Molecular mechanisms of node of Ranvier formation

Current Opinion in Cell Biology

Volumn 20, Issue 6, 2008, Pages 616-623

  Susuki, Keiichiro ^a   Rasband, Matthew N ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN G; BETA4 SPECTRIN; SPECTRIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; CELL ADHESION; CYTOSKELETON; EXTRACELLULAR MATRIX; MOLECULAR BIOLOGY; MYELINATION; NERVE FIBER; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; RANVIER NODE; REVIEW;

ANIMALS; ANKYRINS; CELL ADHESION MOLECULES, NEURONAL; CENTRAL NERVOUS SYSTEM; EXTRACELLULAR MATRIX; HUMANS; MODELS, BIOLOGICAL; NERVE FIBERS, MYELINATED; NERVE TISSUE PROTEINS; PERIPHERAL NERVOUS SYSTEM; RANVIER'S NODES; SPECTRIN;

EID: 56949103144     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2008.09.007     Document Type: Review

References (44)

1. Sherman D.L., and Brophy P.J. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6 (2005) 683-690
2. Hedstrom K.L., and Rasband M.N. Intrinsic and extrinsic determinants of ion channel localization in neurons. J Neurochem 98 (2006) 1345-1352
3. Poliak S., and Peles E. The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4 (2003) 968-980
4. Salzer J.L. Polarized domains of myelinated axons. Neuron 40 (2003) 297-318
5. Susuki K., and Rasband M.N. Spectrin and ankyrin-based cytoskeletons at polarized domains in myelinated axons. Exp Biol Med 233 (2008) 394-400
6. Spiegel I., Adamsky K., Eshed Y., Milo R., Sabanay H., Sarig-Nadir O., Horresh I., Scherer S.S., Rasband M.N., and Peles E. A central role for Necl4 (SynCAM4) in Schwann cell-axon interaction and myelination. Nat Neurosci 10 (2007) 861-869
7. Maurel P., Einheber S., Galinska J., Thaker P., Lam I., Rubin M.B., Scherer S.S., Murakami Y., Gutmann D.H., and Salzer J.L. Nectin-like proteins mediate axon Schwann cell interactions along the internode and are essential for myelination. J Cell Biol 178 (2007) 861-874
8. Eshed Y., Feinberg K., Poliak S., Sabanay H., Sarig-Nadir O., Spiegel I., Bermingham Jr. J.R., and Peles E. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron 47 (2005) 215-229
9. Eshed Y., Feinberg K., Carey D.J., and Peles E. Secreted gliomedin is a perinodal matrix component of peripheral nerves. J Cell Biol 177 (2007) 551-562. This study demonstrates that a secreted glial protein gliomedin is incorporated into nodal ECM and promotes the initial clustering of NF186 in PNS nodes.
10. Melendez-Vasquez C., Carey D.J., Zanazzi G., Reizes O., Maurel P., and Salzer J.L. Differential expression of proteoglycans at central and peripheral nodes of Ranvier. Glia 52 (2005) 301-308
11. Martin S., Levine A.K., Chen Z.J., Ughrin Y., and Levine J.M. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J Neurosci 21 (2001) 8119-8128
12. Saito F., Moore S.A., Barresi R., Henry M.D., Messing A., Ross-Barta S.E., Cohn R.D., Williamson R.A., Sluka K.A., Sherman D.L., et al. Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization. Neuron 38 (2003) 747-758
13. Maertens B., Hopkins D., Franzke C.W., Keene D.R., Bruckner-Tuderman L., Greenspan D.S., and Koch M. Cleavage and oligomerization of gliomedin, a transmembrane collagen required for node of Ranvier formation. J Biol Chem 282 (2007) 10647-10659
14. Koticha D., Maurel P., Zanazzi G., Kane-Goldsmith N., Basak S., Babiarz J., Salzer J., and Grumet M. Neurofascin interactions play a critical role in clustering sodium channels, ankyrin G and βIV spectrin at peripheral nodes of Ranvier. Dev Biol 293 (2006) 1-12
15. Dzhashiashvili Y., Zhang Y., Galinska J., Lam I., Grumet M., and Salzer J.L. Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol 177 (2007) 857-870. This study demonstrates the role of each domain in NF186 and ankyrinG for PNS node or AIS formation in detail, suggesting different mechanisms of formation for each of these domains. It also provides the first evidence to suggest that ankyrinG is necessary for the node of Ranvier formation.
16. Basak S., Raju K., Babiarz J., Kane-Goldsmith N., Koticha D., and Grumet M. Differential expression and functions of neuronal and glial neurofascin isoforms and splice variants during PNS development. Dev Biol 311 (2007) 408-422. This study shows the temporal regulation of each NF isoform in neurons and Schwann cells during the early developmental period.
17. Garver T.D., Ren Q., Tuvia S., and Bennett V. 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 (1997) 703-714
18. McEwen D.P., and Isom L.L. Heterophilic interactions of sodium channel beta1 subunits with axonal and glial cell adhesion molecules. J Biol Chem 279 (2004) 52744-52752
19. Sherman D.L., Tait S., Melrose S., Johnson R., Zonta B., Court F.A., Macklin W.B., Meek S., Smith A.J., Cottrell D.F., and Brophy P.J. Neurofascins are required to establish axonal domains for saltatory conduction. Neuron 48 (2005) 737-742
