Sodium channels and multiple sclerosis: Roles in symptom production, damage and therapy

Brain Pathology

Volumn 17, Issue 2, 2007, Pages 230-242

  Smith, Kenneth J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; BEPRIDIL; CALCIUM CHANNEL BLOCKING AGENT; FLECAINIDE; LIDOCAINE; METHYLPREDNISOLONE; PHENYTOIN; SIPATRIGINE; SODIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ALLERGIC ENCEPHALOMYELITIS; BRAIN FUNCTION; CONFERENCE PAPER; DEMYELINATION; DISEASE COURSE; DRUG EFFICACY; DRUG MECHANISM; ENCEPHALITIS; GUILLAIN BARRE SYNDROME; HUMAN; IMMUNIZATION; LYMPHOCYTE; MONOCYTE; MULTIPLE SCLEROSIS; NERVE BLOCK; NERVE CONDUCTION; NERVE FIBER DEGENERATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; REMYELINIZATION; TREATMENT OUTCOME;

ACTION POTENTIALS; ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NEURONS; SODIUM CHANNELS;

EID: 33947546463     PISSN: 10156305     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2007.00066.x     Document Type: Conference Paper

References (156)

1. Aboul-Enein F, Lassmann H (2005) Mitochondrial damage and histotoxic hypoxia: a pathway of tissue injury in inflammatory brain disease? Acta Neuropathol (Berl) 109:49-55.
2. Aboul-Enein F, Rauschka H, Kornek B, Stadelmann C, Stefferl A, Bruck W, Lucchinetti C, Schmidbauer M, Jellinger K, Lassmann H (2003) Preferential loss of myelin-associated glycoprotein reflects hypoxia-like white matter damage in stroke and inflammatory brain diseases. J Neuropathol Exp Neurol 62:25-33.
3. Ahern GP, Hsu S-F, Klyachko VA, Jackson MB (2000) Induction of persistent sodium current by exogenous and endogenous nitric oxide. J Biol Chem 275:28810-28815.
4. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262.
5. Ames A III (2000) CNS energy metabolism as related to function. Brain Res Brain Res Rev 34:42-68.
6. Aulkemeyer P, Hausner G, Brinkmeier H, Weber F, Wurz A, Rudel R (2000) The small sodium-channel blocking factor in the cerebrospinal fluid of multiple sclerosis patients is probably an oligopeptide. J Neurol Sci 172:49-54.
7. Baker M, Bostock H (1992) Ectopic activity in demyelinated spinal root axons of the rat. J Physiol (Lond) 451:539-552.
8. Bechtold DA, Smith KJ (2005) Sodium-mediated axonal degeneration in inflammatory demyelinating disease. J Neurol Sci 233:27-35.
9. Bechtold DA, Kapoor R, Smith KJ (2002) Axonal protection mediated by flecainide therapy in experimental inflammatory demyelinating disease. J Neurol 249(Suppl. 1):204.
10. Bechtold DA, Kapoor R, Smith KJ (2004) Axonal protection using flecainide in experimental autoimmune encephalomyelitis. Ann Neurol 55:607-616.
11. Bechtold DA, Yue X, Evans RM, Davies M, Gregson NA, Smith KJ (2005) Axonal protection in experimental autoimmune neuritis by the sodium channel blocking agent flecainide. Brain 128:18-28.
12. Bechtold DA, Miller SJ, Dawson AC, Sun Y, Kapoor R, Berry D, Smith KJ (2006) Axonal protection achieved in a model of multiple sclerosis using lamotrigine. J Neurol 253:1542-1551.
13. Bidani A, Heming TA (1997) Effects of lidocaine on cytosolic pH regulation and stimulus-induced effector functions in alveolar macrophages. Lung 175:349-361.
14. Bitsch A, Wegener C, Costa C, Bunkowski S, Reimers CD, Prange HW, Bruck W (1999) Lesion development in Marburg's type of acute multiple sclerosis: from inflammation to demyelination. Mult Scler 5:138-146.
