Genetic dysmyelination alters the molecular architecture of the nodal region

Journal of Neuroscience

Volumn 22, Issue 5, 2002, Pages 1726-1737

  Arroyo, Edgardo J ^a   Xu, Theodore ^a   Grinspan, Judith ^b   Lambert, Stephen ^c   Levinson, S Rock ^d   Brophy, Peter J ^e   Peles, Elior ^f   Scherer, Steven S ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Axon glia interactions; Mutant; Myelin; Oligodendrocytes; Proteolipid protein; Septate junctions

Indexed keywords

ANKYRIN; CONTACTIN; GLYCOPHORIN; NEUROFASCIN 155; PARANODIN; PDZ PROTEIN; POTASSIUM CHANNEL; PROTEIN; PROTEIN CASPR; PROTEOLIPID PROTEIN; SODIUM CHANNEL; SPECTRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DEATH; CELL SUBPOPULATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; GAIT DISORDER; GLIA; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR BIOLOGY; MYELIN DEFICIENCY; MYELIN SHEATH; MYELINATED NERVE; MYELINATION; NERVE FIBER; NERVE FIBER MEMBRANE; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; SPINAL CORD; STUDENT T TEST; TREMOR;

EID: 0036523104     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-05-01726.2002     Document Type: Article

References (60)