20. Zonta B., Tait S., Melrose S., Anderson H., Harroch S., Higginson J., Sherman D.L., and Brophy P.J. Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J Cell Biol 181 (2008) 1169-1177. This study demonstrates that the single NF gene is required for node formation: nodal and paranodal components are absent in NF-null mice. A transgenic approach for rescue experiments revealed the role of each NF isoform, and proved for the first time that paranodal junctions are sufficient to assemble CNS nodal Nav channel clusters.
21. Custer A.W., Kazarinova-Noyes K., Sakurai T., Xu X., Simon W., Grumet M., and Shrager P. The role of the ankyrin-binding protein NrCAM in node of Ranvier formation. J Neurosci 23 (2003) 10032-10039
22. Rosenbluth J. Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain. J Neurocytol 5 (1976) 731-745
23. Rasband M.N., Peles E., Trimmer J.S., Levinson S.R., Lux S.E., and Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19 (1999) 7516-7528
24. Bhat M.A., Rios J.C., Lu Y., Garcia-Fresco G.P., Ching W., St Martin M., Li J., Einheber S., Chesler M., Rosenbluth J., et al. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30 (2001) 369-383
25. Rios J.C., Rubin M., St Martin M., Downey R.T., Einheber S., Rosenbluth J., Levinson S.R., Bhat M., and Salzer J.L. Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J Neurosci 23 (2003) 7001-7011
26. Boyle M.E., Berglund E.O., Murai K.K., Weber L., Peles E., and Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30 (2001) 385-397
27. Rasband M.N., Taylor C.M., and Bansal R. Paranodal transverse bands are required for maintenance but not initiation of Nav1.6 sodium channel clustering in CNS optic nerve axons. Glia 44 (2003) 173-182
28. Yang Y., Ogawa Y., Hedstrom K.L., and Rasband M.N. βIV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J Cell Biol 176 (2007) 509-519. This study shows that the ankyrinG-binding site of βIV spectrin is required for βIV spectrin's localization to nodes and the AIS.
29. Komada M., and Soriano P. βIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 156 (2002) 337-348
30. Lacas-Gervais S., Guo J., Strenzke N., Scarfone E., Kolpe M., Jahkel M., De Camilli P., Moser T., Rasband M.N., and Solimena M. βIVΣ1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J Cell Biol 166 (2004) 983-990
31. Yang Y., Lacas-Gervais S., Morest D.K., Solimena M., and Rasband M.N. βIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J Neurosci 24 (2004) 7230-7240
32. Hedstrom K.L., Xu X., Ogawa Y., Frischknecht R., Seidenbecher C.I., Shrager P., and Rasband M.N. Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol 178 (2007) 875-886. This study reports that brevican is a binding partner of NF186 in the ECM surrounding AIS and CNS nodes of Ranvier. It also demonstrates that NF186 is dispensable for AIS assembly.
33. Jenkins S.M., and 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
34. Vabnick I., Novakovic S.D., Levinson S.R., Schachner M., and Shrager P. The clustering of axonal sodium channels during development of the peripheral nervous system. J Neurosci 16 (1996) 4914-4922
35. Schafer D.P., Custer A.W., Shrager P., and Rasband M.N. Early events in node of Ranvier formation during myelination and remyelination in the PNS. Neuron Glia Biol 2 (2006) 69-79
36. Lambert S., Davis J.Q., and 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
37. Schafer D.P., and Rasband M.N. Glial regulation of the axonal membrane at nodes of Ranvier. Curr Opin Neurobiol 16 (2006) 508-514
38. Schafer D.P., Bansal R., Hedstrom K.L., Pfeiffer S.E., and Rasband M.N. Does paranode formation and maintenance require partitioning of neurofascin 155 into lipid rafts?. J Neurosci 24 (2004) 3176-3185
39. Kaplan M.R., Meyer-Franke A., Lambert S., Bennett V., Duncan I.D., Levinson S.R., and Barres B.A. Induction of sodium channel clustering by oligodendrocytes. Nature 386 (1997) 724-728
40. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., Margolis R.U., Levinson S.R., Shrager P., Montag D., and Schachner M. 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
41. Huang J.K., Phillips G.R., Roth A.D., Pedraza L., Shan W., Belkaid W., Mi S., Fex-Svenningsen A., Florens L., Yates III J.R., and Colman D.R. Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310 (2005) 1813-1817
42. Nie D.Y., Ma Q.H., Law J.W., Chia C.P., Dhingra N.K., Shimoda Y., Yang W.L., Gong N., Chen Q.W., Xu G., et al. Oligodendrocytes regulate formation of nodes of Ranvier via the recognition molecule OMgp. Neuron Glia Biol 2 (2006) 151-164
43. Oohashi T., Hirakawa S., Bekku Y., Rauch U., Zimmermann D.R., Su W.D., Ohtsuka A., Murakami T., and 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
44. Brakebusch C., Seidenbecher C.I., Asztely F., Rauch U., Matthies H., Meyer H., Krug M., Böckers T.M., Zhou X., Kreutz M.R., et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22 (2002) 7417-7427