Development of nodes of Ranvier

Current Opinion in Neurobiology

Volumn 12, Issue 5, 2002, Pages 476-485

  Girault, Jean Antoine ^a   Peles, Elior ^b  

^a INSTITUT DU FER À MOULIN   (France)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; ION; ION CHANNEL; MEMBRANE PROTEIN; POTASSIUM; POTASSIUM CHANNEL; SODIUM CHANNEL; SODIUM ION;

ARTICLE; BIOLOGICAL MODEL; CELL ASSAY; CELL CONTACT; CYTOSKELETON; GLIA CELL; MOLECULAR BIOLOGY; MUTANT; MYELINATED NERVE; NERVE FIBER; NERVE GROWTH; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; RANVIER NODE;

EID: 0036802264     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(02)00370-7     Document Type: Review

References (73)

1. Arroyo E.J., Scherer S.S. On the molecular architecture of myelinated fibers. Histochem Cell Biol. 113:2000;1-18.
2. Pedraza L., Huang J.K., Colman D.R. Organizing principles of the axoglial apparatus. Neuron. 30:2001;335-344.
3. Peles E., Salzer J.L. Molecular domains of myelinated axons. Curr Opin Neurobiol. 10:2000;558-565.
4. Scherer S.S., Arroyo E.J. Recent progress on the molecular organization of myelinated axons. J Peripher Nerv Syst. 7:2002;1-12.
5. Spiegel I., Peles E. Cellular junctions of myelinated nerves. Mol Memb Biol. 19:2002;95-101.
6. Waxman S.G., Ritchie J.M. Molecular dissection of the myelinated axon. Ann Neurol. 33:1993;121-136.
7. Isom L.L. The role of sodium channels in cell adhesion. Front Biosci. 7:2002;12-23.
8. Caldwell J.H., Schaller K.L., Lasher R.S., Peles E., Levinson S.R. Sodium channel Na(v)1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc Natl Acad Sci USA. 97:2000;5616-5620.
9. v1.2 channels and ankyrin G in neurons in culture. This clustering requires an intact actin cytoskeleton, protein synthesis and vesicle trafficking, suggesting the involvement of a nodal-specific transport mechanism.
10. Ratcliffe C.F., Westenbroek R.E., Curtis R., Catterall W.A. Sodium channel beta1 and beta3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain. J Cell Biol. 154:2001;427-434.
11. Malhotra J.D., Kazen-Gillespie K., Hortsch M., Isom L.L. Sodium channel beta subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact. J Biol Chem. 275:2000;11383-11388.
12. 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.
13. + channels and increases their functional expression. J Neurosci. 21:2001;7517-7525.
14. Rios J.C., Melendez-Vasquez C.V., Einheber S., Lustig M., Grumet M., Hemperly J., Peles E., Salzer J.L. Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci. 20:2000;8354-8364.
15. Faivre-Sarrailh C., Gauthier F., Denisenko-Nehrbass N., Le Bivic A., Rougon G., Girault J.A. The GPI-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/caspr. J Cell Biol. 149:2000;491-502.
16. v1.2 and ankyrin G, and challenges the role of the β subunit in anchoring the channel to ankyrin G.
17. Berghs S., Aggujaro D., Dirkx R. Jr, Maksimova E., Stabach P., Hermel J.M., Zhang J.P., Philbrick W., Slepnev V., Ort T., et al. Beta IV spectrin, a new spectrin localized at axon initial segments and nodes of Ranvier in the central and peripheral nervous system. J Cell Biol. 151:2000;985-1002.
18. v1.6 sodium channels at nodes of Ranvier and at axon initial segments. See also [72•] .
19. 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.
20. Koroll M., Rathjen F.G., Volkmer H. The neural cell recognition molecule neurofascin interacts with syntenin-1 but not with syntenin-2, both of which reveal self-associating activity. J Biol Chem. 276:2001;10646-10654.
21. Lustig M., Zanazzi G., Sakurai T., Blanco C., Levinson S.R., Lambert S., Grumet M., Salzer J.L. Nr-CAM and neurofascin interactions regulate ankyrin G and sodium channel clustering at the node of Ranvier. Curr Biol. 11:2001;1864-1869. This study provides evidence for a direct interaction between NrCAM and neurofascin extracellular domains and their role in node organization. The authors also show that a soluble NrCAM-Ig chimera inhibited the accumulation of ankyrin G and sodium channels at nodes of Ranvier.
