Dependence of axon initial segment formation on Na+ channel expression

Journal of Neuroscience Research

Volumn 79, Issue 4, 2005, Pages 428-441

  Xu, Xiaorong ^a   Shrager, Peter ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Ankyrin; Cluster; Initial segment; Na+ channel; ShRNA

Indexed keywords

ACTIN; ANKYRIN; ANKYRIN G; CYTOCHALASIN D; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NEUROFASCIN; PROTEIN NRCAM; RNA; SHORT HAIRPIN RNA; SODIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; MODEL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE FIBER MEMBRANE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; RAT; RNA INTERFERENCE; SODIUM CURRENT; SPINAL CORD MOTONEURON;

ANIMALS; ANKYRINS; AXONS; CELL ADHESION MOLECULES; CELL COUNT; CELLS, CULTURED; COMPUTER SIMULATION; CYTOCHALASIN D; EMBRYO; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MOTOR NEURONS; NERVE GROWTH FACTORS; NEURAL CELL ADHESION MOLECULES; NEUROFILAMENT PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; PATCH-CLAMP TECHNIQUES; RATS; RNA INTERFERENCE; RNA, CATALYTIC; SODIUM CHANNELS; SPINAL CORD; TIME FACTORS; TRANSFECTION;

EID: 14144251283     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20378     Document Type: Article

References (50)

