Ion channel redistribution and function during development of the myelinated axon

Journal of Neurobiology

Volumn 37, Issue 1, 1998, Pages 80-96

  Vabnick, Lan ^a   Shrager, Peter ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Axon; Clustering; Ion channel; Myelin; Node of Ranvier

Indexed keywords

ION CHANNEL; POTASSIUM CHANNEL; SODIUM CHANNEL;

CELL COMMUNICATION; GLIA; HUMAN; MYELINATED NERVE; MYELINATION; NERVE CELL; NERVE CONDUCTION; NERVE FIBER MEMBRANE; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; RANVIER NODE; REVIEW;

ANIMALS; AXONS; ION CHANNELS; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NERVE REGENERATION; NERVOUS SYSTEM; NEUROGLIA; POTASSIUM CHANNELS; RANVIER'S NODES; SODIUM CHANNELS;

EID: 7344229312     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199810)37:1<80::AID-NEU7>3.0.CO;2-4     Document Type: Review

References (90)

1. ALLT, G. (1969). Ultrastructural features of the immature peripheral nerve. J. Anat. 105:283-293.
2. BAKER, M., BOSTOCK, H., GRAFE, P., and MARTIUS, P. (1987). Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J. Physiol. 383:45-67.
3. BARRETT, E. F. and BARRETT, J. N. (1982). Intracellular recording from vertebrate myelinated axons: mechanism of the depolarizing afterpotential. J. Phvsiol. 323:117-144.
4. BIGBEE, J. W. and FOSTER, R. E. (1989). Freeze fracture analysis of the axolemma of cultured dorsal root ganglion neurons in the absence of Schwann cells. Brain Res. 494:182-186.
5. BLACK, J. A., DIB-HAJI, S., MCNABOLA, K., JESTE, S., RIZZO, M. A., KOCSIS, J. D., and WAXMAN, S. G. (1996). Spinal sensory neurons express multiple sodium channel alpha-subunit mRNAs. Mol. Brain Res. 43:117-131.
6. BLACK, J. A., FOSTER, R. E., and WAXMAN, S. G. (1982). Rat optic nerve: freeze-fracture studies during development of myelinated axons. Brain Res. 250:1-20.
7. BLIGHT, A. R. (1985). Computer simulation of action potentials and afterpotentials in mammalian myelinated axons: the case for a lower resistance myelin sheath. Neuroscience 15:13-31.
8. BOWE, C. M., JOHANSSON, C. S., HILDEBRAND, C., and EVANS, N. H. (1994). Functional properties and nodal spacing of myelinated fibers in developing rat mental and sural nerves. Dev. Brain Res. 79:186-194.
9. BOWE, C. M., KOCSIS, J. D., and WAXMAN, S. G. (1985). Differences between mammalian ventral and dorsal spinal roots in response to blockade of potassium channels during maturation. Proc. R. Soc. Lond. B 224:355-366.
10. CARENINI, S., MONTAG, D., CREMER, H., SCHACHNER, M., and MARTINI, R. (1997). Absence of the myelin-associated glycoprotein (MAG) and the neural cell adhesion molecule (N-CAM) interferes with the maintenance, but not with the formation of peripheral myelin. Cell Tissue Res. 287:3-9.
11. CHANG, M. P., BRAMHALL, J., GRAVES, S., BONAVIDA, B., and WISNIESKI, B. J. (1989). Internucleosomal DNA cleavage precedes diphtheria toxin-induced cytolysis. Evidence that cell lysis is not a simple consequence of translation inhibition. J. Biol. Chem. 264:15261-15267.
12. CHIU, S. Y. and RITCHIE, J. M. (1981). Evidence for the presence of potassium channels in the paranodal region of acutely demyelinated mammalian single nerve fibers. J. Physiol. 313:415-437.
13. CHIU, S. Y. and RITCHIE, J. M. (1984). On the physiological role of internodal potassium channels and the security of conduction in myelinated nerve fibers. Proc. R. Soc. Lond. 5220:415-422.