22. Bartsch U., Pesheva P., Raff M., Schachner M. Expression of janusin (J1-160/180) in the retina and optic nerve of the developing and adult mouse. Glia. 9:1993;57-69.
23. Srinivasan J., Schachner M., Catterall W.A. Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci USA. 95:1998;15753-15757.
24. Xiao Z.C., Ragsdale D.S., Malhotra J.D., Mattei L.N., Braun P.E., Schachner M., Isom L.L. Tenascin-R is a functional modulator of sodium channel beta subunits. J Biol Chem. 274:1999;26511-26517.
25. Martin S., Levine A.K., Chen Z.J., Ughrin Y., Levine J.M. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J Neurosci. 21:2001;8119-8128.
26. Oohashi T., Hirakawa S., Bekku Y., Rauch U., Zimmermann D.R., Su W.D., Ohtsuka A., Murakami T., Ninomiya Y. Bral1, a brain-specific link protein, colocalizing with the versican V2 isoform at the nodes of Ranvier in developing and adult mouse central nervous systems. Mol Cell Neurosci. 19:2002;43-57.
27. Melendez-Vasquez C.V., Rios J.C., Zanazzi G., Lambert S., Bretscher A., Salzer J.L. Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci USA. 98:2001;1235-1240. The authors demonstrate the enrichment of ezrin and EBP50 in perinodal Schwann cells processes in vivo and in cocultures of Schwann cells and dorsal root ganglia neurons. Ezrin clusters colocalized with ankyrin G clusters early on during development, providing direct evidence of a direct contact between Schwann cells and axons during the organization of nodal regions. See also [28•], which shows that moesin and radixin have a similar location.
28. Scherer S.S., Xu T., Crino P., Arroyo E.J., Gutmann D.H. Ezrin, radixin, and moesin are components of Schwann cell microvilli. J Neurosci Res. 65:2001;150-164. See annotation to [27••] .
29. Trapp B.D., Andrews S.B., Wong A., O'Connell M., Griffin J.W. Co-localization of the myelin-associated glycoprotein and the microfilament components, F-actin and spectrin, in Schwann cells of myelinated nerve fibres. J Neurocytol. 18:1989;47-60.
30. Ichimura T.E. Three-dimensional fine structure of cytoskeletal-membrane interactions at nodes of Ranvier. J Neurocytol. 20:1991;667-681.
31. Wiley C.A., Ellisman M.H. Rows of dimeric-particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal glial-axonal junction at the node of Ranvier. J Cell Biol. 84:1980;261-280.
32. Menegoz M., Gaspar P., Le Bert M., Galvez T., Burgaya F., Palfrey C., Ezan P., Amos F., Girault J.A. Paranodin, a glycoprotein of neuronal paranodal membranes. Neuron. 19:1997;319-331.
33. Einheber S., Zanazzi G., Ching W., Scherer S., Milner T.A., Peles E., Salzer J.L. 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. 139:1997;1495-1506.
34. + channels. Neuron. 24:1999;1037-1047.
35. Peles E., Nativ M., Lustig M., Grumet M., Schilling J., Martinez R., Plowman G.D., Schlessinger J. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 16:1997;978-988.
36. Spiegel I., Salomon D., Erne B., Schaeren-Wiemers N., Peles E. Caspr3 and Caspr4, two novel members of the Caspr family are expressed in the nervous system and interact with PDZ domains. Mol Cell Neurosci. 20:2002;283-297.
37. Baumgartner S., Littleton J.T., Broadie K., Bhat M.A., Harbecke R., Lengyel J.A., Chiquet-Ehrisman R., Prokop A., Bellen H.J. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell. 87:1996;1059-1068.
38. Yuan L.L., Ganetzky B. A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. Science. 283:1999;1343-1345.
39. + channels to the juxtaparanodal region.
40. Boyle M.E., Berglund E.O., Murai K.K., Weber L., Peles E., Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron. 30:2001;385-397. This paper demonstrates the close functional association of contactin and Caspr/paranodin in vivo. In contactin knockout mice, Caspr/paranodin was absent from axons and paranodes and was retained in cell bodies, showing the importance of the interaction between the two proteins for their proper targeting in vivo (note that, conversely, contactin was not detected at paranodes of Caspr/paranodin knockout mice [39••] ). The morphological and functional phenotype of contactin mutant mice in central and peripheral neuronal fibers was similar to that of Caspr/paranodin knockout mice. Because both proteins were absent from paranodes in either mutant, it is not possible to identify their specific role in these regions.
