Development of an anatomical technique for visualizing the mode of climbing fiber innervation in Purkinje cells and its application to mutant mice lacking GluRδ2 and Cav2.1

Anatomical Science International

Volumn 86, Issue 1, 2011, Pages 10-18

  Miyazaki, Taisuke ^a   Watanabe, Masahiko ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Anterograde tracer labeling; Cerebellum; Climbing fiber; Purkinje cell; Type 2 vesicular glutamate transporter

Indexed keywords

GLUTAMATE RECEPTOR 2; TRACER; VESICULAR GLUTAMATE TRANSPORTER 2; VOLTAGE GATED CALCIUM CHANNEL;

CLIMBING FIBER; DENDRITE; IMMUNOFLUORESCENCE; NERVE CELL PLASTICITY; NERVE FIBER; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; REVIEW; STAINING;

ANIMALS; CALCIUM CHANNELS, N-TYPE; CEREBELLUM; DENDRITES; ELECTROPHYSIOLOGICAL PHENOMENA; MICE; MICE, KNOCKOUT; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PURKINJE CELLS; RECEPTORS, GLUTAMATE;

EID: 79952764296     PISSN: 14476959     EISSN: 1447073X     Source Type: Journal    
DOI: 10.1007/s12565-010-0095-1     Document Type: Review

References (62)