14. CHIU, S. Y., RITCHIE, J. M., ROGART, R. B., and STAGG, D. (1979). A quantitative description of membrane currents in rabbit myelinated nerve. J. Physiol. 292:149-166.
15. DEERINCK, T. J., LEVINSON, S. R., BENNETT, G. V., and ELLISMAN, M. H. (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.
16. DE NEEF, K. J., JANSEN, J. R., and VERSPRILLE, A. (1982). Developmental morphometry and physiology of the rabbit vagus nerve. Brain Res. 256:265-274.
17. DUGANDZIJA-NOVAKOVIC, S., KOSZOWSKI, A. G., LEVINSON, S. R., and SHRAGER, P. (1995). Clustering of Na channels and node of Ranvier formation in remyelinating axons. J. Neurosci. 15:492-502.
18. ENGLAND, J. D., GAMBONI, F., LEVINSON, S. R., and FINGER, T. E. (1990). Changed distribution of sodium channels along demyelinated axons. Proc. Natl. Acad. Sci. USA 87:6777-6780.
19. FELTS, P. A., BAKER, T. A., and SMITH, K. J. (1997a). Conduction in segmentally demyelinated mammalian central axons. J. Neurosci. 17:7267-7277.
20. FELTS, P. A., YOKOYAMA, S., DIB-HAJJ, S., BLACK, J. A., and WAXMAN, S. G. (1997b). Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Mol. Brain Res. 45:71-82.
21. FIELDS, R. D., BLACK, J. A., BOWE, C. M., KOCSIS, J. D., and WAXMAN, S. G. (1986). Differences in intramembranous particle distribution in the paranodal axolemma are not associated with functional differences of dorsal and ventral roots. Neurosci. Lett. 67:13-18.
22. FOSTER, R. E., CONNORS, B. W., and WAXMAN, S. G. (1982). Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development. Brain Res. 255:371-386.
23. FRIEDE, R. L. and BEUCHE, W. (1985). A new approach toward analyzing peripheral nerve fiber populations. J. Neuropathol. Exp. Neurol. 44:60-72.
24. HAIMOVICH, B., BONILLA, E., CASADEI, J., and BARCHI, R. (1984). Immunocytochemical localization of the mammalian voltage-dependent sodium channel using polyclonal antibodies against the purified protein. J. Neurosci. 4:2259-2268.
25. HALL, S. M. and GREGSON, N. A. (1974). The effects of mitomycin C on remyelination in the peripheral nervous system. Nature 252:303-305.
26. HILDEBRAND, C., BOWE, C. M., and REMAHL, I. N. (1994). Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibers. Progr. Neurobiol. 43:85-141.
27. HILDEBRAND, C., REMAHL, S., and WAXMAN, S. G. (1985). Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations. J. Neurocytol. 14:597-617.
28. HILDEBRAND, C. and WAXMAN, S. G. (1984). Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J. Comp. Neurol. 224:25-37.
29. HILLE, B. (1992). Ionic Channels of Excitable Membranes. Sinauer Associates, Sunderland, MA.
30. HUXLEY, A. F. and STAMPFLI, R. (1949). Evidence for saltatory conduction in peripheral myelinated nerve fibers. J. Physiol. 108:315-339.
31. ICHIMURA, T. and ELLISMAN, M. H. (1991). Three-dimensional fine structure of cytoskeletal-membrane interactions at nodes of Ran vier. J. Neurocytol. 20:667-681.
32. ISOM, L. L., RAGSDALE, D. S., DE JONGH, K. S., WESTEN-BROEK, R. E., REBER, B. F. X., SCHEUER, T., and CATTERALL, W. A. (1995). Structure and function of the beta-2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83:433-442.
33. JOE, E. H. and ANGELIDES, K. (1992). Clustering of voltage-dependent sodium channels on axons depends on Schwann cell contact. Nature 356:333-335.
34. JOHNSTON. W. L., DYER, J. R., CASTELLUCCI, V. F., and DUNN. R. J. (1996). Clustered voltage gated Na channels in Aplysia axons. J. Neurosci. 16:1730-1739.
35. KAPLAN, M. R., MEYER-FRANKE, A., LAMBERT, S., BENNETT, V., DUNCAN, I. D., LEVINSON, S. R., and BARRES, B. A. (1997). Induction of sodium channel clustering by oligodendrocytes. Nature 386:724-728.
