Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Na v1.6 and K v1.2 at nodes of Ranvier

Brain

Volumn 129, Issue 5, 2006, Pages 1319-1329

  Black, Joel A ^a,b   Waxman, Stephen G ^a,b   Smith, Kenneth J ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Demyelination; Remyelination; Schwann cell; Sodium channel; Spinal cord

Indexed keywords

ETHIDIUM BROMIDE; POTASSIUM CHANNEL KV1.2; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL NAV1.2; VOLTAGE GATED SODIUM CHANNEL NAV1.6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CONTUSION; DEMYELINATION; IMMUNOHISTOCHEMISTRY; MALE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RANVIER NODE; RAT; REMYELINIZATION; SCHWANN CELL; SPINAL CORD INJURY;

ANIMALS; AXONS; DEMYELINATING DISEASES; ETHIDIUM; KV1.2 POTASSIUM CHANNEL; MYELIN SHEATH; NERVE REGENERATION; NERVE TISSUE PROTEINS; RANVIER'S NODES; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; SODIUM CHANNELS; SPINAL CORD; SPINAL CORD DISEASES;

EID: 33646253436     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl057     Document Type: Article

References (79)

1. Akiyama Y, Radtke C, Kocsis JD. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 2002; 22: 6623-30.
2. Avellana-Adalid V, Bachelin C, Lachapelle F, Escriou C, Ratzkin B, Baron-Van Evercooren A. In vitro and in vivo behaviour of NDF-expanded monkey Schwann cells. Eur J Neurosci 1998; 10: 291-300.
3. Bachelin C, Lachapelle F, Girard C, Moissonnier P, Seguerra-Lagache C, Mallet J, et al. Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 2005; 128: 540-9.
4. Baron-Van Evercooren A, Blakemore WF. Remyelination through engraftment. In: Lazzarini RA, editor. Myelin biology and disorders. Burlington: Elsevier; 2004. p. 143-72.
5. Baron-Van Evercooren A, Gansmuller A, Duhamel E, Pascal F, Gumpel M. Repair of a myelin lesion by Schwann cells transplanted in the adult mouse spinal cord. J Neuroimmunol 1992; 40: 235-42.
6. Bhat MA. Molecular organization of axo-glial junctions. Curr Opin Neurobiol 2003; 13: 552-9.
7. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, et al. Axon-glia interactions and the domain organization of myelinated axons reques neurexin IV/Caspr/paranodin. Neuron 2001; 30: 369-83.
8. Black JA, Liu S, Cummin TR, Waxman SG. Changes in the expression of tetrodotoxin-sensitive sodium channel within dorsal root ganglia neurons in inflammatory pain. Pain 2004; 108: 237-47.
9. Blakemore WF. Remyelination by Schwann cells of axons demyelinated by intraspinal injections of 6-aminonicotinamide in the rat. J Neurocytol 1975; 4: 745-57.
10. Blakemore WF. Remyelination of CNS axons by Schwann cells transplanted from the sciatic nerve. Nature 1977; 266: 68-9.
11. Blakemore WF. The case for a central nervous system (CNS) origin for the Schwann cells that remyelinate CNS axons following concurrent loss of oligodendrocytes and astrocytes. Neuropathol App Neurobiol 2005; 31: 1-10.
12. Blakemore WF, Crang AJ, Franklin RJM, Tang K, Ryder S. Glial cell transplants that are subsequently rejected can be used to influence regeneration of glial cell environments in the CNS. Glia 1995; 13: 79-91.
13. Blight AR. Axonal physiology of chronic spinal cord injury in the cat: intracellular recording in vitro. Neuroscience 1983; 10: 1471-86.
14. Boiko T, Rasband MN, Levinson SR, Caldwell JH, Mandel G, Trimmer JS, et al. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 2001; 30: 91-104.
15. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30: 385-97.
16. Brierley CMH, Crang AJ, Iwashita Y, Gilson JM, Scolding NJ, Compston DAS, et al. Remyelination of demyelinated CNS axons by transplanted human Schwann cells: the deleterious effect of contaminating fibroblasts. Cell Transplant 2001; 10: 305-15.
17. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR. Sodium channel Nav1.6 is localized at nodes of Ranvier, dendrites and synapses. Proc Natl Acad Sci USA 2000; 97: 5616-20.
18. Chang A, Tourtellotte WW, Rudick R, Trapp BD. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002; 17: 346, 165-73.
19. Chari DM, Blakemore WF. New insights into remyelination failure in multiple sclerosis: implications for glial cell transplantation. Multipl Sclerosis 2002; 8: 271-7.