1. Y Aihara H Mashima H Onda S Hisano H Kasuya T Hori S Yamada H Tomura Y Yamada I Inoue I Kojima J Takeda 2000 Molecular cloning of a novel brain-type Na(+)-dependent inorganic phosphate cotransporter J Neurochem 74 2622 2625 1:CAS:528:DC%2BD3cXjsVKrsbo%3D 10.1046/j.1471-4159.2000.0742622.x 10820226 (Pubitemid 30314241)
2. K Araki H Meguro E Kushiya C Takayama Y Inoue M Mishina 1993 Selective expression of the glutamate receptor channel delta 2 subunit in cerebellar Purkinje cells Biochem Biophys Res Commun 197 1267 1276 1:CAS:528: DyaK2cXhvVelsrs%3D 10.1006/bbrc.1993.2614 7506541 (Pubitemid 24042759)
3. M Bravin F Rossi P Strata 1995 Different climbing fibres innervate separate dendritic regions of the same Purkinje cell in hypogranular cerebellum J Comp Neurol 357 395 407 1:STN:280:DyaK2MvgtlOhtg%3D%3D 10.1002/cne.903570306 7673475
4. M Bravin L Morando A Vercelli F Rossi P Strata 1999 Control of spine formation by electrical activity in the adult rat cerebellum Proc Natl Acad Sci USA 96 1704 1709 1:CAS:528:DyaK1MXhsFSqsb0%3D 10.1073/pnas.96.4.1704 9990088 (Pubitemid 29098515)
5. R Cesa L Morando P Strata 2003 Glutamate receptor delta2 subunit in activity-dependent heterologous synaptic competition J Neurosci 23 2363 2370 1:CAS:528:DC%2BD3sXlsV2qtL4%3D 12657696 (Pubitemid 36368925)
6. R Cesa B Scelfo P Strata 2007 Activity-dependent presynaptic and postsynaptic structural plasticity in the mature cerebellum J Neurosci 27 4603 4611 1:CAS:528:DC%2BD2sXltF2jur0%3D 10.1523/JNEUROSCI.5617-06.2007 17460073 (Pubitemid 46663572)
7. Crepel F, Delhaye-Bouchaud N, Dupont JL (1981) Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Brain Res 227:59-71 (Pubitemid 11112070)
8. RT Fremeau Jr MD Troyer I Pahner GO Nygaard CH Tran RJ Reimer EE Bellocchio D Fortin J Storm-Mathisen RH Edwards 2001 The expression of vesicular glutamate transporters defines two classes of excitatory synapse Neuron 31 247 260 1:CAS:528:DC%2BD3MXlvFelt7s%3D 10.1016/S0896-6273(01)00344-0 11502256 (Pubitemid 32762978)
9. JM Guastavino C Sotelo I Damez-Kinselle 1990 Hot-foot murine mutation: behavioral effects and neuroanatomical alterations Brain Res 523 199 210 1:STN:280:DyaK3czotFGjtA%3D%3D 10.1016/0006-8993(90)91488-3 2400906 (Pubitemid 20230148)
10. K Hashimoto M Kano 2003 Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum Neuron 38 785 796 1:CAS:528:DC%2BD3sXkslOls7s%3D 10.1016/S0896-6273(03)00298-8 12797962 (Pubitemid 36694784)
11. K Hashimoto R Ichikawa H Takechi Y Inoue A Aiba K Sakimura M Mishina T Hashikawa A Konnerth M Watanabe M Kano 2001 Roles of glutamate receptor delta 2 subunit (GluRdelta 2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development J Neurosci 21 9701 9712 1:CAS:528:DC%2BD38XivFSn 11739579 (Pubitemid 34184056)
12. K Hashimoto R Ichikawa K Kitamura M Watanabe M Kano 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 1:CAS:528:DC%2BD1MXpsFOnsLw%3D 10.1016/j.neuron. 2009.06.008 19607796
13. E Herzog GC Bellenchi C Gras V Bernard P Ravassard C Bedet B Gasnier B Giros S El Mestikawy 2001 The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons J Neurosci 21 RC181 1:STN:280:DC%2BD3Mnks1WktA%3D%3D 11698619
14. H Hirai T Miyazaki W Kakegawa S Matsuda M Mishina M Watanabe M Yuzaki 2005 Rescue of abnormal phenotypes of the delta2 glutamate receptor-null mice by mutant delta2 transgenes EMBO Rep 6 90 95 1:CAS:528:DC%2BD2MXitVertg%3D%3D 10.1038/sj.embor.7400312 15592450 (Pubitemid 41710080)
15. H Hirai Z Pang D Bao T Miyazaki L Li E Miura J Parris Y Rong M Watanabe M Yuzaki JI Morgan 2005 Cbln1 is essential for synaptic integrity and plasticity in the cerebellum Nat Neurosci 8 1534 1541 1:CAS:528:DC%2BD2MXhtFCrurbO 10.1038/nn1576 16234806 (Pubitemid 41573668)
16. R Ichikawa T Miyazaki M Kano T Hashikawa H Tatsumi K Sakimura M Mishina Y Inoue M Watanabe 2002 Distal extension of climbing fiber territory and multiple innervation caused by aberrant wiring to adjacent spiny branchlets in cerebellar Purkinje cells lacking glutamate receptor delta 2 J Neurosci 22 8487 8503 1:CAS:528:DC%2BD38Xns1Cju7Y%3D 12351723 (Pubitemid 35387589)