36. KIM, E., NIETHAMMER, M., ROTHSCHILD, A., JAN, Y. N., and SHENG, M. (1995). Clustering of Shaker type K+ channels by interaction with a family of membrane associated guanylate kinases. Nature 378:85-88.
37. KOCSIS, J. D., RUIZ, J. A., and WAXMAN, S. G. (1983). Maturation of mammalian myelinated fibers: changes in action-potential characteristics following 4-amino-pyridine application. J. Neurophysiol. 50:449-463.
38. KORDELI, E., LAMBERT, S., and BENNETT, V. (1995). AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270:2352-2359.
39. LAMBERT, S., DAVIS, J. Q., and BENNETT, V. (1997). Morphogensis of the node of Ranvier, coclusters of ankyrin and ankyrin binding integral proteins define early developmental intermediates. J. Neurosci. 15:7025-7036.
40. Li, C., TROPAK, M. B., GERLAI, R., CLAPOFF, S., ABRAMOW-NEWERLY, W., TRAPP, B., PETERSON, A., and RODER, J. (1994). Myelination in the absence of myelin-associated glycoprotein. Nature 369:747-750.
41. MARTINI, R. and SCHACHNER, M. (1986). Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J. Cell Biol. 103:2439-2448.
42. MATA, M., ALESSI, D., and FINK, D. J. (1990). S100 is preferentially distributed in myelin-forming Schwann cells. J. Neurocytol. 19:432-442.
43. MESSING, A., BEHRINGER, R. R., HAMMANG, J. P., PALMITER, R. D., BRINSTER, R. L., and LEMKE, G. (1992). P0 promoter directs expression of reporter and toxin genes to Schwann cells of transgenic mice. Neuron 8:507-520.
44. Mi, H., DEERINCK, T. J., ELLISMAN, M. H., and SCHWARZ, T. L. (1995). Differential distribution of closely related potassium channels in rat Schwann cells. J. Neurosci. 15:3761-3774.
45. MONTAG, D., GIESE, K. P., BARTSCH, U., MARTINI, R., LANG, Y., BLUTHMANN, H., KARTHIGASAN, J., KIRSCHNER, D. A., WINTERGERST, E. S., NAVE, K. A., ZIELASEK, J., TOYKA, K. V., LIPP, H. P., and SCHACHNER, M. (1994). Mice deficient for the myelinassociated glycoprotein show subtle abnormalities in myelin. Neuron 13:229-246.
46. MORIMOTO, H. and BONAVIDA, B. (1992). Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis: ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J. Immunol. 149:2089-2094.
47. NOVAKOVIC, S. D., DEERINCK, T. J., LEVINSON, S. R., SHRAGER, P., and ELLISMAN, M. H. (1996). Clusters of axonal Na+ channels adjacent to remyelinating Schwann cells. J. Neurocytol. 25:403-412.
48. NOVAKOVIC, S. D., LEVINSON, S. R., SCHACHNER, M., and SHRAGER, P. (1998). Disruption and reorganization of sodium channels in experimental allergic neuritis. Muscle Nerve. 21:1019-1032.
49. PETERS, L. L., JOHN, K. M., LU, F. M., EICHER, E. M., HIGGINS, A., YIALAMAS, M., TURTZO, L. C., OTSUKA, A. J., and Lux, S. E. (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.
50. RASBAND, M. N., TRIMMER, J. S., SCHWARZ, T. L., LEVINSON, S. R., ELLISMAN, M. H., SCHACHNER, M., and SHRAGER, P. (1998). Potassium channel distribution, clustering, and function in remyelinating rat axons. J. Neurosci. 18:36-47.
51. RHODES, K. J., MONAGHAN, M. M., BARREZUETA, N. X., NAWOSCHIK, S., BEKELE-ARCURI, Z., MATOS, M. F., NAKAHIRA, K., SCHECHTER, L. E., and TRIMMER, J. S. (1996). Voltage-gated K+ channel beta subunits: expression and distribution of Kv beta 1 and Kv beta 2 in adult rat brain. J. Neurosci. 16:4846-4860.
52. RHODES, K. J., STRASSLE, B. W., MONAGHAN, M. M., BEKELEARCURI, Z., MATOS, M. F., and TRIMMER, J. S. (1997). Association and colocalization of the Kv-beta-1 and Kv-beta-2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes. J. Neurosci. 17:8246-8258.
