Ankyrin(G) is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing

Journal of Cell Biology

Volumn 143, Issue 5, 1998, Pages 1295-1304

  Zhou, Daixing ^a   Lambert, Stephen ^b   Malen, Peter L ^c   Carpenter, Scott ^a   Boland, Linda M ^c   Bennett, Vann ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Action potential; Ankyrin(G); Clustering; Neurofascin; Sodium channel

Indexed keywords

ANKYRIN; CALBINDIN; CELL ADHESION MOLECULE; NEUROFASCIN; SODIUM CHANNEL; UNCLASSIFIED DRUG; NERVE GROWTH FACTOR; NFASC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATAXIA; CEREBELLUM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GRANULE CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVE DEGENERATION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PURKINJE CELL; ACTION POTENTIAL; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; NERVE FIBER; NUCLEOTIDE SEQUENCE; OLIGONUCLEOTIDE PROBE; PATHOLOGY;

ANIMALIA; ATAXIA; EPICOCCUM; MAMMALIA;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; ANKYRINS; ATAXIA; AXONS; BASE SEQUENCE; CELL ADHESION MOLECULES; CEREBELLUM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NERVE DEGENERATION; NERVE GROWTH FACTORS; OLIGONUCLEOTIDE PROBES; PURKINJE CELLS; SODIUM CHANNELS;

EID: 0032582909     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.5.1295     Document Type: Article

References (51)

