The synaptic targeting of mGluR1 by Its carboxyl-terminal domain is crucial for cerebellar function

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2702-2712

  Ohtani, Yoshiaki ^a   Miyata, Mariko ^b,c,d   Hashimoto, Kouichi ^d,e,m   Tabata, Toshihide ^f   Kishimoto, Yasushi ^g   Fukaya, Masahiro ^h   Kase, Daisuke ^b   Kassai, Hidetoshi ^a,i   Nakao, Kazuki ^i,j   Hirata, Tatsumi ^k   Watanabe, Masahiko ^l   Kano, Masanobu ^e   Aiba, Atsu ^a,i  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f UNIVERSITY OF TOYAMA   (Japan)

^g TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^h KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

ⁱ UNIVERSITY OF TOKYO   (Japan)

^j RIKEN Center for Biosystems Dynamics Research   (Japan)

^k GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^l HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^m HIROSHIMA UNIVERSITY   (Japan)

more..

Author keywords

Cerebellum; Eyeblink conditioning; LTD; mGluR1; Purkinje cells; Synapse elimination

Indexed keywords

CEREBELLUM; EYEBLINK CONDITIONING; LTD; MGLUR1; PURKINJE CELLS; SYNAPSE ELIMINATION;

ANIMALS; CEREBELLUM; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84893651363     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3542-13.2014     Document Type: Article

References (62)

1. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, Tonegawa S (1994a) Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in m Glu R1 mutant mice. Cell 79:365-375. CrossRef Medline
2. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994b) Deficient cerebellar long-term depression and impaired motor learning in m Glu R1 mutant mice. Cell 79:377-388. CrossRef Medline
3. Batchelor AM, Garthwaite J (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385:74-77. CrossRef Medline
4. 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. CrossRef Medline
5. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700. CrossRef Medline
6. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking m Glu R1. Nature 372: 237-243. CrossRef Medline
7. Dale LB, Bhattacharya M, Anborgh PH, Murdoch B, Bhatia M, Nakanishi S, Ferguson SS (2000) G protein-coupled receptor kinase-mediated desentization of metabotropic glutamate receptor 1A protects against cell death. J Biol Chem 275:38213-38220. CrossRef Medline
8. Das SS, Banker GA (2006) The role of protein interaction motifs in regulating the polarity and clustering of the metabotropic glutamate receptor m Glu R1a. J Neurosci 26:8115-8125. CrossRef Medline
9. Ferraguti F, Crepaldi L, Nicoletti F (2008) Metabotropic glutamate 1 receptor: current concepts and perspectives. Pharmacol Rev 60:536-581. CrossRef Medline
10. Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396:753-756. CrossRef Medline
11. Flor PJ, Gomeza J, Tones MA, Kuhn R, Pin JP, Knöpfel T (1996) The C-terminal domain of the m Glu R1 metabotropic glutamate receptor affects sensitivity to agonists. J Neurochem 67:58-63. CrossRef Medline
12. Fotuhi M, Sharp AH, Glatt CE, Hwang PM, von Krosigk M, Snyder SH, Dawson TM (1993) Differential localization of phosphoinositidelinked metabotropic glutamate receptor (m Glu R1) and the inositol 1,4,5-trisphosphate receptor in rat brain. J Neurosci 13:2001-2012. Medline
13. Francesconi A, Duvoisin RM (2002) Alternative splicing unmasks dendritic and axonal targeting signals in metabotropic glutamate receptor 1. J Neurosci 22:2196-2205. Medline
14. Fukaya M, Hayashi Y, Watanabe M (2005) NR2 to NR3B subunit switchover of NMDA receptors in early postnatal motoneurons. Eur J Neurosci 21:1432-1436. CrossRef Medline
15. Harris KM, Stevens JK (1988) Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 8:4455-4469. Medline
16. Hartmann J, Konnerth A (2009) Mechanisms of metabotropic glutamate receptor-mediated synaptic signalling in cerebellar Purkinje cells. Acta Physiol (Oxf) 195:79-90. CrossRef Medline
17. 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. CrossRef Medline
18. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796. CrossRef Medline
19. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63:106-118. CrossRef Medline
20. Hirata T, Kumada T, Kawasaki T, Furukawa T, Aiba A, Conquet F, Saga Y, Fukuda A (2012) Guidepost neurons for the lateral olfactory tract: expression of metabotropic glutamate receptor 1 and innervation by glutamatergic olfactory bulb axons. Dev Neurobiol 72:1559-1576. CrossRef Medline
21. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein: III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388. CrossRef Medline
22. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A (2000) m Glu R1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288:1832-1835. CrossRef Medline
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. Medline
24. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143-1195. Medline
25. Kakizawa S, Kishimoto Y, Hashimoto K, Miyazaki T, Furutani K, Shimizu H, Fukaya M, Nishi M, Sakagami H, Ikeda A, Kondo H, Kano M, Watanabe M, Iino M, Takeshima H (2007) Junctophilin-mediated channel crosstalk essential for cerebellar synaptic plasticity. EMBO J 26:1924-1933. CrossRef Medline
26. Kano M, Hashimoto K (2009) Synapse elimination in the central nervous system. Curr Opin Neurobiol 19:154-161. CrossRef Medline
27. 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 PKCγ mutant mice. Cell 83:1223-1231. CrossRef Medline
28. 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 m Glu R1. Neuron 18:71-79. CrossRef Medline
29. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Simon MI, Wu D (1998) Phospholipase Cβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci U S A 95:15724-15729. CrossRef Medline
30. 3 receptors and store-operated Htrp3 channels. Nature 396:478-482. CrossRef Medline
31. Kishimoto Y, Kano M (2006) Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning. J Neurosci 26:8829-8837. CrossRef Medline
32. Kishimoto Y, Fujimichi R, Araishi K, Kawahara S, Kano M, Aiba A, Kirino Y (2002) m Glu R1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur J Neurosci 16:2416-2424. CrossRef Medline
33. 2+ channel. J Biol Chem 278:25101-25108. CrossRef Medline
34. Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci U S A 87:2662-2665. CrossRef Medline
35. Kumpost J, Syrova Z, Kulihova L, Frankova D, Bologna JC, Hlavackova V, Prézeau L, Kralikova M, Hruskova B, Pin JP, Blahos J (2008) Surface expression of metabotropic glutamate receptor variants m Glu R1a and m Glu R1b in transfected HEK293 cells. Neuropharmacology 55:409-418. CrossRef Medline
