Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination

Brain

Volumn 126, Issue 7, 2003, Pages 1552-1561

  Craner, Matthew J ^b   Lo, Albert C ^b   Black, Joel A ^b   Waxman, Stephen G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

Demyelination; Multiple sclerosis; Nodes of Ranvier; Sodium channels; Visual pathways

Indexed keywords

SODIUM CHANNEL;

ACTION POTENTIAL; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMYELINATION; IMMUNOCYTOCHEMISTRY; MOUSE; MULTIPLE SCLEROSIS; MYELINATED NERVE; NERVE FIBER MEMBRANE; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RANVIER NODE; RETINA GANGLION CELL;

EID: 0037819578     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awg153     Document Type: Article

References (48)

1. Arroyo EJ, Scherer SS. On the molecular architecture of myelinated fibers. Histochem Cell Biol 2000; 113: 1-18.
2. Arroyo EJ, Xu T, Grinspan J, et al. Genetic dysmyelination alters the molecular architecture of the nodal region. J Neurosci 2002; 22: 1726-37.
3. Bhat MA, Rios JC, Lu Y, et al. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 2001; 30: 369-83.
4. Black JA, Waxman SG, Hildebrand C. Axo-glial relations in the retina-optic nerve junction of the adult rat: freeze-fracture observations on axon membrane structure. J Neurocytol 1985; 14: 887-907.
5. Black JA, Dib-Hajj SD, McNabola K, et al. Spinal sensory neurons express multiple sodium channel α-subunit mRNAs. Brain Res Mol Brain Res 1996; 43: 117-31.
6. v1.6 is expressed along nonmyelinated axons and it contributes to conduction. Brain Res Mol Brain Res 2002; 105: 19-28.
7. Boiko T, Rasband MN, Levinson SR, et al. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 2001; 30: 91-104.
8. Bostock H, Sears TA. Continuous conduction in demyelinated mammalian nerve fibers. Nature 1976; 263: 786-7.
9. Bostock H, Sears TA. The internodal axon membrane: electrical excitability and continuous conduction in segmental demyelination. J Physiol 1978; 280: 273-301.
10. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR. Sodium channel Na(v)1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 2000; 97: 5616-20.
11. Craner MJ, Klein JP, Renganathan M, Black JA, Waxman SG. Changes of sodium channel expression in experimental painful diabetic neuropathy. Ann Neurol 2002; 52: 786-92.
12. Deerinck TJ, Levinson SR, Bennett GV, Ellisman MH. Clustering of voltage-sensitive sodium channels on axons is independent of direct Schwann cell contact in the dystrophic mouse. J Neurosci 1997; 17: 5080-8.
13. + channels and node of Ranvier formation in remyelinating axons. J Neurosci 1995; 15: 492-503.
14. Dupree JL, Girault JA, Popko B. Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 1999; 147: 1145-52.
15. Einheber S, Zanazzi G, Ching W, et al. The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J Cell Biol 1997; 139: 1495-506.
16. England JD, Gamboni F, Levinson SR, Finger TE. Changed distribution of sodium channels along demyelinated axons. Proc Natl Acad Sci USA 1990; 87: 6777-80.
17. Fjell J, Dib-Hajj S, Fried K, Black JA, Waxman SG. Differential expression of sodium channel genes in retinal ganglion cells. Brain Res Mol Brain Res 1997; 50: 197-204
18. Forrester J, Peters A. Nerve fibres in optic nerve of rat. Nature 1967; 214: 245-7.
19. Foster RE, Connors BW, Waxman SG. Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development. Brain Res 1982; 255: 371-86.
20. + channel alpha-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J Comp Neurol 1999; 412: 342-52.
21. Hains BC, Black JA, Waxman SG. Primary motor neurons fail to up-regulate voltage-gated sodium channel Na(v)1.3/brain type III following axotomy resulting from spinal cord injury. J Neurosci Res 2002; 70: 546-52.
22. Ishibashi T, Dupree JL, Ikenaka K, et al. A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J Neurosci 2002; 22: 6507-14.
