerebellitis: a primary autoimmune disease? Arch Neurol 67:627-630.
45. Matilla-Dueñas A, Sánchez I, Corral-Juan M, Dávalos A, Alvarez R, Latorre P (2010) Cellular and molecular pathways triggering neurodegeneration in the spinocerebellar ataxias. Cerebellum 9:148-166.
46. Matsuda K, Yuzaki M (2011) Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions. Eur J Neurosci 33:1447-1461.
47. Matsuda K, Miura E, Miyazaki T, Kakegawa W, Emi K, Narumi S, Fukazawa Y, Ito-Ishida A, Kondo T, Shigemoto R, Watanabe M, Yuzaki M (2010) Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 328:363-368.
48. Matsuda S, Yuzaki M (2002) Mutation in hotfoot-4J mice results in retention of delta2 glutamate receptors in ER. Eur J Neurosci 16:1507-1516.
49. Matsumoto H, Okabe S, Hirakawa-Yamada M, Takahashi Y, Satoh N, Igeta Y, Hashida H (2012) Steroid-responsive focal epilepsy with focal dystonia accompanied by glutamate receptor delta2 antibody. J Neuroimmunol 249:101-104.
50. Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno J, Sakakibara S, Yamada M, Yoneshima H, Miyawaki A, Fukuuchi Y, Furuichi T, Okano H, Mikoshiba K, Noda T (1996) Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379:168-171.
51. Miyagi Y, Yamashita T, Fukaya M, Sonoda T, Okuno T, Yamada K, Watanabe M, Nagashima Y, Aoki I, Okuda K, Mishina M, Kawamoto S (2002) Delphilin: a novel PDZ and formin homology domain-containing protein that synaptically colocalizes and interacts with glutamate receptor 2 subunit. J Neurosci 22:803-814.
52. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y, Jun K, Wu D, Kano M, Shin HS (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur J Neurosci 13:1945-1954.
53. Nishizuka Y (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607-614.
54. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Galphaq. Proc Natl Acad Sci U S A 94:14089-14094.
55. Pin JP, Waeber C, Prezeau L, Bockaert J, Heinemann SF (1992) Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc Natl Acad Sci U S A 89:10331-10335.
56. Reichelt W, Knöpfel T (2002) Glutamate uptake controls expression of a slow postsynaptic current mediated by mGluRs in cerebellar Purkinje cells. J Neurophysiol 87:1974-1980.
57. Roche KW, Ly CD, Petralia RS, Wang YX, McGee AW, Bredt DS, Wenthold RJ (1999) Postsynaptic density-93 interacts with the 2 glutamate receptor subunit at parallel fiber synapses. J Neurosci 19:3926-3934.
58. Schmid SM, Hollmann M (2008) To gate or not to gate: are the delta subunits in the glutamate receptor family functional ion channels? Mol Neurobiol 37:126-141.
59. Schmitt-Ulms G, Hansen K, Liu J, Cowdrey C, Yang J, DeArmond SJ, Cohen FE, Prusiner SB, Baldwin MA (2004) Time-controlled transcardiac perfusion cross-linking for the study of protein interactions in complex tissues. Nat Biotechnol 22:724-731.
60. Shiihara T, Kato M, Konno A, Takahashi Y, Hayasaka K (2007) Acute cerebellar ataxia and consecutive cerebellitis produced by glutamate receptor delta2 autoantibody. Brain Dev 29:254-256.
61. Shimokaze T, Kato M, Yoshimura Y, Takahashi Y, Hayasaka K (2007) A case of acute cerebellitis accompanied by autoantibodies against glutamate receptor delta2. Brain Dev 29:224-226.
62. Sillevis Smitt P, Kinoshita A, De Leeuw B, Moll W, Coesmans M, Jaarsma D, Henzen-Logmans S, Vecht C, De Zeeuw C, Sekiyama N, Nakanishi S, Shigemoto R (2000) Paraneoplastic cerebellar ataxia due to auto-antibodies against a glutamate receptor. N Engl J Med 342:21-27.
63. Soloviev MM, Ciruela F, Chan WY, McIlhinney RA (1999) Identification, cloning and analysis of expression of a new alternatively spliced form of the metabotropic glutamate receptor mGluR1 mRNA1. Biochim Biophys Acta 1446:161-166.
64. Sumner LW, Wolf-Sumner B, White SP, Asirvatham VS (2002) Silver stain removal using H2O2 for enhanced peptide mass mapping by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 16:160-168.
65. Takayasu Y, Iino M, Ozawa S (2004) Roles of glutamate transporters in shaping excitatory synaptic currents in cerebellar Purkinje cells. Eur J Neurosci 19:1285-1295.
66. Takeuchi T, Miyazaki T, Watanabe M, Mori H, Sakimura K, Mishina M (2005) Control of synaptic connection by glutamate receptor 2 in the adult cerebellum. J Neurosci 25:2146-2156.
67. Tempia F, Alojado ME, Strata P, Knöpfel T (2001) Characterization of the mGluR(1)-mediated electrical and calcium signaling in Purkinje cells of mouse cerebellar slices. J Neurophysiol 86:1389-1397.
68. Trebak M, Vazquez G, Bird GS, Putney JW Jr (2003) The TRPC3/6/7 subfamily of cation channels. Cell Calcium 33:451-461.
69. Uemura T, Mishina M (2008) The amino-terminal domain of glutamate receptor delta2 triggers presynaptic differentiation. Biochem Biophys Res Commun 377:1315-1319.
70. Uemura T, Mori H, Mishina M (2004) Direct interaction of GluRdelta2 with Shank scaffold proteins in cerebellar Purkinje cells. Mol Cell Neurosci 26:330-341.
71. Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T, Ra M, Taguchi R, Sakimura K, Mishina M (2010) Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141:1068-1079.
72. Venkatachalam K, Zheng F, Gill DL (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 278:29031-29040.
73. Xiao B, Tu JC, Worley PF (2000) Homer: a link between neural activity and glutamate receptor function. Curr Opin Neurobiol 10:370-374.
74. Yamasaki M, Miyazaki T, Azechi H, Abe M, Natsume R, Hagiwara T, Aiba A, Mishina M, Sakimura K, Watanabe M (2011) Glutamate receptor 2 is essential for input pathway-dependent regulation of synaptic AMPAR contents in cerebellar Purkinje cells. J Neurosci 31:3362-3374.
75. Yasumura M, Uemura T, Yamasaki M, Sakimura K, Watanabe M, Mishina M (2008) Role of the internal Shank-binding segment of glutamate receptor delta2 in synaptic localization and cerebellar functions. Neurosci Lett 433:146-151.
76. Yawata S, Tsuchida H, Kengaku M, Hirano T (2006) Membrane-proximal region of glutamate receptor 2 subunit is critical for long-term depression and interaction with protein interacting with C kinase 1 in a cerebellar Purkinje neuron. J Neurosci 26:3626-3633.
77. Yuzaki M (2011) Cbln1 and its family proteins in synapse formation and maintenance. Curr Opin Neurobiol 21:215-220.