1. Arroyo EJ, Scherer SS (2000) On the molecular architecture of myelinated fibers. Histochem Cell Biol 113:1-18.
2. Arroyo EJ, Xu T, Poliak S, Watson M, Peles E, Scherer SS (2001) Internodal specializations of myelinated axons in the CNS. Cell Tissue Res 305:53-66.
3. Baba H, Akita H, Ishibashi T, Inoue Y, Nakahira K, Ikenaka K (1999) Completion of myelin compaction, but not the attachment of oligodendroglial processes triggers K+ channel clustering. J Neurosci Res 58:752-764.
4. Baron P, Kamholz J, Scherer SS, Honda Scherer, Shy M, Scarpini E, Scarlato G, Pleasure D (1993) Appearance of PLP mRNA in specific regions of the developing rat lumbosacral spinal cord as revealed by in situ hybridization. Exp Neurol 121:139-147.
5. Barron KD, Dentinger MP, Csiza CK, Keegan SM, Mankes R (1987) Abnormalities of central axons in a dysmyelinative rat mutant. Exp Mol Pathol 47:125-142.
6. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li JJ, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axon-glia interactions, the domain organization of myelinated axons requires Neurexin IV/Caspr/Paranodin. Neuron 30:369-383.
7. Boiko T, Rasb MN, Levinson SR, Coldwell 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. 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.
9. Bronstein JM, Chen K, TiwariWoodruff S, Kornblum HI (2000) Developmental expression of OSP/claudin-11. J Neurosci Res 60:284-290.
10. v1.6 is localized at nodes of Ranvier, dendrites, synapses. Proc Natl Acad Sci USA 97:5616-5620.
11. Dentinger MP, Barron KD, Csiza CK (1982) Ultrastructure of the central nervous system in a myelin deficient rat. J Neurocytol 11:671-691.
12. + channels and node of Ranvier formation in remyelinating axons. J Neurosci 15:492-503.
13. Duncan ID, Hammang JP, Trapp BD (1987) Abnormal compact myelin in the myelin-deficient rat: Absence of proteolipid protein correlates with a defect in the intraperiod line. Proc Natl Acad Sci USA 84:6287-6291.
14. Dupree JL, Girault JA, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147:1145-1151.
15. ffrench-Constant C, Miller RH, Kruse J, Schachner M, Raff MC (1986) Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve. J Cell Biol 102:844-852.
16. ffrench-Constant C, Raff MC (1986) The oligodendrocyte-type-2 astrocyte cell lineage is specialized for myelination. Nature 323:335-338.
17. Fjell J, Hjelmstrom P, Hormuzdiar W, Milenkovic M, Aglieco F, Tyrrell L, Dib-Haji S, Waxman SG, Black JA (2000) Localization of the tetrodotoxin-resistant sodium channel NaN in nociceptors. Neuro-Report 11:199-202.
18. Goldin AL (1999) Diversity of mammalian voltage-gated sodium channels. Ann NY Acad Sci 868:38-50.
19. Gow A, Southwood CM, Lazzarini RA (1998) Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus-Merzbacher disease. J Cell Biol 140:925-934.
20. Gow A, Southwood CM, Li JS, Pariali M, Riordan GP, Brodie SE, Dania J, Branstein JM, Kachar B, Lazzarini RA (1999) CNS myelin and Sertoli cell tight junctions strands are absent in Osp/claudin-11 null mice. Cell 99:649-659.
21. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610-1613.
22. Grinspan JB, Marchionni M, Reeves M, Coulaloglou M, Scherer SS (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: Neuregulin receptors and the role of neuregulins. J Neurosci 16:6107-6118.
23. Grinspan JB, Coulaloglou M, Beesley JS, Carpio D, Scherer SS (1998) Maturation-dependent apoptotic cell death of oligodendroglial cells in myelin-deficient rats. J Neurosci Res 54:623-634.
24. Hildebrand C, Waxman SG (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.
25. Kaplan MR, Meyer-Franke A, Lambert S, Bennett V, Duncan ID, Levinson SR, Barres BA (1997) Induction of sodium channel clustering by oligodendrocytes. Nature 386:724-728.
26. v1.6 at developing CNS nodes of Ranvier. Neuron 40:105-119.
27. Lambert S, Davis JQ, Bennett V (1997) Morphogenesis of the node of Ranvier: Co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J Neurosci 17:7025-7036.
28. Langford LA, Coggeshall RE (1981) Unmyelinated axons in the posterior funiculi. Science 211:176-177.
29. Lee V, Wu HL, Schlaepfer WW (1982) Monoclonal antibodies recognized individual neurofilament triplet proteins. Proc Natl Acad Sci USA 79:6089-6092.
30. Lee VM-Y, Carden MJ, Schlaepfer WW, Trojanowski JQ (1987) Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J Neurosci 7:3474-3488.
31. Lipsitz D, Goetz BD, Duncan ID (1998) Apoptotic glial cell death and kinetics in the spinal cord of the myelin-deficient rat. J Neurosci Res 51:497-507.
32. Morita K, Sasaki H, Fujimoto K, Furuse M, Tsukita S (1999) Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145:579-588.
33. Nave K-A, Boespflug-Tanguy O (1996) Developmental defects of myelin formation: From X-linked mutations to human dysmyelinating diseases. Neuroscientist 2:33-43.
34. Noebels JL, Marcom PK, Jalilina-Tehrani MH (1991) Sodium channel density in hypomyelinated brain increased by myelin basic protein gene deletion. Nature 352:431-434.
35. + channels adjacent to remyelinating Schwann cells. J Neurocytol 25:403-412.
36. Pedraza L, Owens GC, Green LAD, Salzer JL (1990) The myelin-associated glycoproteins: Membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation. J Cell Biol 111:2651-2661.
37. Peles E, Salzer JL (2000) Molecular domains of myelinated fibers. Curr Opin Neurobiol 10:558-565.
38. Peles E, Nativ M, Campbell PL, Sakurai T, Martinez R, Lev S, Clary DO, Schilling J, Barnea G, Plowman GD, Grumet M, Schlessinger J (1995) The carbonic anhydrase domain of receptor tyrosine phosphatase β is a functional ligand for the axonal cell recognition molecule contactin. Cell 82:251-260.
39. Peles E, Nativ M, Lustig M, Grumet M, 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.
40. + channels. Neuron 24:1037-1047.
41. Poliak S, Gollan L, Salomon D, Berglund EO, Ranscht B, Peles E (2001) Localization of Caspr2 in myelinated nerves depends on axon-glia interactions, the generation of barriers along the axon. J Neurosci 21:7568-7575.
42. Popko B (2000) Myelin galactolipids mediators of axon-glial interactions? Glia 29:149-153.
43. Rasband M, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, Shrager P (1998) Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18:36-47.
44. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P (1999) Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19:7516-7528.
45. Rasband MN, Shrager P (2000) Ion channel sequestration in central nervous system axons J Physiol (Lond) 525:63-73.
46. Rasband MN, Trimmer JS (2001a) Developmental clustering of ion channels at and near the node of Ranvier. Dev Biol 236:5-16.
47. + channels in spinal cord. J Comp Neurol 429:166-176.
48. Rios JC, MelandezVasquez CV, Einheber S, Lustig M, Grumet M, Hemperly J, Peles E, Salzer JL (2000) Contactin-associated protein (Caspr), contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20:8354-8364.
49. Rosenbluth J (1981) Axoglial junctions in the mouse mutant shiverer. Brain Res 208:283-297.
50. Rosenbluth J (1987) Abnormal axoglial junctions in the myelin-deficient rat mutant. J Neurocytol 16:497-509.
51. Rosenbluth J (1995) Pathology of demyelinated and dysmyelinated axons. In: The Axon (Waxman S, Kocsis J, and Stys P, eds), pp 391-411. New York: Oxford UP.
52. Schaller KL, Caldwell JH (2000) Developmental, regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J Comp Neurol 420:84-97.
53. Struckhoff G, Przyrembel C, Bahr M, Gocht A (1997) Fate of developing astrocytes in the optic nerve of the myelin-deficient rat. J Comp Neurol 378:105-116.
54. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C, Pedraza L, Sherman DL, Colman DR, Brophy PJ (2000) An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150:657-666.
55. Trimmer PA, Wunderlich RE (1990) Changes in astroglial scar formation in rat optic nerve as a function of development. J Comp Neurol 296:359-378.
56. Vabnick I, Messing A, Chiu SY, Levinson SR, Schachner M, Roder J, Li CM, Novakovic S, Shrager P (1997) Sodium channel distribution in axons of hypomyelinated and MAG null mutant mice. J Neurosci Res 50:321-336.
57. + channel expression in mouse mutants shiverer and Trembler. Neuron 15:1337-1347.
58. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, Schachner M (1999) Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19:4245-4262.
59. + channel subtypes in central neurons. Neuron 3:695-704.
60. + channels in hypomyelinated axons of shiverer mouse brain. J Neurosci 12:2259-2267.