Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment

Cell

Volumn 119, Issue 2, 2004, Pages 257-272

  Ango, Fabrice ^a   Di Cristo, Graziella ^a   Higashiyama, Hiroyuki ^a   Bennett, Vann ^b   Wu, Priscilla ^a   Huang, Z Josh ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; IMMUNOGLOBULIN; INTERCELLULAR ADHESION MOLECULE 1; NEUROFASCIN; PROTEIN; UNCLASSIFIED DRUG;

ACCURACY; ANIMAL CELL; ARTICLE; CELL DISRUPTION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; DENSITY GRADIENT; GABAERGIC SYSTEM; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOUSE; NERVE FIBER; NERVE GROWTH; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN TARGETING; PURKINJE CELL; SYNAPSE;

ANIMALIA;

EID: 5444260773     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2004.10.004     Document Type: Article

References (50)

1. Bayer S.A., Altman J. Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog. Neurobiol. 29:1987;57-106
2. Bennett V., Baines A.J. Spectrin and ankyrin-based pathways. metazoan inventions for integrating cells into tissues Physiol. Rev. 81:2001;1353-1392
3. Brummendorf T., Kenwrick S., Rathjen F.G. Neural cell recognition molecule L1. from cell biology to human hereditary brain malformations Curr. Opin. Neurobiol. 8:1998;87-97
4. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. 378:1995;75-78
5. Cohen N.R., Taylor J.S., Scott L.B., Guillery R.W., Soriano P., Furley A.J. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8:1998;26-33
6. Dahme M., Bartsch U., Martini R., Anliker B., Schachner M., Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17:1997;346-349
7. Davis J.Q., Bennett V. Brain ankyrin. Purification of a 72,000 Mr spectrin-binding domain. J. Biol. Chem. 259:1984;1874-1881
8. Davis J.Q., Lambert S., Bennett V. Molecular composition of the node of Ranvier. identification of ankyrin-binding cell adhesion molecules neurofascin (mucin+/third FNIII domain-) and NrCAM at nodal axon segments J. Cell Biol. 135:1996;1355-1367
9. Di Cristo G., Wu C., Chattopadhyaya B., Ango F., Knott G., Welker E., Svoboda K., Huang Z.J. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat. Neurosci. in press:2004
10. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14:1994;1834-1855
11. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470
12. Greif K.F., Erlander M.G., Tillakaratne N.J., Tobin A.J. Postnatal expression of glutamate decarboxylases in developing rat cerebellum. Neurochem. Res. 16:1991;235-242
13. Heintz N., De Felipe J., Marco P., Fairen A., Jones E.G. BAC to the future. the use of bac transgenic mice for neuroscience research Nat. Rev. Neurosci. 2:2001;861-870
14. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 98:1999;739-755
15. Hummel T., Vasconcelos M.L., Clemens J.C., Fishilevich Y., Vosshall L.B., Zipursky S.L. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron. 37:2003;221-231
16. Jenkins S.M., Bennett V. Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155:2001;739-746
17. Kapfer C., Seidl A.H., Schweizer H., Grothe B. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat. Neurosci. 5:2002;247-253
18. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science. 274:1996;1133-1138
19. Klausberger T., Magill P.J., Marton L.F., Roberts J.D., Cobden P.M., Buzsaki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature. 421:2003;844-848
20. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 34:2002;265-273
21. Komada M., Soriano P. IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J. Cell Biol. 156:2002;337-348. [Beta]
22. Michaely P., Bennett V. Mechanism for binding site diversity on ankyrin. Comparison of binding sites on ankyrin for neurofascin and the Cl-/HCO3- anion exchanger. J. Biol. Chem. 270:1995;31298-31302
23. Miles R., Toth K., Gulyas A.I., Hajos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron. 16:1996;815-823
24. Montag-Sallaz M., Schachner M., Montag D. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol. Cell. Biol. 22:2002;7967-7981
