Pinceau organization in the cerebellum requires distinct functions of neurofascin in purkinje and basket neurons during postnatal development

Journal of Neuroscience

Volumn 32, Issue 14, 2012, Pages 4724-4742

  Buttermore, Elizabeth D ^a   Piochon, Claire ^b   Wallace, Michael L ^a   Philpot, Benjamin D ^a   Hansel, Christian ^b   Bhat, Manzoor A ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN G; BREVICAN; CALBINDIN; NERVE CELL ADHESION MOLECULE; NEUROFASCIN; PARVALBUMIN; POSTSYNAPTIC DENSITY PROTEIN 95; POTASSIUM CHANNEL KV1.2; SODIUM CHANNEL; SODIUM CHANNEL NAV1.6; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATAXIA; BASKET NERVE CELL; BRAIN NERVE CELL; CELL MATURATION; CEREBELLUM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; LOCOMOTION; MALE; MOUSE; NERVE CELL DEGENERATION; NERVE ENDING; NEUROFILAMENT; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; ROTAROD TEST; SPIKE; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANIMALS, NEWBORN; AXONS; CELL ADHESION MOLECULES; CELL DEATH; CEREBELLUM; FEMALE; MALE; MICE; MICE, TRANSGENIC; NERVE GROWTH FACTORS; NEURONS; ORGAN CULTURE TECHNIQUES; PURKINJE CELLS;

EID: 84859361784     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5602-11.2012     Document Type: Article

References (76)

1. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, Huang ZJ (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119:257-272.
2. Barski JJ, Dethleffsen K, Meyer M (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28:93-98.
3. Bastianelli E (2003) Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2:242-262.
4. Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81:1353-1392.
5. Benton MD, Raman IM (2009) Stabilization of Ca current in Purkinje neurons during high-frequency firing by a balance of Ca-dependent facilitation and inactivation. Channels 3:393-401.
6. Berrebi AS, Oberdick J, Sangameswaran L, Christakos S, Morgan JI, Mugnaini E (1991) Cerebellar Purkinje cell markers are expressed in retinal bipolar neurons. J Comp Neurol 308:630-649.
7. Bobik M, Ellisman MH, Rudy B, Martone ME (2004) Potassium channel subunit Kv3.2 and the water channel aquaporin-4 are selectively localized to cerebellar pinceau. Brain Res 1026:168-178.
8. Boiko T, Vakulenko M, Ewers H, Yap CC, Norden C, Winckler B (2007) Ankyrin-dependent and-independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/ neuron-glia cell adhesion molecule. J Neurosci 27:590-603.
9. Browne DL, Gancher ST, Nutt JG, Brunt ER, Smith EA, Kramer P, Litt M (1994) Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet 8:136-140.
10. Brümmendorf T, Kenwrick S, Rathjen FG (1998) Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr Opin Neurobiol 8:87-97.
11. Buttermore ED, Dupree JL, Cheng J, An X, Tessarollo L, Bhat MA (2011) The cytoskeletal adaptor protein band 4.1B is required for the maintenance of paranodal axoglial septate junctions in myelinated axons. J Neurosci 31:8013-8024.
12. Catterall WA (1981) Localization of sodium channels in cultured neural cells. J Neurosci 1:777-783.
13. Davis TH, Chen C, Isom LL (2004) Sodium channel beta1 subunits promote neurite outgrowth in cerebellar granule neurons. J Biol Chem 279:51424-51432.
14. Doherty P, Williams G, Williams EJ (2000) CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci 16:283-295.
15. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
16. Garcia-Fresco GP, Sousa AD, Pillai AM, Moy SS, Crawley JN, Tessarollo L, Dupree JL, Bhat MA (2006) Disruption of axo-glial junctions causes cytoskeletal disorganization and degeneration of Purkinje neuron axons. Proc Natl Acad Sci U S A 103:5137-5142.
17. Gold DA, Baek SH, Schork NJ, Rose DW, Larsen DD, Sachs BD, Rosenfeld MG, Hamilton BA (2003) RORalpha coordinates reciprocal signaling in cerebellar development through sonic hedgehog and calcium-dependent pathways. Neuron 40:1119-1131.
18. Grubb MS, Burrone J (2010) Building and maintaining the axon initial segment. Curr Opin Neurobiol 20:481-488.
19. Hamilton BA, Frankel WN, Kerrebrock AW, Hawkins TL, FitzHugh W, Kusumi K, Russell LB, Mueller KL, van Berkel V, Birren BW, Kruglyak L, Lander ES (1996) Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379:736-739.
20. Hansen SM, Berezin V, Bock E (2008) Signaling mechanisms of neurite outgrowth induced by the cell adhesion molecules NCAM and N-cadherin. Cell Mol Life Sci 65:3809-3821.
21. Hedstrom KL, Xu X, Ogawa Y, Frischknecht R, Seidenbecher CI, Shrager P, Rasband MN (2007) Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol 178:875-886.
22. Hedstrom KL, Ogawa Y, Rasband MN (2008) AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 183:635-640.
23. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3:e159.
24. Huang ZJ (2006) Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules. Nat Neurosci 9:163-166.
25. Huang ZJ, Di Cristo G, Ango F (2007) Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci 8:673-686.
26. Isom LL (2002) The role of sodium channels in cell adhesion. Front Biosci 7:12-23.
27. John N, Krügel H, Frischknecht R, Smalla KH, Schultz C, Kreutz MR, Gundelfinger ED, Seidenbecher CI (2006) Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 31:774-784.
28. Khaliq ZM, Raman IM (2006) Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci 26:1935-1944.
29. Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-4912.
30. Kirschbaum K, Kriebel M, Kranz EU, Pötz O, Volkmer H (2009) Analysis of non-canonical fibroblast growth factor receptor 1 (FGFR1) interaction reveals regulatory and activating domains of neurofascin. J Biol Chem 284:28533-28542.
31. Kolodkin AL, Tessier-Lavigne M (2011) Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol 3. pii: a001727.
32. Koticha D, Babiarz J, Kane-Goldsmith N, Jacob J, Raju K, Grumet M (2005) Cell adhesion and neurite outgrowth are promoted by neurofascin NF155 and inhibited by NF186. Mol Cell Neurosci 30:137-148.
33. Koticha D, Maurel P, Zanazzi G, Kane-Goldsmith N, Basak S, Babiarz J, Salzer J, Grumet M (2006) Neurofascin interactions play a critical role in clustering sodium channels, ankyrin G and beta IV spectrin at peripheral nodes of Ranvier. Dev Biol 293:1-12.
34. Kriebel M, Metzger J, Trinks S, Chugh D, Harvey RJ, Harvey K, Volkmer H (2011) The Cell Adhesion Molecule Neurofascin Stabilizes Axo-axonic GABAergic Terminals at the Axon Initial Segment. J Biol Chem 286:24385-24393.
35. Levin SI, Khaliq ZM, Aman TK, Grieco TM, Kearney JA, Raman IM, Meisler MH (2006) Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar purkinje neurons and granule cells. J Neurophysiol 96:785-793.
36. Li XG, Somogyi P, Tepper JM, Buzsáki G (1992) Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Experimental brain research Experimentelle Hirnforschung Experimentation cerebrale 90:519-525.
37. Lu B, Wang KH, Nose A (2009) Molecular mechanisms underlying neural circuit formation. Curr Opin Neurobiol 19:162-167.
38. Manto M, Marmolino D (2009) Cerebellar ataxias. Curr Opin Neurol 22:419-429.