53. RITCHIE, J. M. (1982). Sodium and potassium channels in regenerating and developing mammalian myelinated nerves. Proc. R. Soc. Lond. B. 215:273-287.
54. ROPER, J. and SCHWARZ, J. R. (1989). Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibers. J. Physiol. 416:93-110.
55. ROSENBLUTH, J. (1976). Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain. J. Neurocytol. 5:731-745.
56. ROSENBLUTH, J. (1988). Role of glial cells in the differentiation and function of myelinated axons. Int. J. Dev. Neurosci. 6:3-24.
57. SANGAMESWARAN, L., DELGADO, S. G., FISH, L. M., KOCH, B. D., JAKEMAN, L. B., STEWART, G. R., SZE, P., HUNTER, J. C., EGLEN, R. M., and HERMAN, R. C. (1996). Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271:5953-5956.
58. SANGAMESWARAN, L., FISH, L. M., KOCH, B. D., RABERT, D. K., DELGADO, S. G., ILNICKA, M., JAKEMAN, L. B., NOVAKOVIC, S., WONG, K., SZE, P., TZOUMAKA, E., STEWART, G. R., HERMAN, R. C., CHAN, H., EGLEN, R. M., and HUNTER, J. C. (1997). A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J. Biol. Chem. 272:14805-14809.
59. SHERRATT, R. M., BOSTOCK, H., and SEARS, T. A. (1980). Effects of 4-aminopyridine on normal and demyelinated mammalian nerve fibers. Nature 283:570-572.
60. SHI, G., NAKAHIRA, K., HAMMOND, S., RHODES, K. J., SCHECHTER, L. E., and TRIMMER, J. S. (1996). Beta subunits promote K+ channel surface expression through effects early in biosynthesis. Neuron 16:843-852.
61. SHRAGER. P. (1987). The distribution of sodium and potassium channels in single demyelinated axons of the frog. J. Physiol. 392:587-602.
62. SHRAGER, P. (1988). Ionic channels and signal conduction in single remyelinating frog nerve fibers. J. Physiol. 404:695-712.
63. SHRAGER, P. (1989). Sodium channels in single demyelinated mammalian axons. Brain Res. 483:149-154.
64. SHRAGER, P. (1993). Axonal coding of action potentials in demyelinated nerve fibers. Brain Res. 619:278-290.
65. SHRAGER, P. and RUBINSTEIN, C. T. (1990). Optical measurement of conduction in single demyelinated axons. J. Gen. Physiol. 95:867-889.
66. SRINIVASAN, J., LAENG, P., SCHACHNER, M., and CATTERALL, W. A. (1997). Interaction between neuronal voltage gated sodium channels and the extracellular matrix protein, tenascin. Soc. Neurosci. Abstr. 23:362.12.
67. SRINIVASAN, Y., ELMER, L., DAVIS, J., BENNETT, V., and ANGELIDES, K. (1988). Ankyrin and spectrin associate with voltage-dependent sodium channels in brain. Nature 333:117-180.
68. TAO-CHENG, J. H. and ROSENBLUTH, J. (1982). Development of nodal and paranodal membrane specializations in amphibian peripheral nerves. Brain Res. 255:577-594.
69. TAO-CHENG, J. H. and ROSENBLUTH, J. (1983). Axolemmal differentiation in myelinated fibers of rat peripheral nerves. Brain Res. 285:251-263.
70. TASAKI, I. and TAKEUCHI, T. (1942). Weitere Studien uber den Aktionsstrom der markhaltigen Nervensfasern und uber die elektrosaltatorische Ubertragung des Nervenimpulses. Pflugers Arch. 245:764-782.
71. TEJEDOR, F. J., BOKHARI, A., ROGERO, O., GORCZYCA, M., ZHANG, J., KIM, E., SHENG, M., and BUDNIK, V. (1997). Essential role for dig in synaptic clustering of Shaker K+ channels in vivo. J. Neurosci. 17:152-159.
72. TOLEDO-ARAL, J. J., BREHM, P., HALEGOUA, S., and MANDEL, G. (1995). A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron 14:607-611.
