Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of ranvier

Journal of Neuroscience

Volumn 23, Issue 18, 2003, Pages 7001-7011

  Rios, Jose C ^a   Rubin, Marina ^a   St Martin, Mary ^a   Downey, Ryan T ^b   Einheber, Steven ^a   Rosenbluth, Jack ^a   Levinson, S Rock ^b   Bhat, Manzoor ^c,d   Salzer, James L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Caspr; Myelin; Nodes; Paranodal junction; Potassium channels; Sodium channels

Indexed keywords

CONTACTIN; PROTEIN SUBUNIT; SODIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CENTRAL NERVOUS SYSTEM FUNCTION; CHANNEL GATING; CONTROLLED STUDY; DIFFUSION; MOUSE; MOUSE MUTANT; MYELINATED NERVE; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE GROWTH; NEURULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANVIER NODE; REGULATORY MECHANISM;

EID: 0041624581     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-18-07001.2003     Document Type: Article

References (41)

1. Arroyo EJ, Xu YT, Zhou L, Messing A, Peles E, Chiu SY, Scherer SS (1999) Myelinating Schwann cells determine the internodal localization of Kv1.1, Kv1.2, Kvbeta2, and Caspr. J Neurocytol 28:333-347.
2. Arroyo EJ, Xu T, Grinspan J, Lambert S, Levinson SR, Brophy PJ, Peles E, Scherer SS (2002) Genetic dysmyelination alters the molecular architecture of the nodal region. J Neurosci 22:1726-1737.
3. Bennett V, Lambert S (1999) Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J Neurocytol 28:303-318.
4. Berghs S, Aggujaro D, Dirkx Jr R, 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. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, Martin MS, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axonglia interactions and the domain organization of myelinated axons requires Neurexin IV/Caspr/Paranodin. Neuron 30:369-383.
6. Black JA, Fjell J, Dib-Hajj S, Duncan ID, O'Connor LT, Fried K, Gladwell Z, Tate S, Waxman SG (1999) Abnormal expression of SNS/PN3 sodium channel in cerebellar Purkinje cells following loss of myelin in the taiep rat. NeuroReport 10:913-918.
7. 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.
8. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, Matthews G (2003) Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23:2306-2313.
9. Boyle MET, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30:385-397.
10. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR (2000) Sodium channel Na(v) 1.6 is localized at nodes of ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 97:5616-5620.
11. Dupree JL, Coetzee T, Blight A, Suzuki K, Popko B (1998) Myelin galactolipids are essential for proper node of Ranvier formation in the CNS. J Neurosci 18:1642-1649.
12. Dupree JL, Girault JA, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147:1145-1152.
13. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA, Peles E, Salzer JL (1997) 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 139:1495-1506.
14. 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.
15. Hildebrand C, Bowe CM, Remahl IN (1994) Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibres. Prog Neurobiol 43:85-141.
16. Hille B (2001) Ion channels of excitatory membranes. Sunderland, MA: Sinauer Associates.
17. Honke K, Hirahara Y, Dupree J, Suzuki K, Popko B, Fukushima K, Fukushima J, Nagasawa T, Yoshida N, Wada Y, Taniguchi N (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci USA 99:4227-4232.
18. Ishibashi T, Dupree JL, Ikenaka K, Hirahara Y, Honke K, Peles E, Popko B, Suzuki K, Nishino H, Baba H (2002) A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J Neurosci 22:6507-6514.
19. 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 USA 99:2303-2308.
20. Kaplan MR, Cho M, 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.
21. Kearney JA, Buchner DA, De Haan G, Adamska M, Levin SI, Furay AR, Albin RL, Jones JM, Montal M, Stevens MJ, Sprunger LK, Meisler MH (2002) Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a (Na(v) 1.6). Hum Mol Genet 11:2765-2775.
22. Knapp PE, Skoff RP, Redstone DW (1986) Oligodendroglial cell death in jimpy mice: an explanation for the myelin deficit. J Neurosci 6:2813-2822.
23. Komada M, Soriano P (2002) βIV-Spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 156:337-348.
24. Marcus J, Dupree JL, Popko B (2002) Myelin-associated glycoprotein and myelin galactolipids stabilize developing axo-glial interactions. J Cell Biol 156:567-577.
25. Massa PT, Mugnaini E (1982) Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7:523-538.
26. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert S, Bretscher A, Salzer JL (2001) Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci USA 98:1235-1240.
27. Menegoz M, Gaspar P, Bert ML, Galvez T, Burgaya F, Palfrey C, Ezan P, Arnos F, Girault J-A (1997) Paranodin, a glycoprotein of neuronal paranodal membranes. Neuron 19:319-331.
28. Peles E, Salzer JL (2000) Molecular domains of myelinated axons. Curr Opin Neurobiol 10:558-565.
29. Peles E, Nativ M, Lustig M, Grumet M, Schilling J, Martinez R, Plowman GD, Schlessinger J (1997) Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J 16:978-988.
30. Poliak S, Gollan L, Martinez R, Custer A, Einheber S, Salzer JL, Trimmer JS, Shrager P, Peles E (1999) Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels. Neuron 24:1037-1047.
31. Poliak S, Gollan L, Salomon D, Berglund EO, Ohara R, Ranscht B, Peles E (2001) Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J Neurosci 21:7568-7575.
32. Rasband MN, Shrager P (2000) Ion channel sequestration in central nervous system axons. J Physiol (Lond) 525:63-73.
33. Rash JE, Yasumura T, Dudek FE, Nagy JI (2001) Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci 21:1983-2000.
34. Ratcliffe CF, Westenbroek RE, Curtis R, Catterall WA (2001) Sodium channel β1 and β3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain. J Cell Biol 154:427-434.
35. Rios JC, Melendez-Vasquez CV, Einheber S, Lustig M, Grumet M, Hemperly J, Peles E, Salzer JL (2000) Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20:8354-8364.
36. 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.
37. Rosenbluth J, Dupree JL, Popko B (2003) Nodal sodium channel domain integrity depends on the conformation of the paranodal junction, not on the presence of transverse bands. Glia 41:318-325.
38. Sandri C, Van Buren JM, Akert K (1977) Membrane morphology of the vertebrate nervous system. Prog Brain Res 46:201-265.
39. Tao-Cheng JH, Rosenbluth J (1983) Axolemmal differentiation in myelinated fibers of rat peripheral nerves. Brain Res 285:251-263.
40. Traka M, Dupree JL, Popko B, Karagogeos D (2002) 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 22:3016-3024.
41. Westenbroek RE, Noebels JL, Catterall WA (1992) Elevated expression of type II Na+ channels in hypomyelinated axons of shiverer mouse brain. J Neurosci 12:2259-2267.