20. Coutzee T, Fujita N, Dupree J, Shi R, Blight A, Suzuki K, Popko B. Myelination in the absence of galactocerebroside and sulfatide: normal structure and abnormal function and regional instability. Cell 1996; 86: 209-19.
21. Craner MJ, Lo AC, Black JA, Waxman SG. Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination. Brain 2003; 126: 1552-61.
22. Dupree JL, Coetzee T, Blight A, Suzuki K, Popko B. Myelin galactolipids are essential for proper node of Ranvier formation in the CNS. J Neurosci 1998; 18: 1642-9.
23. Dupree JL, Mason JL, Marcus JR, Stull M, Levinson, R, Matsushima GK, et al. Oligodendrocytes assist in the maintenance of sodium channel clusters independent of the myelin sheath. Neuron Glia Biol 2005; 1: 1-14.
24. 0: new knowledge and new roles. Neurochem Res 2002; 27: 1331-40.
25. Felts PA, Smith KJ. Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Res 1992; 574: 178-92.
26. Felts PA, Smith KJ. Blood-brain barrier permeability in astrocyte-free regions of the central nervous system remyelinated by Schwann cells. Neuroscience 1996; 75: 643-55.
27. Felts PA, Baker TA, Smith KJ. Conduction in segmentally demyelinated mammalian central axons. J Neurosci. 1997; 17: 7267-77.
28. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG. Sodium channel α-subunit mRNAs I, II, III, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Mol Brain Res 1997; 45: 71-82.
29. Fjell J, Dib-Hajj S, Fried K, Black JA, Waxman SG. Differential expression of sodium channel genes in retinal ganglion cells. Mol Brain Res 1997; 50: 197-204.
30. Franklin RJM. Remyelination of the demyelinated CNS: the case for and against transplantation of central, peripheral and olfactory glia. Brain Res Bull 2002; 57: 827-32.
31. Gilson JM, Blakemore WF. Schwann cell remyelination is not replaced by oligodendrocyte remyelination following ethidium bromide induced demyelination. NeuroReport 2002; 13: 1205-8.
32. Girard C, Bemelmans A-P, Dufour N, Mallet J, Bachelin C, Nait-Oumesmar B, et al. Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J Neurosci 2005; 25: 7924-33.
33. Girault J-A, Peles E. Development of nodes of Ranvier. Curr Opin Neurobiol 2002; 12: 476-85.
34. Ghatak NR, Hirano A, Doron Y, Zimmerman HM. Remyelination in multiple sclerosis with peripheral type myelin. Arch Neurol 1973; 29: 262-7.
35. Goldin AL, Barchi, RL, Caldwell JH, Hofmann F, Howe JR, Hunter JC, et al. Nomenclature of voltage-gated sodium channels. Neuron 2000; 28: 365-8.
36. Honmou O, Felts PA, Waxman SG, Kocsis JD. Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 1996; 16: 3199-208.
37. Hughes RAC. Demyelinating neuropathy. In: Vinken PJ, Bruyn GW, Klawans HL, editors. Handbook of clinical neurology. Amersterdam: Elsevier; 1985. p. 605-27.
38. Itoyama Y, Ohnishi A, Tateishi J, Kuroiwa Y, Webster HdeF. Spinal cord multiple sclerosis lesion in Japanese patients: Schwann cell remyelination occurs in areas that lack glial fibrillary acidic protein (GFAP). Acta Neuropathol (Berl) 1985; 65: 217-23.
39. Jenkins SM, Bennett V. Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc Natl Acad Sci USA 2002; 99: 2303-8.
40. Johns TG, Bernard CCA. The structure and function of myelin oligodendrocyte glycoprotein. J Neurochem 1999; 72: 1-9.
41. v1.6 at developing CNS nodes of Ranvier. Neuron 2001; 30: 105-19.
42. Keirstead HS, Blakemore WF. The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Adv Exp Med Biol 1999; 468: 183-97.
43. Kocsis JD, Akiyama Y, Radtke C. Neural precursors as a cell source to repair the demyelinated spinal cord. J Neurotrama 2004; 21: 441-9.
44. Kohama I, Lankford K, Preiningerova J, White FA, Vollmer TL, Kocsis JD. Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinateed spinal cord. J Neurosci 2001; 21: 944-50.
45. Lachapelle F, Bachelin C, Moissonnier P, Nait-Oumesmar B, Hidalgo A, Fontaine D, et al. Failure of remyelination in the nonhuman primate optic nerve. Brain Pathol 2005; 15: 198-207.
46. Lankford K, Imaizumi T, Honmou O, Kocsis JD. A quantitative morphometric analysis of rat spinal cord remyelination following transplantation of allogenic Schwann cells. J Comp Neurol 2002; 443: 259-74.