39. McEwen DP, Isom LL (2004) Heterophilic interactions of sodium channel beta1 subunits with axonal and glial cell adhesion molecules. J Biol Chem 279:52744-52752.
40. Nordquist DT, Kozak CA, Orr HT (1988) cDNA cloning and characterization of three genes uniquely expressed in cerebellum by Purkinje neurons. J Neurosci 8:4780-4789.
41. 2+ channel gene CACNL1A4. Cell 87:543-552.
42. Palay SL, Palay VC (1974) Cerebellar cortex. New York: Springer.
43. Perkins EM, Clarkson YL, Sabatier N, Longhurst DM, Millward CP, Jack J, Toraiwa J, Watanabe M, Rothstein JD, Lyndon AR, Wyllie DJ, Dutia MB, Jackson M (2010) Loss of beta-III spectrin leads to Purkinje cell dysfunction recapitulating the behavior and neuropathology of spinocerebellar ataxia type 5 in humans. J Neurosci 30:4857-4867.
44. Pillai AM, Thaxton C, Pribisko AL, Cheng JG, Dupree JL, Bhat MA (2009) Spatiotemporal ablation of myelinating glia-specific neurofascin (Nfasc NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains. J Neurosci Res 87:1773-1793.
45. Pruss T, Niere M, Kranz EU, Volkmer H (2004) Homophilic interactions of chick neurofascin in trans are important for neurite induction. Eur J Neurosci 20:3184-3188.
46. Pruss T, Kranz EU, Niere M, Volkmer H (2006) A regulated switch of chick neurofascin isoforms modulates ligand recognition and neurite extension. Mol Cell Neurosci 31:354-365.
47. Rader C, Stoeckli ET, Ziegler U, Osterwalder T, Kunz B, Sonderegger P (1993) Cell-cell adhesion by homophilic interaction of the neuronal recognition molecule axonin-1. Eur J Biochem 215:133-141.
48. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
49. Raman IM, Bean BP (1999) Properties of sodium currents and action potential firing in isolated cerebellar Purkinje neurons. Ann N Y Acad Sci 868:93-96.
50. Ramon y Cajal S (1911) Histologie du systéme nerveux de l'hommes et des verte ́bre ́s. Paris: Maloine.
51. Ramon y Cajal S (1995) Histology of the nervous system of man and vertebrates. New York: Oxford UP.
52. Rinaldo L, Hansel C (2010) Ataxias and cerebellar dysfunction: involvement of synaptic plasticity deficits? Funct Neurol 25:135-139.
53. Sacco T, De Luca A, Tempia F (2006) Properties and expression of Kv3 channels in cerebellar Purkinje cells. Mol Cell Neurosci 33:170-179.
54. 2+)-dependent steps controlling synaptic vesicle fusion and replenishment at the cerebellar basket cell terminal. Neuron 57:406-419.
55. Shiga T, Shirai T, Grumet M, Edelman GM, Oppenheim RW (1993) Differential expression of neuron-glia cell adhesion molecule (Ng-CAM) on developing axons and growth cones of interneurons in the chick embryo spinal cord: an immunoelectron microscopic study. J Comp Neurol 329:512-518.
56. Slemmer JE, De Zeeuw CI, Weber JT (2005) Don't get too excited: mechanisms of glutamate-mediated Purkinje cell death. Prog Brain Res 148:367-390.
57. Somogyi P, Hámori J (1976) A quantitative electron microscopic study of the Purkinje cell axon initial segment. Neuroscience 1:361-365.
58. Somogyi P, Nunzi MG, Gorio A, Smith AD (1983) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259:137-142.
59. Somogyi P, Tamás G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26:113-135.
60. Sotelo C (2008) Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamatergic and gamma-aminobutyric acidergic inputs in developing Purkinje cells. J Comp Neurol 506:240-262.
61. Sudarov A, Turnbull RK, Kim EJ, Lebel-Potter M, Guillemot F, Joyner AL (2011) Ascl1 genetics reveals insights into cerebellum local circuit assembly. J Neurosci 31:11055-11069.
62. Thaxton C, Pillai AM, Pribisko AL, Labasque M, Dupree JL, Faivre-Sarrailh C, Bhat MA (2010) In vivo deletion of immunoglobulin domains 5 and 6 in neurofascin (Nfasc) reveals domain-specific requirements in myelinated axons. J Neurosci 30:4868-4876.
63. Thaxton C, Pillai AM, Pribisko AL, Dupree JL, Bhat MA (2011) Nodes of Ranvier act as barriers to restrict invasion of flanking paranodal domains in myelinated axons. Neuron 69:244-257.
64. Ushkaryov YA, Petrenko AG, Geppert M, Südhof TC (1992) Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257:50-56.
65. Van Wart A, Matthews G (2006) Impaired firing and cell-specific compensation in neurons lacking nav1.6 sodium channels. J Neurosci 26:7172-7180.
66. Walsh FS, Doherty P (1997) Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu Rev Cell Dev Biol 13:425-456.
67. Wang VY, Zoghbi HY (2001) Genetic regulation of cerebellar development. Nat Rev Neurosci 2:484-491.
68. Waters MF, Minassian NA, Stevanin G, Figueroa KP, Bannister JP, Nolte D, Mock AF, Evidente VG, Fee DB, Müller U, Dürr A, Brice A, Papazian DM, Pulst SM (2006) Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat Genet 38:447-451.
69. Wiencken-Barger AE, Mavity-Hudson J, Bartsch U, Schachner M, Casagrande VA (2004) The role of L1 in axon pathfinding and fasciculation. Cereb Cortex 14:121-131.
70. Xie G, Harrison J, Clapcote SJ, Huang Y, Zhang JY, Wang LY, Roder JC (2010) A new Kv1.2 channelopathy underlying cerebellar ataxia. J Biol Chem 285:32160-32173.
71. Zagha E, Lang EJ, Rudy B (2008) Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform. J Neurosci 28:1291-1300.
72. Zhang L, Goldman JE (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16:47-54.
73. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143:1295-1304.
74. Zhuchenko O, Bailey J, Bonnen P, Ashizawa T, Stockton DW, Amos C, Dobyns WB, Subramony SH, Zoghbi HY, Lee CC (1997) Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat Genet 15:62-69.
75. Zoghbi HY (2000) Spinocerebellar ataxias. Neurobiol Dis 7:523-527.
76. Zonta B, Desmazieres A, Rinaldi A, Tait S, Sherman DL, Nolan MF, Brophy PJ (2011) A critical role for Neurofascin in regulating action potential initiation through maintenance of the axon initial segment. Neuron 69:945-956.