73. TOLEDO-ARAL, J. J., Moss, B. L., HE, Z. J., KOSZOWSKI, A. G., WHISENAND, T., LEVINSON, S. R., WOLF, J. J., SILOS-SANTIAGO, L, HALEGOUA, S., and MANDEL, G. (1997). Identification of PN1, a predominant voltage-dependent sodium channel expressed principally in peripheral neurons. Proc. Natl. Acad. Sci. USA 94:1527-1532.
74. TZOUMAKA, E., NOVAKOVIC, S. D., LEVINSON, S. R., and SHRAGER, P. (1995). Na+ channel aggregation in remyelinating mouse sciatic axons following transection. Glia 15:188-194.
75. VABNICK, I., MESSING, A., CHIU, S. Y., LEVINSON, S. R., SCHACHNER, M., RODER, J., LI, C., NOVAKOVIC, S., and SHRAGER, P. (1997a). Sodium channel distribution in axons of hypomyelinated and MAG null mutant mice. J. Neurosci. Res. 50:321-336.
76. VABNICK, I., NOVAKOVIC, S. D., LEVINSON, S. R., SCHACHNER, M., and SHRAGER, P. (1996). The clustering of axonal sodium channels during development of the peripheral nervous system. J. Neurosci. 16:4914-4922.
77. VABNICK, I., SCHWARZ, T. L., TRIMMER, J. S., LEVINSON, S. R., and SHRAGER, P. (1997b). K+ channel distribution during axonal development. Soc. Neurosci. Abstr. 23:476.17.
78. WANG, H., ALLEN, M. L., GRIGG, J. J., NOEBELS, J. L., and TEMPEL, B. L. (1995). Hypomyelination alters K+ channel expression in mouse mutants shiverer and Trembler. Neuron 15:1337-1347.
79. WANG, H., KUNKEL, D. D., MARTIN, T. M., SCHWARTZKROIN, P. A., and TEMPEL, B. L. (1993). Heteromultimeric K+ channels in terminal and juxta-paranodal regions of neurons. Nature 365:75-79.
80. WAXMAN, S. G., BLACK, J. A., and FOSTER, R. E. (1982). Freeze-fracture heterogeneity of the axolemma of premyelinated fibers in the CNS. Neurology 32:418-421.
81. WAXMAN, S. G., BLACK, J. A., KOCSIS, J. D., and RITCHIE, J. M. (1989). Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc. Natl. Acad. Sci. USA 86:1406-1410.
82. WAXMAN, S. G. and FOSTER, R. E. (1980). Development of the axon membrane during differentiation of myelinated fibers in spinal nerve roots. Proc. R. Soc. Lond. B 209:441-446.
83. WIGGINS, R. C., CHONGJIE, G., DELANEY, C., and SAMORAJSKI, T. (1988). Development of axonal-oligodendroglial relationships and junctions during myelination of the optic nerve. Int. J. Dev. Neurosci. 6:233-243.
84. WILEY-LIVINGSTON, C. and ELLISMAN, M. H. (1980). Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration. Dev. Biol. 79:334-355.
85. WOLLNER, D. A., MESSNER, D. J., and CATTERALL, W. A. (1987). Beta2 subunits of sodium channels from vertebrate brain: studies with subunit specific antibodies. J. Biol. Chem. 262:14709-14715.
86. WOLLNER, D. A., SCHEINMAN, R., and CATTERALL, W. A. (1988). Sodium channel expression and assembly during development of retinal ganglion cells. Neuron 1:727-737.
87. XIAO, Z. C., TAYLOR, J., MONTAG, D., ROUGON, G., and SCHACHNER, M. (1996). Distinct effects of recombinant tenascin-R domains in neuronal cell functions and identification of the domain interacting with the neuronal recognition molecule F3/11. Eur. J. Neurosci. 8:766-782.
88. YAMAMOTO, K., MERRY, A. C., and SIMA, A. A. (1996). An orderly development of paranodal axoglial junctions and bracelets of Nageotte in the rat sural nerve. Dev. Brain Res. 96:36-45.
89. ZISKIND-CONHEIM, L. (1988). Physiological and morphological changes in developing peripheral nerves of rat embryos. Dev. Brain Res. 42:15-28.
90. ZUR, K. B., OH, Y., WAXMAN, S. G., and BLACK, J. A. (1995). Differential up-regulation of sodium channel alpha- and beta 1-subunit mRNAs in cultured embryonic DRG neurons following exposure to NGF. Mol. Brain Res. 30:97-105.