15. Black JA, Felts P, Smith KJ, Kocsis JD, Waxman SG (1991) Distribution of sodium channels in chronically demyelinated spinal cord axons: immuno-ultrastructural localization and electrophysiological observations. Brain Res 544:59-70.
16. Black JA, Dib-Hajj S, Baker D, Newcombe J, Cuzner ML, Waxman SG (2000) Sensory neuronspecific sodium channel SNS is abnormally expressed in the brains of mice with experimental allergic encephalomyelitis and humans with multiple sclerosis. Proc Natl Acad Sci USA 97:11598-11602.
17. Black JA, Liu S, Hains BC, Saab CY, Waxman SG (2006) Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 129:3196-3208.
18. Black JA, Waxman SG, Smith KJ (2006) Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Nav1.6 and Kv1.2 at nodes of Ranvier. Brain 129:1319-1329.
19. Blakemore WF, Smith KJ (1983) Node-like axonal specializations along demyelinated central nerve fibres: ultrastructural observations. Acta Neuropathol 60:291-296.
20. 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.
21. Bolanos JP, Almeida A, Stewart V, Peuchen S, Land JM, Clark JB, Heales SJR (1997) Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J Neurochem 68:2227-2240.
22. Bornstein MB, Crain SM (1965) Functional studies of cultured brain tissues as related to "demyelinative disorders". Science 148:1242-1244.
23. Bostock H (1994) The pathophysiology of demyelination. In: Multiple Sclerosis: Current Status of Research and Treatment. RM Herndon, FJ Seil (eds), pp. 89-112. Demos Publications, Inc.: New York.
24. Bostock H, Grafe P (1985) Activity-dependent excitability changes in normal and demyelinated rat spinal root axons. J Physiol (Lond) 365:239-257.
25. Bostock H, Rothwell JC (1997) Latent addition in motor and sensory fibres of human peripheral nerve. J Physiol 498:277-294.
26. Bostock H, Sears TA (1976) Continuous conduction in demyelinated mammalian nerve fibers. Nature 263:786-787.
27. Bostock H, Sears TA (1978) The internodal axon membrane: electrical excitability and continuous conduction in segmental demyelination. J Physiol (Lond) 280:273-301.
28. Bradford AL, Ismailov II, Achard JM, Warnock DG, Bubien JK, Benos DJ (1995) Immunopurification and functional reconstitution of a Na+ channel complex from rat lymphocytes. Am J Physiol 269:C601-C611.
29. Brickner RM (1950) The significance of localised vasoconstrictions in multiple sclerosis. Res Publ Assoc Res Nerv Ment Dis 28:236-244.
30. Brinkmeier H, Aulkemeyer P, Wollinsky KH, Rudel R (2000) An endogenous pentapeptide acting as a sodium channel blocker in inflammatory autoimmune disorders of the central nervous system. Nat Med 6:808-811.
31. Brinkmeier H, Weber F, Aulkemeyer P, Wollinsky KH, Rudel R (2003) The pentapeptide QYNAD does not block voltage-gated sodium channels. Neurology 60:1871-1872.
32. Brown GC, Borutaite V (2002) Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic Biol Med 33:1440-1450.
33. Brusa A, Jones SJ, Plant GT (2001) Long-term remyelination after optic neuritis: a 2-year visual evoked potential and psychophysical serial study. Brain 124:468-479.
34. Bubien JK, Warnock DG (1993) Amiloride-sensitive sodium conductance in human B lymphoid cells. Am J Physiol 265:C1175-C1183.
35. 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.
36. Centonze D, Rossi S, Boffa L, Versace V, Palmieri MG, Caramia MD, Bernardi G (2005) CSF from MS patients can induce acute conduction block in the isolated optic nerve. Eur J Neurol 12:45-48.
37. Charcot JM (1868) Histologie de la sclerose en plaque. Gaz Hop (Paris) 41:554-566.
38. Coles AJ, Wing MG, Molyneux P, Paolillo A, Davie CM, Hale G, Waldmann H, Compston A (1999) Monoclonal antibody treatment exposes three mechanisms underlying the clinical course of multiple sclerosis. Ann Neurol 46:296-304.