1. Alessandri-Haber N, Paillart C, Arsac C, Gola M, Couraud F, Crest M. 1999. Specific distribution of sodium channels in axons of rat embryo spinal motoneurones. J Physiol 518:203-214.
2. Alessandri-Haber N, Alcaraz G, Deleuze C, Jullien F, Manrique C, Couraud F, Crest M, Giraud P. 2002. Molecular determinants of emerging excitability in rat embryonic motoneurons. J Physiol 541:25-39.
3. Bartsch U, Pesheva P, Raff M, Schachner M. 1993. Expression of janusin (J1-160/180) in the retina and optic nerve of the developing and adult mouse. Glia 9:57-69.
4. Berghs S, Aggujaro D, Dirkx R Jr, Maksimova E, Stabach P, Hermel JM, Zhang JP, Philbrick W, Slepnev V, Ort T, Solimena M. 2000. BetaIV spectrin, a new spectrin localized at axon initial segments and nodes of ranvier in the central and peripheral nervous system. J Cell Biol 151:985-1002.
5. Boiko T, Rasband MN, Levinson SR, Caldwell JH, Mandel G, Trimmer JS, Matthews G. 2001. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 30:91-104.
6. Bradke F, Dotti CG. 1999. The role of local actin instability in axon formation. Science 283:1931-1934.
7. Brummelkamp TR, Bernards R, Agami R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
8. Camu W, Henderson CE. 1992. Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor. J Neurosci Methods 44:59-70.
9. Charles P, Tait S, Faivre-Sarrailh C, Barbin G, Gunn-Moore F, Denisenko-Nehrbass N, Guennoc AM, Girault JA, Brophy PJ, Lubetzki C. 2002. Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol 12:217-220.
10. Ching W, Zanazzi G, Levinson SR, Salzer JL. 1999. Clustering of neuronal sodium channels requires contact with myelinating Schwann cells. J Neurocytol 28:295-301.
11. Crank J. 1975. The mathematics of diffusion. London: Oxford University Press. 414 p.
12. Custer AW, Kazarinova-Noyes K, Sakurai T, Xu X, Simon W, Grumet M, Shrager P. 2003. The role of the ankyrin-binding protein NrCAM in node of Ranvier formation. J Neurosci 23:10032-10039.
13. Davis JQ, Bennett V. 1994. Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J Biol Chem 269:27163-27166.
14. Dugandzija-Novakovic S, Koszowski AG, Levinson SR, Shrager P. 1995. Clustering of Na channels and node of Ranvier formation in remyelinating axons. J Neurosci 15:492-502.
15. Garrido JJ, Fernandes F, Giraud P, Mouret I, Pasqualini E, Fache MP, Jullien F, Dargent B. 2001. Identification of an axonal determinant in the C-terminus of the sodium channel Na(v)1.2. EMBO J 20:5950-5961.
16. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B. 2003. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300:2091-2094.
17. Garver TD, Ren Q, Tuvia S, Bennett V. 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.
18. Grumet M, Mauro V, Burgoon MP, Edelman GM, Cunningham BA. 1991. Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules. J Cell Biol 113:1399-1412.
19. Hanson MG Jr, Shen S, Wiemelt AP, McMorris FA, Barres BA. 1998. Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18:7361-7371.
20. Jenkins SM, Bennett V. 2001. 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 155:739-746.
21. Jenkins SM, Bennett V. 2002. Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc Natl Acad Sci U S A 99:2303-2308.
22. Jenkins SM, Kizhatil K, Kramarcy NR, Sen A, Sealock R, Bennett V. 2001. FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons. J Cell Sci 114:3823-3835.
23. Joe EH, Angelides KJ. 1993. Clustering and mobility of voltage-dependent sodium channels during myelination. J Neurosci 13:2993-3005.
24. Kaplan MR, Cho MH, Ullian EM, Isom LL, Levinson SR, Barres BA. 2001. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier. Neuron 30:105-119.
25. Kazarinova-Noyes K, Shrager P. 2002. Molecular constituents of the node of Ranvier. Mol Neurobiol 26:167-182.
26. Komada M, Soriano P. 2002. [Beta]IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 156:337-348.
27. 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.
28. Krzemien DM, Schaller KL, Levinson SR, Caldwell JH. 2000. Immunolocalization of sodium channel isoform NaCh6 in the nervous system. J Comp Neurol 420:70-83.
29. Lambert S, Davis JQ, Bennett V. 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.
30. Lemaillet G, Walker B, Lambert S. 2003. Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278:27333-27339.
31. Lustig M, Erskine L, Mason CA, Grumet M, Sakurai T. 2001. Nr-CAM expression in the developing mouse nervous system: ventral midline structures, specific fiber tracts, and neuropilar regions. J Comp Neurol 434:13-28.
32. Malhotra JD, Koopmann MC, Kazen-Gillespie KA, Fettman N, Hortsch M, Isom LL. 2002. Structural requirements for interaction of sodium channel beta 1 subunits with ankyrin. J Biol Chem 277:26681-26688.
33. Mooney RA, Anderson DL. 1989. Phosphorylation of the insulin receptor in permeabilized adipocytes is coupled to a rapid dephosphorylation reaction. J Biol Chem 264:6850-6857.
34. Mooney RA, Bordwell KL. 1992. Differential dephosphorylation of the insulin receptor and its 160-kDa substrate (pp160) in rat adipocytes. J Biol Chem 267:14054-14060.
35. Nakada C, Ritchie K, Oba Y, Nakamura M, Hotta Y, Iino R, Kasai RS, Yamaguchi K, Fujiwara T, Kusumi A. 2003. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat Cell Biol 5:626-632.
36. Pedraza L, Huang JK, Colman DR. 2001. Organizing principles of the axoglial apparatus. Neuron 30:335-344.
37. Peters LL, John KM, Lu FM, Eicher EM, Higgins A, Yialamas M, Turtzo LC, Otsuka AJ, Lux SE. 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. Poliak S, Peles E. 2003. The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968-980.
39. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P. 1999. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19:7516-7528.
40. Rasband MN, Kagawa T, Park EW, Ikenaka K, Trimmer JS. 2003. Dysregulation of axonal sodium channel isoforms after adult-onset chronic demyelination. J Neurosci Res 73:465-470.
41. Ratcliffe CF, Qu Y, McCormick KA, Tibbs VC, Dixon JE, Scheuer T, Catterall WA. 2000. A sodium channel signaling complex: modulation by associated receptor protein tyrosine phosphatase beta. Nat Neurosci 3:437-444.
42. Salzer JL. 2003. Polarized domains of myelinated axons. Neuron 40:297-318.
43. Schaller KL, Krzemien DM, Yarowsky PJ, Krueger BK, Caldwell JH. 1995. A novel, abundant sodium channel expressed in neurons and glia. J Neurosci 15:3231-3242.
44. Shrager P, Novakovic SD. 1995. Control of myelination, axonal growth, and synapse formation in spinal cord explants by ion channels and electrical activity. Brain Res Dev Brain Res 88:68-78.
45. Shrager P, Simon W, Kazarinova-Noyes K. 2004. Sodium channel reorganization in demyelinated axons. In: Waxman SG, editor. Multiple sclerosis as a neuronal disease. San Diego: Academic Press.
46. Simon W. 1986. Mathematical techniques for biology and medicine. New York: Dover Publications, Inc. 295 p.
47. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C, Pedraza L, Sherman DL, Colman DR, Brophy PJ. 2000. An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150:657-666.
48. Vabnick I, Novakovic SD, Levinson SR, Schachner M, Shrager P. 1996. The clustering of axonal sodium channels during development of the peripheral nervous system. J Neurosci 16:4914-4922.
49. Winckler B, Forscher P, Mellman I. 1999. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397:698-701.
50. G 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.