23. Kaplan MR, Cho MH, Ullian EM, Isom LL, Levinson SR, Barres BA. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier. Neuron 2001; 30: 105-19.
24. Menegoz M, Gaspar P, Le Bert M, et al. Paranodin, a glycoprotein of neuronal paranodal membranes. Neuron 1997; 19: 319-31.
25. Novakovic SD, Deerinck TJ, Levinson SR, Shrager P, Ellisman MH. Clusters of axonal Na+ channels adjacent to remyelinating Schwann cells. J Neurocytol 1996; 25: 403-12.
26. Novakovic SD, Levinson SR, Schachner M, Shrager P. Disruption and reorganization of sodium channels in experimental allergic neuritis. Muscle Nerve 1998; 21: 1019-32.
27. Peles E, Salzer JL. Molecular domains of myelinated axons. Curr Opin Neurobiol 2000; 10: 558-65.
28. Pender MP. Recovery from acute experimental allergic encephalomyelitis in the Lewis rat. Early restoration of nerve conduction and repair by Schwann cells and oligodendrocytes. Brain 1989; 112: 393-416.
29. Prineas J, Raine CS, Wisniewski H. An ultrastructural study of experimental demyelination and remyelination. 3. Chronic experimental allergic encephalomyelitis in the central nervous system. Lab Invest 1969; 21: 472-83.
30. Raman IM, Sprunger LK, Meisler MH, Bean BP. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 1997; 19: 881-91.
31. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P. Dependence of nodal sodium channel clustering on paranodal axo-glial contact in the developing CNS. J Neurosci 1999; 19: 7516-28.
32. Rios JC, Melendez-Vasquez CV, Einheber S, et al. Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 2000; 20: 8354-64.
33. Ritchie JM, Rogart RB. Density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath. Proc Natl Acad Sci USA 1977; 74: 211-5.
34. Rosenbluth J. Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain. J Neurocytol 1976; 5: 731-45.
35. Rothe T, Juttner R, Bahring R, Grantyn R. Ion conductances related to development of repetitive firing in mouse retinal ganglion neurons in situ. J Neurobiol 1999; 38: 191-206.
36. Schmid S, Guenther E. Alterations in channel density and kinetic properties of the sodium current in retinal ganglion cells of the rat during in vivo differentiation. Neuroscience 1998; 85: 249-58
37. Skaliora I, Scobey RP, Chalupa LM. Prenatal development of excitability in cat retinal ganglion cells: action potentials and sodium currents. J Neurosci 1993; 13: 313-23.
38. Smith KJ, Bostock H, Hall SM. Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline. J Neurol Sci 1982; 54: 13-31.
39. Smith MR, Smith RD, Plummer NW, Meisler MH, Goldin AL. Functional analysis of the mouse Scn8a sodium channel. J Neurosci 1998; 18: 6093-102.
40. + channel aggregation in remyelinating mouse sciatic axons following transection. Glia 1995; 15: 188-94.
41. Vabnick I, Shrager P. Ion channel redistribution and function during development of the myelinated axon. J Neurobiol 1998; 37: 80-96.
42. Vabnick I, Messing A, Chiu SY, et al. Sodium channel distribution in axons of hypomyelinated and MAG null mutant mice. J Neurosci Res 1997; 50: 321-36.
43. Wang GY, Ratto G, Bisti S, Chalupa LM. Functional development of intrinsic properties in ganglion cells of the mammalian retina. J Neurophysiol 1997; 78: 2895-903.
44. Waxman SG. Conduction in myelinated, unmyelinated and demyelinated fibers. Arch Neurol 1977; 34: 585-590
45. Waxman SG, Foster RE. Development of the axon membrane during differentiation of myelinated fibres in spinal nerve roots. Proc R Soc Lond B Biol Sci 1980; 209: 441-6.
46. Westenbroek RE, Merrick DK, Catterall WA. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron 1989; 3: 695-704.
47. Whitaker WR, Clare JJ, Powell AJ, Chen YH, Faull RL, Emson PC. Distribution of voltage-gated sodium channel alpha-subunit and beta-subunit mRNAs in human hippocampal formation, cortex, and cerebellum. J Comp Neurol 2000; 422: 123-39.
48. v1.2 sodium channels [abstract]. Soc Neurosci Abstr 2002; 32: Prog. No. 834.4