39. Craner MJ, Lo AC, Black JA, Baker D, Newcombe J, Cuzner ML, Waxman SG (2003) Annexin II/p11 is up-regulated in Purkinje cells in EAE and MS. Neuroreport 14:555-558.
40. Craner MJ, Lo AC, Black JA, Waxman SG (2003) Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination. Brain 126:1552-1561.
41. Craner MJ, Hains BC, Lo AC, Black JA, Waxman SG (2004) Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE. Brain 127:294-303.
42. Craner MJ, Newcombe J, Black JA, Hartle C, Cuzner ML, Waxman SG (2004) Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger. Proc Natl Acad Sci USA 101:8168-8173.
43. Craner MJ, Damarjian TG, Liu S, Hains BC, Lo AC, Black JA, Newcombe J, Cuzner ML, Waxman SG (2005) Sodium channels contribute to microglia/macrophage activation and function in EAE and MS. Glia 49:220-229.
44. Cummins TR, Renganathan M, Stys PK, Herzog RI, Scarfo K, Horn R, Dib-Hajj SD, Waxman SG (2003) The pentapeptide QYNAD does not block voltage-gated sodium channels. Neurology 60:224-229.
45. Davis FA, Schauf CL (1981) Approaches to the development of pharmacological interventions in multiple sclerosis. Adv Neurol 31:505-510.
46. Davis FA, Bergen D, Schauf C, McDonald I, Deutsch W (1976) Movement phosphenes in optic neuritis: a new clinical sign. Neurology 26:1100-1104.
47. Deerinck TJ, Levinson SR, Bennett GV, Ellisman MH (1997) Clustering of voltage-sensitive sodium channels on axons is independent of direct Schwann cell contact in the dystrophic mouse. J Neurosci 17:5080-5088.
48. DeLuca GC, Williams K, Evangelou N, Ebers GC, Esiri MM (2006) The contribution of demyelination to axonal loss in multiple sclerosis. Brain 129:1507-1516.
49. Denny-Brown D, Brenner C (1944) Lesion in peripheral nerve resulting from compression by spring clip. Arch Neurol Psychiatry 52:1-19.
50. Devaux J, Forni C, Beeton C, Barbaria J, Beraud E, Gola M, Crest M (2003) Myelin basic protein-reactive T cells induce conduction failure in vivo but not in vitro. Neuroreport 14:317-320.
51. Duchen MR (2004) Roles of mitochondria in health and disease. Diabetes 53(Suppl. 1):S96-S102.
52. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, Gudz T, Macklin WB, Lewis DA, Fox RJ, Rudick R, Mirnics K, Trapp BD (2006) Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59:478-489.
53. Eder C (1998) Ion channels in microglia (brain macrophages). Am J Physiol 275:C327-C342.
54. Elliott AA, Elliott JR (1993) Characterization of TTX-sensitive and TT X-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol (Lond) 463:39-56.
55. England S, Bevan S, Docherty RJ (1996) PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase a cascade. J Physiol 495:429-440.
56. Felts PA, Smith KJ (1992) Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Res 574:178-192.
57. Felts PA, Kapoor R, Smith KJ (1995) A mechanism for ectopic firing in central demyelinated axons. Brain 118:1225-1231.
58. Felts PA, Baker TA, Smith KJ (1997) Conduction in segmentally demyelinated mammalian central axons. J Neurosci 17:7267-7277.
59. Ferguson B, Matyszak MK, Esiri MM, Perry VH (1997) Axonal damage in acute multiple sclerosis lesions. Brain 120:393-399.
60. Gallin EK (1991) Ion channels in leukocytes. Physiol Rev 71:775-811.
61. Garthwaite G, Goodwin DA, Garthwaite J (1999) Nitric oxide stimulates cGMP formation in rat optic nerve axons, providing a specific marker of axon viability. Eur J Neurosci 11:4367-4372.
62. Garthwaite G, Goodwin DA, Batchelor AM, Leeming K, Garthwaite J (2002) Nitric oxide toxicity in CNS white matter: an in vitro study using rat optic nerve. Neuroscience 109:145-155.