17. A Ikeda T Miyazaki S Kakizawa Y Okuno S Tsuchiya A Myomoto SY Saito T Yamamoto T Yamazaki M Iino G Tsujimoto M Watanabe H Takeshima 2007 Abnormal features in mutant cerebellar Purkinje cells lacking junctophilins Biochem Biophys Res Commun 363 835 839 1:CAS:528:DC%2BD2sXhtFCjtrbM 10.1016/j.bbrc.2007. 09.062 17904530 (Pubitemid 47513705)
18. 2+ permeability of the channel pore is not essential for the delta2 glutamate receptor to regulate synaptic plasticity and motor coordination J Physiol 579 729 735 1:CAS:528:DC%2BD2sXktVOgtLk%3D 10.1113/jphysiol.2006. 127100 17255161 (Pubitemid 46404355)
19. Kakegawa W, Kohda K, Yuzaki M (2007b) The delta2 "ionotropic" glutamate receptor functions as a non-ionotropic receptor to control cerebellar synaptic plasticity. J Physiol 584:89-96 (Pubitemid 47500542)
20. S Kakizawa T Miyazaki D Yanagihara M Iino M Watanabe M Kano 2005 Maintenance of presynaptic function by AMPA receptor-mediated excitatory postsynaptic activity in adult brain Proc Natl Acad Sci USA 102 19180 19185 1:CAS:528:DC%2BD28XivV2ntg%3D%3D 10.1073/pnas.0504359103 16357208 (Pubitemid 43049586)
21. M Kano U Rexhausen J Dreessen A Konnerth 1992 Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells Nature 356 601 604 1:CAS:528:DyaK38Xit1yrtr4%3D 10.1038/356601a0 1313949
22. M Kano K Hashimoto C Chen A Abeliovich A Aiba H Kurihara M Watanabe Y Inoue S Tonegawa 1995 Impaired synapse elimination during cerebellar development in PKC gamma mutant mice Cell 83 1223 1231 1:CAS:528:DyaK28XhsVOmsg%3D%3D 10.1016/0092-8674(95)90147-7 8548808 (Pubitemid 26007812)
23. M Kano K Hashimoto H Kurihara M Watanabe Y Inoue A Aiba S Tonegawa 1997 Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1 Neuron 18 71 79 1:CAS:528:DyaK2sXpslykug%3D%3D 10.1016/S0896-6273(01)80047-7 9010206 (Pubitemid 27053831)
24. M Kano K Hashimoto M Watanabe H Kurihara S Offermanns H Jiang Y Wu K Jun HS Shin Y Inoue MI Simon D Wu 1998 Phospholipase cbeta4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum Proc Natl Acad Sci USA 95 15724 15729 1:CAS:528:DyaK1MXhvFehtQ%3D%3D 10.1073/pnas.95.26. 15724 9861037 (Pubitemid 29018767)
25. N Kashiwabuchi K Ikeda K Araki T Hirano K Shibuki C Takayama Y Inoue T Kutsuwada T Yagi Y Kang, et al. 1995 Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice Cell 81 245 252 1:CAS:528:DyaK2MXlt1Kisrg%3D 10.1016/0092-8674(95) 90334-8 7736576
26. A Konnerth J Dreessen GJ Augustine 1992 Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells Proc Natl Acad Sci USA 89 7051 7055 1:CAS:528:DyaK38XlsVyjtLY%3D 10.1073/pnas.89.15.7051 1323125
27. H Kurihara K Hashimoto M Kano C Takayama K Sakimura M Mishina Y Inoue M Watanabe 1997 Impaired parallel fiber → Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor delta2 subunit J Neurosci 17 9613 9623 1:CAS:528:DyaK2sXotVWgsbw%3D 9391016 (Pubitemid 28006405)
28. A Lalouette A Lohof C Sotelo J Guenet J Mariani 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 1:CAS:528:DC%2BD3MXlslert7w%3D 10.1016/S0306-4522(01)00193-2 11672610 (Pubitemid 32728127)
29. AS Landsend M Amiry-Moghaddam A Matsubara L Bergersen S Usami RJ Wenthold OP Ottersen 1997 Differential localization of delta glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses J Neurosci 17 834 842 1:CAS:528:DyaK2sXlt1Crsw%3D%3D 8987804 (Pubitemid 27024594)
30. H Lomeli R Sprengel DJ Laurie G Kohr A Herb PH Seeburg W Wisden 1993 The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family FEBS Lett 315 318 322 1:CAS:528:DyaK3sXktVWis7s%3D 10.1016/0014-5793(93) 81186-4 8422924 (Pubitemid 23025031)
31. G Mandolesi R Cesa E Autuori P Strata 2009 An orphan ionotropic glutamate receptor: the delta2 subunit Neuroscience 158 67 77 1:CAS:528: DC%2BD1MXns1ynuw%3D%3D 10.1016/j.neuroscience.2008.02.050 18424007