41. Tait S., Gunn-Moore F., Collinson J.M., Huang J., Lubetzki C., Pedraza L., Sherman D.L., Brophy P.J. An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol. 150:2000;657-666.
42. Poliak S., Gollan L., Salomon D., Berglund E.O., Ohara R., Ranscht B., Peles E. Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J Neurosci. 21:2001;7568-7575. This paper provides a detailed study of the localization of Caspr/paranodin and Caspr2 in wild-type and various mutant mice, showing that their distribution is mutually exclusive, and suggesting their possible role in the generation of 'barriers' along the axon.
43. Charles P., Tait S., Faivre-Sarrailh C., Barbin G., Gunn-Moore F., Denisenko-Nehrbass N., Guennoc A.M., Girault J.A., Brophy P.J., Lubetzki C. Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol. 12:2002;217-220. This paper shows that NF155 associates with the Caspr/paranodin and contactin complex. Surprisingly, the addition of a soluble NF155 protein to cocultures of neurons and oligodendrocytes inhibits myelination, suggesting a possible role for NF155 in myelination.
44. Girault J.A., Labesse G., Mornon J.-P., Callebaut I. The FAKs and JAKs play in the 4.1 band: a superfamily of band 4.1 domains important for cell structure and signal transduction. Mol Med. 4:1998;751-769.
45. Ohara R., Yamakawa H., Nakayama M., Ohara O. Type II brain 4.1 (4.1B/KIAA0987), a member of the protein 4.1 family, is localized to neuronal paranodes. Brain Res Mol Brain Res. 85:2000;41-52.
46. Gollan L., Sabanay H., Poliak S., Berglund S.R., Ranscht B., Peles E. Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J Cell Biol. 157:2002;1247-1256. Here Gollan et al. demonstrate that the extracellular region of Caspr/paranodin is sufficient to direct it to the paranodal junction. However, retention of the Caspr/paranodin and contactin complex at this site requires its intracellular domain, which interacts with protein 4.1B.
47. Lamb R.S., Ward R.E., Schweizer L., Fehon R.G. Drosophila Coracle, a member of the protein 4.1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol Biol Cell. 9:1998;3505-3519.
48. Rasband M.N., Trimmer J.S. Developmental clustering of ion channels at and near the node of Ranvier. Dev Biol. 236:2001;5-16.
49. Baba H., Akita H., Ishibashi T., Inoue Y., Nakahira K., Ikenaka K. Completion of myelin compaction, but not the attachment of oligodendroglial processes triggers K(+) channel clustering. J Neurosci Res. 58:1999;752-764.
50. Traka M., Dupree J.L., Popko B., Karagogeos D. The neuronal adhesion protein TAG-1 is expressed by Schwann cells and oligodendrocytes and is localized to the juxtaparanodal region of myelinated fibers. J Neurosci. 22:2002;3016-3024. These authors demonstrate the expression of TAG1 in myelinating glial cells and its enrichment at juxtaparanodes.
51. + ion removal from the periaxonal space.
52. Rasband M.N., Shrager P. Ion channel sequestration in central nervous system axons. J Physiol. 525:2000;63-73.
53. Rasband M.N., Peles E., Trimmer J.S., Levinson S.R., Lux S.E., Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci. 19:1999;7516-7528.
54. Dupree J.L., Girault J.A., Popko B. Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol. 147:1999;1145-1152.
55. Arroyo E.J., Xu T., Grinspan J., Lambert S., Levinson S.R., Brophy P.J., Peles E., Scherer S.S. Genetic dysmyelination alters the molecular architecture of the nodal region. J Neurosci. 22:2002;1726-1737. This paper provides a careful and detailed study of the distribution of nodal, paranodal and juxtaparanodal proteins in md rats, which carry a mutation of the plp protein. The alterations in md rats are similar to those observed in jimpy mice, which also have a plp mutation [57••] .