63. Gilliatt RW (1982) Electrophysiology of peripheral neuropathies - an overview. Muscle Nerve 5:S108-S116.
64. Gold MS, Zhang L, Wrigley DL, Traub RJ (2002) Prostaglandin E(2) modulates TTX-R I(Na) in rat colonic sensory neurons. J Neurophysiol 88:1512-1522.
65. Guzman NJ, Fang MZ, Tang SS, Ingelfinger JR, Garg LC (1995) Autocrine inhibition of Na+/K(+)-ATPase by nitric oxide in mouse proximal tubule epithelial cells. J Clin Invest 95:2083-2088.
66. Hammarstrom AKM, Gage PW (1999) Nitric oxide increases persistent sodium current in rat hippocampal neurons. J Physiol (Lond) 520:451-461.
67. Herzog RI, Liu C, Waxman SG, Cummins TR (2003) Calmodulin binds to the C terminus of sodium channels Nav1.4 and Nav1.6 and differentially modulates their functional properties. J Neurosci 23:8261-8270.
68. Hjorth RJ, Willison RG (1973) The electromyogram in facial myokymia and hemifacial spasm. J Neurol Sci 20:117-126.
69. Honmou O, Felts PA, Waxman SG, Kocsis JD (1996) Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 16:3199-3208.
70. Imaizumi T, Lankford KL, Kocsis JD (2000) Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res 854:70-78.
71. Iwata A, Stys PK, Wolf JA, Chen XH, Taylor AG, Meaney DF, Smith DH (2004) Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J Neurosci 24:4605-4613.
72. Jeffery ND, Blakemore WF (1997) Locomotor deficits induced by experimental spinal cord demyelination are abolished by spontaneous remyelination. Brain 120:27-37.
73. Kanchandani R, Howe JG (1982) Lhermitte's sign in multiple sclerosis: a clinical survey and review of the literature. J Neurol Neurosurg Psychiat 45:308-312.
74. Kaplan MR, Cho MH, 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.
75. Kapoor R, Li YG, Smith KJ (1997) Slow sodium-dependent potential oscillations contribute to ectopic firing in mammalian demyelinated axons. Brain 120:647-652.
76. Kapoor R, Davies M, Blaker PA, Hall SM, Smith KJ (2003) Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 53:174-180.
77. Kaspar A, Brinkmeier H, Rudel R (1994) Local anaesthetic-like effect of interleukin-2 on muscular Na+ channels: no evidence for involvement of the IL-2 receptor. Pflugers Arch 426:61-67.
78. Khan NA, Poisson JP (1999) 5-HT3 receptorchannels coupled with Na+ influx in human T cells: role in T cell activation. J Neuroimmunol 99:53-60.
79. Kohama I, Lankford KL, Preiningerova J, White FA, Vollmer TL, Kocsis JD (2001) Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinated spinal cord. J Neurosci 21:944-950.
80. Kornek B, Storch MK, Weissert R, Wallstroem E, Stefferl A, Olsson T, Linington C, Schmidbauer M, Lassmann H (2000) Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 157:267-276.
81. Korotzer AR, Cotman CW (1992) Voltage-gated currents expressed by rat microglia in culture. Glia 6:81-88.
82. Lai ZF, Chen YZ, Nishimura Y, Nishi K (2000) An amiloride-sensitive and voltage-dependent Na+ channel in an HLA-DR-restricted human T cell clone. J Immunol 165:83-90.
83. Lassmann H, Wekerle H (2006) The pathology of multiple sclerosis. In: McAlpine's Multiple Sclerosis. A Compston, C Confavreux, H Lassmann, I McDonald, D Miller, J Noseworthy, K Smith, H Wekerle (eds), pp. 557-599. Churchill Livingstone: London.
84. Lhermitte J, Bollack J, Nicholas M (1924) Les douleurs à type de décharge électrique consécutives à la flexion céphalique dans la sclérose en plaques. Rev Neurol 2:56-62.
85. Li Z, Chapleau MW, Bates JN, Bielefeldt K, Lee H-C, Abboud FM (1998) Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 20:1039-1049.