32. J Mariani 1982 Extent of multiple innervation of Purkinje cells by climbing fibers in the olivocerebellar system of weaver, reeler, and staggerer mutant mice J Neurobiol 13 119 126 1:STN:280:DyaL387ksVGjuw%3D%3D 10.1002/neu.480130204 7062017 (Pubitemid 12187034)
33. K Matsuda E Miura T Miyazaki W Kakegawa K Emi S Narumi Y Fukazawa A Ito-Ishida T Kondo R Shigemoto M Watanabe M Yuzaki 2010 Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer Science 328 363 368 1:CAS:528:DC%2BC3cXks1Sgu70%3D 10.1126/science.1185152 20395510
34. IM Mintz VJ Venema KM Swiderek TD Lee BP Bean ME Adams 1992 P-type calcium channels blocked by the spider toxin omega-Aga-IVA Nature 355 827 829 1:CAS:528:DyaK38XisFSitL8%3D 10.1038/355827a0 1311418
35. IM Mintz BL Sabatini WG Regehr 1995 Calcium control of transmitter release at a cerebellar synapse Neuron 15 675 688 1:CAS:528:DyaK2MXosVWlsrs%3D 10.1016/0896-6273(95)90155-8 7546746
36. T Miyazaki M Fukaya H Shimizu M Watanabe 2003 Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum Eur J Neurosci 17 2563 2572 10.1046/j.1460-9568. 2003.02698.x 12823463 (Pubitemid 36819281)
37. 2+ channel alpha1A regulates synaptic competition on developing cerebellar Purkinje cells J Neurosci 24 1734 1743 1:CAS:528:DC%2BD2cXhvVCnsrw%3D 10.1523/JNEUROSCI.4208-03.2004 14973254 (Pubitemid 38240971)
38. T Miyazaki K Hashimoto A Uda H Sakagami Y Nakamura SY Saito M Nishi H Kume A Tohgo I Kaneko H Kondo K Fukunaga M Kano M Watanabe H Takeshima 2006 Disturbance of cerebellar synaptic maturation in mutant mice lacking BSRPs, a novel brain-specific receptor-like protein family FEBS Lett 580 4057 4064 1:CAS:528:DC%2BD28XntV2rtrc%3D 10.1016/j.febslet.2006.06.043 16814779 (Pubitemid 44037568)
39. T Miyazaki M Yamasaki T Takeuchi K Sakimura M Mishina M Watanabe 2010 Ablation of glutamate receptor GluRδ2 in adult Purkinje cells causes multiple innervation of climbing fibers by inducing aberrant invasion to parallel fiber innervation territory J Neurosci 30 15196 15209 1:CAS:528:DC%2BC3cXhsV2nurbN 10.1523/JNEUROSCI.0934-10.2010 21068325
40. L Morando R Cesa R Rasetti R Harvey P Strata 2001 Role of glutamate delta-2 receptors in activity-dependent competition between heterologous afferent fibers Proc Natl Acad Sci USA 98 9954 9959 1:CAS:528: DC%2BD3MXmtlCmtro%3D 10.1073/pnas.171098398 11493687 (Pubitemid 32769409)
41. H Nishiyama M Fukaya M Watanabe DJ Linden 2007 Axonal motility and its modulation by activity are branch-type specific in the intact adult cerebellum Neuron 56 472 487 1:CAS:528:DC%2BD2sXhtlWitrvL 10.1016/j.neuron.2007.09.010 17988631 (Pubitemid 350026267)
42. S Offermanns K Hashimoto M Watanabe W Sun H Kurihara RF Thompson Y Inoue M Kano MI Simon 1997 Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Galphaq Proc Natl Acad Sci USA 94 14089 14094 1:CAS:528:DyaK2sXotVaks74%3D 10.1073/pnas.94.25.14089 9391157 (Pubitemid 28009714)
43. Palay S, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Springer, New York, pp 63-69 (see also pp 242-287)
44. WG Regehr IM Mintz 1994 Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses Neuron 12 605 613 1:CAS:528:DyaK2cXis1Kks7g%3D 10.1016/0896-6273(94)90216-X 8155322 (Pubitemid 24100891)
45. F Rossi JJ van der Want L Wiklund P Strata 1991 Reinnervation of cerebellar Purkinje cells by climbing fibres surviving a subtotal lesion of the inferior olive in the adult rat. II. Synaptic organization on reinnervated Purkinje cells J Comp Neurol 308 536 554 1:STN:280:DyaK3MzisVGltw%3D%3D 10.1002/cne.903080404 1865016
46. C Sotelo DE Hillman AJ Zamora R Llinas 1975 Climbing fiber deafferentation: its action on Purkinje cell dendritic spines Brain Res 98 574 581 1:STN:280:DyaE28%2FktFWjtA%3D%3D 10.1016/0006-8993(75)90374-1 1182538
47. A Stea WJ Tomlinson TW Soong E Bourinet SJ Dubel SR Vincent TP Snutch 1994 Localization and functional properties of a rat brain alpha 1A calcium channel reflect similarities to neuronal Q- and P-type channels Proc Natl Acad Sci USA 91 10576 10580 1:CAS:528:DyaK2cXmslOhtLY%3D 10.1073/pnas.91.22.10576 7524096 (Pubitemid 24329041)