56. Jenkins S.M., Bennett V. Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc Natl Acad Sci USA. 99:2002;2303-2308.
57. Mathis C., Denisenko-Nehrbass N., Girault J.A., Borrelli E. Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions. Development. 128:2001;4881-4890.
58. Mathis C., Hindelang C., LeMeur M., Borrelli E. A transgenic mouse model for inducible and reversible dysmyelination. J Neurosci. 20:2000;7698-7705.
59. Ching W., Zanazzi G., Levinson S.R., Salzer J.L. Clustering of neuronal sodium channels requires contact with myelinating Schwann cells. J Neurocytol. 28:1999;295-301.
60. Deerinck T.J., Levinson S.R., Bennett G.V., Ellisman M.H. Clustering of voltage-sensitive sodium channels on axons is independent of direct Schwann cell contact in the dystrophic mouse. J Neurosci. 17:1997;5080-5088.
61. Kaplan M.R., Meyer-Franke A., Lambert S., Bennett V., Duncan I.D., Levinson S.R., Barres B.A. Induction of sodium channel clustering by oligodendrocytes. Nature. 386:1997;724-728.
62. v1.2 is found in unmyelinated fibers. In shiverer mice, which lack compact myelin, this shift is severely altered.
63. 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. Jenkins and Bennett demonstrate the requirement for ankyrin G in the organization of axon initial segments. These results underline the important role of ankyrin G in a region that has a high degree of homology with the nodes of Ranvier.
64. Lambert S., Davis J.Q., Bennett V. Morphogenesis of the node of Ranvier: Co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J Neurosci. 17:1997;7025-7036.
65. Zhou D., Lambert S., Malen P.L., Carpenter S., Boland L.M., Bennett V. Ankyrin G 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.
66. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., Margolis R.U., Levinson S.R., Shrager P., Montag D., et al. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci. 19:1999;4245-4262.
67. Arroyo E.J., Xu Y.T., Zhou L., Messing A., Peles E., Chiu S.Y., Scherer S.S. Myelinating Schwann cells determine the internodal localization of Kv1.1, Kv1.2, Kvbeta2, and Caspr. J Neurocytol. 28:1999;333-347.
68. Honke K., Hirahara Y., Dupree J., Suzuki K., Popko B., Fukushima K., Fukushima J., Nagasawa T., Yoshida N., Wada Y., et al. Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci USA. 99:2002;4227-4232.
69. Ishibashi T., Dupree J.L., Ikenaka K., Hirahara Y., Honke K., Peles E., Popko B., Suzuki K., Nishino H., Baba H. A myelin galactolipid, sulfatide is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J Neurosci. 22:2002;6507-6514. Here the previously reported phenotype of mice deficient in galactosylsulfamide transferase [68], which lack sulfatides, is studied in much more detail. The alterations in the nodal regions of these mice are shown to be very similar to those in mice deficient in both ceramides and sulfatides [54] .
70. Marcus J., Dupree J.L., Popko B. Myelin-associated glycoprotein and myelin galactolipids stabilize developing axo-glial interactions. J Cell Biol. 156:2002;567-577. In this paper, a detailed morphological study of the role of galactolipids in the formation of paranodal junctions is presented. The authors also study their functional interaction with myelin-associated glycoprotein. This study provides interesting clues about the development of the ultrastructural features of paranodes.
71. Vabnick I., Novakovic S.D., Levinson S.R., Schachner M., Shrager P. The clustering of axonal sodium channels during development of the peripheral nervous system. J Neurosci. 16:1996;4914-4922.
72. + channels in the absence of nodal βIV spectrin. They suggest that the different nodal domains are coupled through the cortical cytoskeleton.
73. Malhotra J.D., Tsiotra P., Karagogeos D., Hortsch M. Cis-activation of L1-mediated ankyrin recruitment by TAG-1 homophilic cell adhesion. J Biol Chem. 273:1998;33354-33359.