36. Luján R, Roberts JD, Shigemoto R, Ohishi H, Somogyi P (1997) Differential plasma membrane distribution of metabotropic glutamate receptors m Glu R1α, m Glu R2 and m Glu R5, relative to neurotransmitter release sites. J Chem Neuroanat 13:219-241. CrossRef Medline
37. Mary S, Gomeza J, Prézeau L, Bockaert J, Pin JP (1998) A cluster of basic residues in the carboxyl-terminal tail of the short metabotropic glutamate receptor 1 variants impairs their coupling to phospholipase C. J Biol Chem 273:425-432. CrossRef Medline
38. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765. CrossRef Medline
39. 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. CrossRef Medline
40. Miyata M, Okada D, Hashimoto K, Kano M, Ito M (1999) Corticotropinreleasing factor plays a permissive role in cerebellar long-term depression. Neuron 22:763-775. CrossRef Medline
41. Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI, Inouye M, Takagishi Y, Augustine GJ, Kano M (2000) Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28:233-244. CrossRef Medline
42. 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 Cβ4 mutant mice. Eur J Neurosci 13:1945-1954. CrossRef Medline
43. Miyata M, Kishimoto Y, Tanaka M, Hashimoto K, Hirashima N, Murata Y, Kano M, Takagishi Y (2011) A role for myosin Va in cerebellar plasticity and motor learning: a possible mechanism underlying neurological disorder in myosin Va disease. J Neurosci 31:6067-6078. CrossRef Medline
44. Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, Watanabe M (2004) Signaling complex formation of phospholipase Cβ4 with metabotropic glutamate receptor type 1α and 1,4,5-trisphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci 20:2929-2944. CrossRef Medline
45. Oberdick J, Smeyne RJ, Mann JR, Zackson S, Morgan JI (1990) A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science 248:223-226. CrossRef Medline
46. 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 Gαq. Proc Natl Acad Sci U S A 94:14089-14094. CrossRef Medline
47. Pickering DS, Thomsen C, Suzdak PD, Fletcher EJ, Robitaille R, Salter MW, MacDonald JF, Huang XP, Hampson DR (1993) A comparison of two alternatively spliced forms of a metabotropic glutamate receptor coupled to phosphoinositide turnover. J Neurochem 61:85-92. CrossRef Medline
48. Prézeau L, Gomeza J, Ahern S, Mary S, Galvez T, Bockaert J, Pin JP (1996) Changes in the carboxyl-terminal domain of metabotropic glutamate receptor 1 by alternative splicing generate receptors with differing agonistindependent activity. Mol Pharmacol 49:422-429. Medline
49. Sallese M, Salvatore L, D'Urbano E, Sala G, Storto M, Launey T, Nicoletti F, Knöpfel T, De Blasi A (2000) The G-protein-coupled receptor kinase GRK4 mediates homologous desensitization of metabotropic glutamate receptor 1. FASEB J 14:2569-2580. CrossRef Medline
50. Sato M, Tabata T, Hashimoto K, Nakamura K, Nakao K, Katsuki M, Kitano J, Moriyoshi K, Kano M, Nakanishi S (2004) Altered agonist sensitivity and desensitization of neuronal m Glu R1 responses in knock-in mice by a single amino acid substitution at the PKC phosphorylation site. Eur J Neurosci 20:947-955. CrossRef Medline
51. Schonewille M, Gao Z, Boele HJ, Veloz MF, Amerika WE, Simek AA, De Jeu MT, Steinberg JP, Takamiya K, Hoebeek FE, Linden DJ, Huganir RL, De Zeeuw CI (2011) Reevaluating the role of LTD in cerebellar motor learning. Neuron 70:43-50. CrossRef Medline
52. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, Fujisaki T, Fujimoto K, Katoh A, Ikeda T, Chen C, Thompson RF, Itohara S (1996) Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16:587-599. CrossRef Medline
53. Tabata T, Sawada S, Araki K, Bono Y, Furuya S, Kano M (2000) A reliable method for culture of dissociated mouse cerebellar cells enriched for Purkinje neurons. J Neurosci Methods 104:45-53. CrossRef Medline
54. 2+ activity at GABAB receptors constitutively promotes metabotropic glutamate signaling in the absence of GABA. Proc Natl Acad Sci U S A 101:16952-16957. CrossRef Medline
55. Takagishi Y, Hashimoto K, Kayahara T, Watanabe M, Otsuka H, Mizoguchi A, Kano M, Murata Y (2007) Diminished climbing fiber innervation of Purkinje cells in the cerebellum of myosin Va mutant mice and rats. Dev Neurobiol 67:909-923. CrossRef Medline
56. Takechi H, Eilers J, Konnerth A (1998) Anew class of synaptic response involving calcium release in dendritic spines. Nature 396:757-760. CrossRef Medline
57. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S (1992) A family of metabotropic glutamate receptors. Neuron 8:169-179. CrossRef Medline
58. Tanaka J, Nakagawa S, Kushiya E, Yamasaki M, Fukaya M, Iwanaga T, Simon MI, Sakimura K, Kano M, Watanabe M (2000) Gq protein α subunits Gαq and Gα11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12:781-792. CrossRef Medline
59. Tempia F, Miniaci MC, Anchisi D, Strata P (1998) Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J Neurophysiol 80:520-528. Medline
60. 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. CrossRef Medline
61. Uemura T, Mori H, Mishina M (2004) Direct interaction of Glu Rδ2 with Shank scaffold proteins in cerebellar Purkinje cells. Mol Cell Neurosci 26:330-341. CrossRef Medline
62. Xiao B, Tu JC, Petralia RS, Yuan JP, Doan A, Breder CD, Ruggiero A, Lanahan AA, Wenthold RJ, Worley PF (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21:707-716. CrossRef Medline