25. Palay S.L., Palay V.C. Cerebellar Cortex. 1974;Springer-Verlag, New York
26. Porter J.T., Johnson C.K., Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci. 21:2001;2699-2710
27. Pouille F., Scanziani M. Routing of spike series by dynamic circuits in the hippocampus. Nature. 429:2004;717-723
28. Ramon y Cajal, S. (1911). Histologie du Systeme Nerveux de l'Homme et des Vertebres, par S. Ramon Cajal. Ed francaise revue & mise a jour par l'auteur Traduite de l'espagnol par L'Azoulay Paris, A Maloine, 1909-1911.
29. Rathjen F.G., Wolff J.M., Chang S., Bonhoeffer F., Raper J.A. Neurofascin. a novel chick cell-surface glycoprotein involved in neurite-neurite interactions Cell. 51:1987;841-849
30. Rosina A., Morara S., Provini L. GAT-1 developmental expression in the rat cerebellar cortex. basket and pinceau formation Neuroreport. 10:1999;1613-1618
31. Rougon G., Hobert O. New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu. Rev. Neurosci. 26:2003;207-238. Published online February 13, 2003.
32. Sakurai T., Lustig M., Babiarz J., Furley A.J., Tait S., Brophy P.J., Brown S.A., Brown L.Y., Mason C.A., Grumet M. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. J. Cell Biol. 154:2001;1259-1273
33. Schmucker D., Clemens J.C., Shu H., Worby C.A., Xiao J., Muda M., Dixon J.E., Zipursky S.L. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell. 101:2000;671-684
34. Shen K., Fetter R.D., Bargmann C.I. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell. 116:2004;869-881
35. Somogyi P., Tamas G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26:1998;113-135
36. Stein P.L., Lee H.M., Rich S., Soriano P. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell. 70:1992;741-750
37. Swadlow H.A. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb. Cortex. 13:2003;25-32
38. Tamas G., Buhl E.H., Lorincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3:2000;366-371
39. Tamas G., Lorincz A., Simon A., Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science. 299:2003;1902-1905
40. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133
41. Tuvia S., Garver T.D., Bennett V. The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation. Proc. Natl. Acad. Sci. USA. 94:1997;12957-12962
42. Tyler J.M., Hargreaves W.R., Branton D. Purification of two spectrin-binding proteins. biochemical and electron microscopic evidence for site-specific reassociation between spectrin and bands 2.1 and 4.1 Proc. Natl. Acad. Sci. USA. 76:1979;5192-5196
43. Volkmer H., Leuschner R., Zacharias U., Rathjen F.G. Neurofascin induces neurites by heterophilic interactions with axonal NrCAM while NrCAM requires F11 on the axonal surface to extend neurites. J. Cell Biol. 135:1996;1059-1069
44. Volkmer H., Zacharias U., Norenberg U., Rathjen F.G. Dissection of complex molecular interactions of neurofascin with axonin-1, F11, and tenascin-R, which promote attachment and neurite formation of tectal cells. J. Cell Biol. 142:1998;1083-1093
45. Yamagata M., Weiner J.A., Sanes J.R. Sidekicks. synaptic adhesion molecules that promote lamina-specific connectivity in the retina Cell. 110:2002;649-660
46. Yang X.W., Model P., Heintz N. Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotechnol. 15:1997;859-865
47. Yi S.J., Liu S.C., Derick L.H., Murray J., Barker J.E., Cho M.R., Palek J., Golan D.E. Red cell membranes of ankyrin-deficient nb/nb mice lack band 3 tetramers but contain normal membrane skeletons. Biochemistry. 36:1997;9596-9604
48. Zhang L., Goldman J.E. Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron. 16:1996;47-54
49. Zhang X., Davis J.Q., Carpenter S., Bennett V. Structural requirements for association of neurofascin with ankyrin. J. Biol. Chem. 273:1998;30785-30794
50. Zhou D., Lambert S., Malen P.L., Carpenter S., Boland L.M., Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol. 143:1998;1295-1304