86. Lo AC, Saab CY, Black JA, Waxman SG (2003) Phenytoin protects spinal cord axons and P axonal conduction and neurological function in a model of neuroinflammation in vivo. J Neurophysiol 90:3566-3571.
87. Lu JL, Sheikh KA, Wu HS, Zhang J, Jiang ZF, Cornblath DR, Asbury AK, Griffin JW, Ho TW (2000) Physiologic-pathologic correlation in Guillain-Barre syndrome in children. Neurology 54:33-39.
88. Mackay RP, Hirano A (1967) Forms of benign multiple sclerosis with report of two "clinically silent" cases discovered at autopsy. Trans Am Neurol Assoc 92:143-149.
89. Makowska A, Bechtold DA, Sajic M, Gregson N, Hughes RAC, Smith KJ (2004) Effect of sodium channel blocking agents on T cell activation. J Immunol 154:88.
90. Mathey E, Derfuss T, Storch M, Hales K, Rasband M, Velhin S, Hohlfeld R, Meint E, Linington C (2007) Neurofascin: a novel target for antibody mediated axonal injury in multiple sclerosis. Eur J Neurol (in press).
91. McDonald I (1998) Pathophysiology of multiple sclerosis. In: McAlpine's Multiple Sclerosis. A Compston, G Ebers, H Lassmann, I McDonald, B Matthews, H Wekerle (eds), pp. 359-378. Churchill Livingstone: London.
92. McDonald WI (1963) The effects of experimental demyelination on conduction in peripheral nerve: a histological and electrophysiological study. II. Electrophysiological observations. Brain 86:501-524.
93. McDonald WI (1975) Mechanisms of functional loss and recovery in spinal cord damage. In: Outcome of Severe Damage to the Central Nervous System. 23-33.
94. McDonald WI, Sears TA (1969) Effect of demyelination on conduction in the central nervous system. Nature 221:182-183.
95. McDonald WI, Sears TA (1970) The effects of experimental demyelination on conduction in the central nervous system. Brain 93:583-598.
96. McDonald WI, Sears TA (1970) Effect of a demyelinating lesion on conduction in the central nervous system studied in single nerve fibres. J Physiol (Lond) 207:53P-54P.
97. Meuth SG, Budde T, Duyar H, Landgraf P, Broicher T, Elbs M, Brock R, Weller M, Weissert R, Wiendl H (2003) Modulation of neuronal activity by the endogenous pentapeptide QYNAD. Eur J Neurosci 18:2697-2706.
98. Mogyoros I, Bostock H, Burke D (2000) Mechanisms of paresthesias arising from healthy axons. Muscle Nerve 23:310-320.
99. Moreau T, Coles A, Wing M, Isaacs J, Hale G, Waldmann H, Compston A (1996) Transient increase in symptoms associated with cytokine release in patients with multiple sclerosis. Brain 119:225-237.
100. Nordin M, Nystrom B, Wallin U, Hagbarth KE (1984) Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns. Pain 20:231-245.
101. Norenberg W, Illes P, Gebicke-Haerter PJ (1994) Sodium channel in isolated human brain macrophages (microglia). Glia 10:165-172.
102. Novakovic SD, Levinson SR, Schachner M, Shrager P (1998) Disruption and reorganization of sodium channels in experimental allergic neuritis. Muscle Nerve 21:1019-1032.
103. O'Riordan JI, Losseff NA, Phatouros C, Thompson AJ, Moseley IF, Macmanus DG, McDonald WI, Miller DH (1998) Asymptomatic spinal cord lesions in clinically isolated optic nerve, brain stem, and spinal cord syndromes suggestive of demyelination. J Neurol Neurosurg Psychiat 64:353-357.
104. Oh Y, Warnock DG (1997) Expression of the amiloride-sensitive sodium channel beta subunit gene in human B lymphocytes. J Am Soc Nephrol 8:126-129.
105. Otto F, Kieseier BC, Gortz P, Hartung HP, Siebler M (2005) The pentapeptide QYNAD does not inhibit neuronal network activity. Can J Neurol Sci 32:344-348.