1. Armstrong, C.M., and B. Hille. 1998.Voltage-gated ion channels and electrical excitability. Neuron. 20:371-380.
2. Bennett, V., S. Lambert, J.Q. Davis, and X. Zhang. 1997. Molecular architecture of the specialized axonal membrane at the node of Ranvier. Soc. Gen. Physiol. Ser. 52:107-120.
3. Boakes, R.J., J.M. Candy, D.J. Dick, J.B. Harris, S. Pollard, and J. Thompson. 1984. Abnormal electrophysiological and anatomical characteristics of cerebellar Purkinje cells in the mutant mouse jolting. J. Physiol. (Lond.). 346:27P.
4. Burgess, D.L., D.C. Kohrman, J. Galt, N.W. Plummer, J.M. Jones, B. Spear, and M.H. Meisler. 1995. Mutation of a new sodium channel gene, Scn8a, in the mouse mutant "motor endplate disease." Nat. Genet. 10:461-465.
5. Catterall, W.A. 1981. Localization of sodium channels in cultured neural cells. J. Neurosci. 1:777-783.
6. B: structure of the major developmentally regulated domain and selective localization in unmyelinated axons. J. Cell Biol. 123:1463-1473.
7. Davis, J.Q., T. McLaughlin, and V. Bennett. 1993. Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J. Cell Biol. 121:121-133.
8. Davis, J.Q., S. Lambert, and V. Bennett. 1996. 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. 135:1355-1367.
9. De Miera, E.V.S., B. Rudy, M. Sugimori, and R. Llinas. 1997. Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA. 94:7059-7064.
10. Deerinck, T.J., S.R. Levinson, G.V. Bennett, and E.H. Ellisman. 1997. Clustering of voltage-sensitive sodium channels on axons is independent of direct Schwann cell contact in the dystrophic mouse. J. Neurosci. 17:5080-5088.
11. Devarajan, P., P.R. Stabach, M.A. De Matteis, and J.S. Morrow. 1997. Na,K-ATPase transport from endoplasmic reticulum to Golgi requires the Golgi spectrin-ankyrin G119 skeleton in Madin Darby canine kidney cells. Proc. Natl. Acad. Sci. USA. 94:10711-10716.
12. Dick, D.J., P.J. Boakes, J.M. Candy, J.B. Harris, and M.J. Cullen. 1986. Cerebellar structure and function in the murine mutant "jolting." J. Neurolog. Sci. 76:255-267.
13. Edwards, F.A. 1995. Patch clamp recording in brain slices. In Brain Slices in Basic and Clinical Research. A. Schurr and B.M. Rigor, editors. CRC Press, Boca Raton, FL. 99-116.
14. Ellisman, M.H., and S.R. Levinson. 1982. Immunocytochemical localization of sodium channel distributions in the excitable membranes of Electrophorus electricus. Proc. Natl. Acad. Sci. USA. 79:6707-6711.
15. + channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kD protein. Neuron. 3:163-175.
16. Garver, T., Q. Ren, S. Tuvia, and V. Bennett. 1997. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and Increases lateral mobility of neurofascin. J. Cell Biol. 137:703-714.
17. Gautam, M., P.G. Noakes, J. Mudd, M. Nichol, G.C. Chu, J.R. Sanes, and J.P. Merlie. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature. 377:232-236.
18. Gee, S.H., R. Madhavan, S.R. Levinson, J.H. Caldwell, R. Sealock, and S.C. Froehner. 1998. Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J. Neurosci. 18:128-137.
19. Gordon, D., D. Merrick, D.A. Wollner, and W.A. Catterall. 1988. Biochemical properties of sodium channels in a wide range of excitable tissues studied with site-directed antibodies. Biochemistry. 27:7032-7038.
20. Hortsch, M. 1996. The L1 family of neural cell adhesion molecules: old proteins performing new tricks. Neuron. 17:587-593.
21. Isom, L.L., D.S. Ragsdale, K.S. De Jongh, R.E. Westenbroek, B.F. Reber, T. Scheuer, and W.A. Catterall. 1995. Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell. 83:433-442.
22. Isom, L.L., and W.A. Catterall. 1996. Na+ channel subunits and Ig domains. Nature. 383:307-308.
23. Kaplan, M.R., A. Meyer-Franke, S. Lambert, V. Bennett, I.D. Duncan, S.R. Levinson, and B.A. Barres. 1997. Induction of sodium channel clustering by oligodendrocytes. Nature. 386:724-728.
24. Kohrman, D.C., M.R. Smith, A.L. Goldin, J. Harris, and M.H. Meisler. 1996. A missense mutation in the sodium channel Scn8a is responsible tor cerebellar ataxia in the mouse mutant jolting. J. Neurosci. 16:5993-5999.
25. Konnerth, A., I. Llano, and C.M. Armstrong. 1990. Synaptic currents in currents in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA. 87:2662-2665.
26. Kordeli, E., and V. Bennett. 1991. Distinct ankyrin isoforms at neuron cell bodies and nodes of Ranvier resolved using erythrocyte ankyrin-deficient mice J. Cell Biol. 114:1243-1259.
27. Kordeli, E., J. Davis, B. Trapp, and V. Bennett. 1990. An isoform of ankyrin is localized at nodes of Ranvier in myelinated axons of central and peripheral nerves. J. Cell Biol. 110:1341-1352.
28. G. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270:2352-2359.
29. Kordeli, E., M.A. Ludosky, C. Deprette, T. Frappier, and J. Cartaud. 1998. AnkyrinG is associated with the postsynaptic membrane and the sarcoplasmic reticulum in the skeletal muscle fiber. J. Cell Sci. 111:2197-2207.
30. Kunimoto, M., E. Otto, and V. Bennett. 1991. A new 440-kD isoform is the major ankyrin in neonatal rat brain. J. Cell Biol. 115:1319-1331.
31. Lambert, S., J.Q. Davis, and V. Bennett. 1997. Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J. Neurosci. 17:7025-7036.
32. 2+ exchanger binds to the cytoskclctal protein ankyrin. J. Biol. Chem. 268:11489-11491.
33. Michaely, P., and V. Bennett. 1993. The membrane-binding domain of ankyrin contains four independently folded subdomains, each comprised of six ankyrin repeats. J. Biol. Chem. 268:22703-22709.
34. Michaely, P., and V. Bennett. 1995a. The ANK repeats of erythrocyte ankyrin form two distinct but cooperative binding sites for the erythrocyte anion exchanger. J. Biol. Chem. 270:22050-22057.
35. 3- anion exchanger. J. Biol. Chem. 270:31298-31302.
36. +)ATPase and implications for the organization of membrane domains in polarized cells. Nature. 328:533-536.
37. Peters, L.L., K.M. John, F.M. Lu, E.M. Eicher, A. Higgins, M. Yialamas, L.C. Turtzo, A.J. Otsuka, and S.E. Lux. 1995. Ank3 (epithelial ankyrin), a widely distributed new member of the ankyrin gene family and the major ankyrin in kidney, is expressed in alternatively spliced forms, including forms that lack the repeat domain. J. Cell Biol. 130:313-330.
38. Raman, I.M., L.K., Sprunger, M.H. Meisler, and B.P. Bean. 1997. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron. 19:881-891.
39. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 7.40-7.42.
40. Schaller, K.L., D.M. Krzemien, P.J. Yarowsky, B. Krueger, and J.H. Caldwell. 1995. A novel, abundant sodium channel expressed in neurons and glia. J. Neurosci. 15:3231-3242.
41. Schultz, J., U. Hoffmuller, G. Krause, J. Ashurst, M.J. Macias, P. Schmieder, J. Schneider-Mergener, and H. Oschkinat. 1998. Specific interactions between the syntrophin PDZ domain and voltage-gated sodium channels. Nat. Struct. Biol. 5:19-24.
42. Srinivasan, Y., L. Elmer, J. Davis, V. Bennett, and K. Angelides. 1988. Ankyrin and spectrin associate with voltage-dependent sodium channels in brain. Nature. 333:177-180.
43. Srinivasan, Y., M. Lewallen, and K. Angelides. 1992. Mapping the binding site on ankyrin for the voltage-dependent sodium channel from brain. J. Biol. Chem. 267:7483-7489.
44. + channels in vivo. J. Neurosci. 17:152-159.
45. + channel subtypes in central neurons. Neuron. 3:695-704.
46. + channels in hypomyelinated axons of shiverer mouse brain. J. Neurosci. 12:2259-2267.
47. Wollner, D.A., and W.A. Catterall. 1986. Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells. Proc. Natl. Acad. Sci. USA. 83:8424-8428.
48. G at the adult rat neuromuscular junction. J. Cell Biol. 140:675-684.
49. G isoforms targeted to nodes of Ranvier. J. Biol. Chem. 271:31391-31398.
50. Zhang, X., and V. Bennett. 1998. Restriction of 480/270-kD ankyrin-G to axon proximal segments requires multiple ankyrin-G-specific domains. J. Cell Biol. 142:1571-1581.
51. Zito, K., R.D. Fetter, C.S. Goodman, and E.Y. Isacoff. 1997. Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron. 19:1007-1016.