48. I Sugihara H Wu Y Shinoda 1999 Morphology of single olivocerebellar axons labeled with biotinylated dextran amine in the rat J Comp Neurol 414 131 148 1:STN:280:DyaK1MvkslOmtA%3D%3D 10.1002/(SICI)1096-9861(19991115)414:2<131:: AID-CNE1>3.0.CO;2-F 10516588 (Pubitemid 29489899)
49. I Sugihara Y Bailly J Mariani 2000 Olivocerebellar climbing fibers in the granuloprival cerebellum: morphological study of individual axonal projections in the X-irradiated rat J Neurosci 20 3745 3760 1:CAS:528:DC%2BD3cXjtlKqsLY%3D 10804216 (Pubitemid 30266237)
50. Sugihara I, Wu HS, Shinoda Y (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci 21:7715-7723 (Pubitemid 32904970)
51. C Takayama S Nakagawa M Watanabe M Mishina Y Inoue 1995 Light- and electron-microscopic localization of the glutamate receptor channel delta 2 subunit in the mouse Purkinje cell Neurosci Lett 188 89 92 1:CAS:528: DyaK2MXkvValu7k%3D 10.1016/0304-3940(95)11403-J 7792064
52. T Takeuchi T Miyazaki M Watanabe H Mori K Sakimura M Mishina 2005 Control of synaptic connection by glutamate receptor delta2 in the adult cerebellum J Neurosci 25 2146 2156 1:CAS:528:DC%2BD2MXitVSms7c%3D 10.1523/JNEUROSCI.4740-04. 2005 15728855 (Pubitemid 40289420)
53. A Tohgo M Eiraku T Miyazaki E Miura SY Kawaguchi M Nishi M Watanabe T Hirano M Kengaku H Takeshima 2006 Impaired cerebellar functions in mutant mice lacking DNER Mol Cell Neurosci 31 326 333 1:CAS:528:DC%2BD28Xhtlaksrs%3D 10.1016/j.mcn.2005.10.003 16298139 (Pubitemid 43214542)
54. Y Tomioka T Miyazaki S Taharaguchi S Yoshino M Morimatsu T Uede E Ono M Watanabe 2008 Cerebellar pathology in transgenic mice expressing the pseudorabies virus immediate-early protein IE180 Eur J Neurosci 27 2115 2132 10.1111/j.1460-9568.2008.06174.x 18412631 (Pubitemid 351521492)
55. T Uemura S Kakizawa M Yamasaki K Sakimura M Watanabe M Iino M Mishina 2007 Regulation of long-term depression and climbing fiber territory by glutamate receptor delta2 at parallel fiber synapses through its C-terminal domain in cerebellar Purkinje cells J Neurosci 27 12096 12108 1:CAS:528:DC%2BD2sXhtlSktrvF 10.1523/JNEUROSCI.2680-07.2007 17978051 (Pubitemid 350072108)
56. T Uemura SJ Lee M Yasumura T Takeuchi T Yoshida M Ra R Taguchi K Sakimura M Mishina 2010 Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum Cell 141 1068 1079 1:CAS:528:DC%2BC3cXnvValtLg%3D 10.1016/j.cell.2010.04.035 20537373
57. M Watanabe 2008 Molecular mechanisms governing competitive synaptic wiring in cerebellar Purkinje cells Tohoku J Exp Med 214 175 190 1:CAS:528:DC%2BD1cXkt1Wgs7g%3D 10.1620/tjem.214.175 18323688 (Pubitemid 351513530)
58. M Watanabe M Mishina Y Inoue 1994 Distinct spatiotemporal expressions of five NMDA receptor channel subunit mRNAs in the cerebellum J Comp Neurol 343 513 519 1:CAS:528:DyaK2cXkt1OlsLg%3D 10.1002/cne.903430402 7518474 (Pubitemid 24138945)
59. F Watanabe T Miyazaki T Takeuchi M Fukaya T Nomura S Noguchi H Mori K Sakimura M Watanabe M Mishina 2008 Effects of FAK ablation on cerebellar foliation, Bergmann glia positioning and climbing fiber territory on Purkinje cells Eur J Neurosci 27 836 854 10.1111/j.1460-9568.2008.06069.x 18279360 (Pubitemid 351365180)
60. DJ Woodward BJ Hoffer J Altman 1974 Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal x-irradiation J Neurobiol 5 283 304 1:STN:280:DyaE2M%2Fps1Ogtw%3D%3D 10.1002/neu.480050402 4155719
61. K Yamada M Fukaya H Shimizu K Sakimura M Watanabe 2001 NMDA receptor subunits GluRepsilon1, GluRepsilon3 and GluRzeta1 are enriched at the mossy fibre-granule cell synapse in the adult mouse cerebellum Eur J Neurosci 13 2025 2036 1:STN:280:DC%2BD3Mzmt1Wrsw%3D%3D 10.1046/j.0953-816x.2001.01580.x 11422443 (Pubitemid 32578788)
62. M Yuzaki 2009 New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the delta2 glutamate receptor Neuroscience 162 633 643 1:CAS:528:DC%2BD1MXptVantbY%3D 10.1016/j.neuroscience.2008.12.002 19124061