106. Padmashri R, Chakrabarti KS, Sahal D, Mahalakshmi R, Sarma SP, Sikdar SK (2004) Functional characterization of the pentapeptide QYNAD on rNav1.2 channels and its NMR structure. Pflugers Arch 447:895-907.
107. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, Sorensen P, Brueck W, Lucchinetti C, Lassmann H (2006) Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129:3165-3172.
108. Phadke JG, Best PV (1983) Atypical and clinically silent multiple sclerosis: a report of 12 cases discovered unexpectedly at necropsy. J Neurol Neurosurg Psychiat 46:414-420.
109. Pieri C, Recchioni R, Moroni F, Balkay L, Marian T, Tron L, Damjanovich S (1989) Ligand and voltage gated sodium channels may regulate electrogenic pump activity in human, mouse and rat lymphocytes. Biochem Biophys Res Commun 160:999-1002.
110. Prineas JW, Connell F (1979) Remyelination in multiple sclerosis. Ann Neurol 5:22-31.
111. Prineas JW, Kwon EE, Sharer LR, Cho E-S (1987) Massive early remyelination in acute multiple sclerosis. Neurology 37(Suppl. 1):109.
112. Quasthoff S, Pojer C, Mori A, Hofer D, Liebmann P, Kieseier BC, Schreibmayer W (2003) No blocking effects of the pentapeptide QYNAD on Na+ channel subtypes expressed in Xenopus oocytes or action potential conduction in isolated rat sural nerve. Neurosci Lett 352:93-96.
113. Redford EJ, Kapoor R, Smith KJ (1997) Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120:2149-2157.
114. + currents in axotomized C-type DRG neurons. J Neurophysiol 83:2431-2442.
115. Renganathan M, Gelderblom M, Black JA, Waxman SG (2003) Expression of Nav1.8 sodium channels perturbs the firing patterns of cerebellar Purkinje cells. Brain Res 959:235-242.
116. Ritchie JM, Rogart RB (1977) Density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath. Proc Natl Acad Sci USA 74:211-215.
117. Rizzo MA, Kocsis JD, Waxman SG (1996) Mechanisms of paresthesiae, dysesthesiae, and hyperesthesiae: role of Na+ channel heterogeneity. Eur Neurol 36:3-12.
118. Rosenbluth J, Tao-Cheng J-H, Blakemore WF (1985) Dependence of axolemmal differentiation on contact with glial cells in chronically demyelinated lesions of cat spinal cord. Brain Res 358:287-302.
119. Rush AM, Dib-Hajj SD, Waxman SG (2005) Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J Physiol 564:803-815.
120. Saab CY, Craner MJ, Kataoka Y, Waxman SG (2004) Abnormal Purkinje cell activity in vivo in experimental allergic encephalomyelitis. Exp Brain Res 158:1-8.
121. +)-ATPase activity from porcine cerebral cortex by NO generating drugs. Brain Res 704:117-120.
122. + conductance by tumor necrosis factor in identified neurons of Aplysia kurodai. J Neurosci Res 28:466-473.
123. + conductance in identified neurons of Aplysia. Brain Res 670:248-256.
124. Selhorst JB, Saul RF (1995) Uhthoff and his symptom. J Neuroophthalmol 15:63-69.
125. Shrager P (1977) Slow sodium inactivation in nerve after exposure to sulhydryl blocking reagents. J Gen Physiol 69:183-202.
126. Shrager P, Custer AW, Kazarinova K, Rasband MN, Mattson D (1998) Nerve conduction block by nitric oxide that is mediated by the axonal environment. J Neurophysiol 79:529-536.
127. Smith KJ (1994) Conduction properties of central demyelinated and remyelinated axons, and their relation to symptom production in demyelinating disorders. Eye 8:224-237.
128. Smith KJ, Lassmann H (2002) The role of nitric oxide in multiple sclerosis. Lancet Neurol 1:232-241.
129. Smith KJ, McDonald WI (1980) Spontaneous and mechanically evoked activity due to central demyelinating lesion. Nature 286:154-155.
130. Smith KJ, McDonald WI (1982) Spontaneous and evoked electrical discharges from a central demyelinating lesion. J Neurol Sci 55:39-47.