47. Lubetzki C, Williams A, Stankoff B. Promoting repair in multiple sclerosis: problems and prospects. Curr Opin Neurol 2005; 18: 237-44.
48. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol; 2000; 47: 707-17.
49. Mackay-Sim A. Olfactory ensheathing cells and spinal cord repair. Keio J Med 2005; 54: 8-14.
50. McDonald WI, Sears TA. The effects of experimental demyelination on conduction in the central nervous system. Brain 1970; 93: 583-98.
51. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert St, Bretscher A, Salzer JL. Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci USA 2001; 98: 1235-40.
52. Menegoz M, Gaspar P, Bert ML, Galvez T, Burgaya F, Palfrey C, et al. Paranodin, a glycoprotein of neuronal paranodal membranes. Neuron 1997; 19: 319-31.
53. Mi H, Deerinck TJ, Ellisman MH, Schwarz TL. Differential distribution of closely related potassium channels in rat Schwann cells. J Neurosci 1995; 15: 3761-74.
54. Peles E, Nativ M, Lustig M, Grumet M, Schilling J, Martinez R, et al. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J 1997; 16: 978-88.
55. Pluchino S, Furlan R, Martino G. Cell-based remyelinating therapies in multiple sclerosis: evidence from experimental studies. Curr Opin Neurol 2004; 17: 247-55.
56. Poliak S, Peles E. The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 2003; 4: 968-80.
57. Prineas JW, Connell F. Remyelination in multiple sclerosis. Ann Neurol 1979; 5: 22-31.
58. Prineas JW, Kwon EE, Cho E-S, Sharer LR. Continual breakdown and regeneration of myelin in progress multiple sclerosis plaques. Ann NY Acad Sci 1984; 436: 11-32.
59. Prineas JW, Barnard RO, Revesz T, Kwon EE, Sharer L, Cho ES. Pathology of recurrent lesions. Brain 1993; 116: 681-93.
60. Rasband MN. It's 'juxta' potassium channel! J Neurosci Res 2004; 76: 749-57.
61. Rasband MN, Trimmer JS. Developmental clustering of ion channels at and near the node of Ranvier. Dev Biol 2001a; 236: 5-16.
62. + channels in spinal cord. J Comp Neurol 2001b; 429: 166-171
63. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 1999a; 19: 7516-28
64. + channel distribution and clustering in developing and hypomyelinated axons of the optic nerve. J Neurocytol 1999b; 28: 319-31.
65. Rasband MN, Kagawa T, Park EW, Ikenaka K, Trimmer JS. Dysregulation of axonal sodium channel isoforms after adult-onset chronic demyelination. J Neurosci Res 2003; 73: 465-70.
66. Rios JC, Rubin M, St Martin M, Downey RT, Einheber S, Rosenbluth J, et al. Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J Neurosci 2003; 23: 7001-11.
67. Rodriquez M, Oleszak E, Leibowitz J. Theiler's murine encephalomyelitis: a model of demyelination and persistence of virus. Crit Rev Immunol 1987; 7: 325-65.
68. Salzer JL. Nodes of Ranvier come of age. Trends Neurosci 2002; 25: 2-5.
69. Sasaki M, Lankford KL, Zemedkun M, Kocsis JD. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 2004; 24:8485-93.
70. Schafer DP, Custer AW, Shrager P, Rasband MN. Early events in node of Ranvier formation during myelination and remyelination in the PNS. Neuron Glia Biology 2006. In press.
71. Schaller KL, Caldwell JH. Developmental regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J Comp Neurol 2000; 420: 84-97
72. Scherer SS, Xu T, Crino P, Arroyo EJ, Gutmann DH. Ezrin, radixin, and moesin are components of Schwann cell microvilli. J Neurosci Res 2001; 65150-64.
73. Smith KJ, Blakemore WF, McDonald WI. Central remyelination restores secure conduction. Nature 1979; 280: 395-6.
74. Smith KJ, Blakemore WF, McDonald WI. Restoration of conduction by central remyelination. Brain 1981; 104: 383-404.
75. Vabnick I, Novakovic SD, Levinson SR, Schachner M, Shrager P. The clustering of axonal sodium channels during development of the peripheral nervous system. J Neurosci 1996; 16: 4914-22.
76. Wang H, Kunkel DD, Martin TM Schwartzkroin PA, Tempel BL. Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365: 75-9.
77. Waxman SG. Demyelination in spinal cord injury and multiple sclerosis: what can we do to enhance functional recovery? J Neurotrama 1992; 9 (Suppl 1): S105-17.
78. Waxman SG, Ritchie JM. Molecular dissection of the myelinated axon. Ann Neurol 1993; 33: 121-36.
79. + channel subtypes in central neurons. Neuron 1989; 3: 695-704.