131. Smith KJ, Blakemore WF, McDonald WI (1979) Central remyelination restores secure conduction. Nature 280:395-396.
132. Smith KJ, Blakemore WF, McDonald WI (1981) The restoration of conduction by central remyelination. Brain 104:383-404.
133. Smith KJ, Bostock H, Hall SM (1982) Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline. J Neurol Sci 54:13-31.
134. Smith KJ, Felts PA, Kapoor R (1997) Axonal hyperexcitability: mechanisms and role in symptom production in demyelinating diseases. Neuroscientist 3:237-246.
135. Smith KJ, Kapoor R, Hall SM, Davies M (2001) Electrically active axons degenerate when exposed to nitric oxide. Ann Neurol 49:470-476.
136. Smith KJ, McDonald I, Miller D, Lassmann H (2006) The pathophysiology of multiple sclerosis. In: McAlpine's Multiple Sclerosis. A Compston, C Confavreux, H Lassmann, I McDonald, D Miller, J Noseworthy, K Smith, H Wekerle (eds), pp. 601-659. Churchill Livingstone: London.
137. Stys PK (1998) Anoxic and ischemic injury of myelinated axons in CNS white matter: from mechanistic concepts to therapeutics. J Cereb Blood Flow Metab 18:2-25.
138. Stys PK, Sontheimer H, Ransom BR, Waxman SG (1993) Noninactivating, tetrodotoxin-sensitive Na+ conductance in rat optic nerve axons. Proc Natl Acad Sci USA 90:6976-6980.
139. Sumner AJ, Saida K, Saida T, Silberberg DH, Asbury AK (1982) Acute conduction block associated with experimental antiserum-mediated demyelination of peripheral nerve. Ann Neurol 11:469-477.
140. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L (1998) Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338:278-285.
141. Ulrich J, Groebke-Lorenz W (1983) The optic nerve in multiple sclerosis: a morphological study with retrospective clinico-pathological correlations. Neuro-Ophthalmology 3:149-159.
142. Utzschneider DA, Archer DR, Kocsis JD, Waxman SG, Duncan ID (1994) Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelin-deficient rat. Proc Natl Acad Sci USA 91:53-57.
143. Waxman SG (1977) Conduction in myelinated, unmyelinated, and demyelinated fibers. Arch Neurol 34:585-589.
144. Waxman SG (1981) Clinicopathological correlations in multiple sclerosis and related diseases. Adv Neurol 31:169-182.
145. Waxman SG (1989) Demyelination in spinal cord injury. J Neurol Sci 91:1-14.
146. Waxman SG (1995) Sodium channel blockade by antibodies: a new mechanism of neurological disease? Ann Neurol 37:421-423.
147. Waxman SG (2000) Do "demyelinating" diseases involve more than myelin? Nat Med 6:738-739.
148. Waxman SG (2005) Cerebellar dysfunction in multiple sclerosis: evidence for an acquired channelopathy. Prog Brain Res 148:353-365.
149. Waxman SG, Ritchie JM (1993) Molecular dissection of the myelinated axon. Ann Neurol 33:121-136.
150. Waxman SG, Black JA, Kocsis JD, Ritchie JM (1989) Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc Natl Acad Sci USA 86:1406-1410.
151. Weber F, Rudel R, Aulkemeyer P, Brinkmeier H (2002) The endogenous pentapeptide QYNAD induces acute conduction block in the isolated rat sciatic nerve. Neurosci Lett 317:33-36.
152. Wing MG, Moreau T, Greenwood J, Smith RM, Hale G, Isaacs J, Lachmann PJ, Compston A (1996) Mechanism of first-dose cytokine-release syndrome by CAMPATH 1-H: involvement of CD16 (FcgammaRIII) and CD11a/CD18 (LFA-1) on NK cells. J Clin Invest 98:2819-2826.
153. Wolswijk G, Balesar R (2003) Changes in the expression and localization of the paranodal protein Caspr on axons in chronic multiple sclerosis. Brain 126:1638-1649.
154. Yarom Y, Naparstek Y, Lev-Ram V, Holoshitz J, Ben-Nun A, Cohen IR (1983) Immunospecific inhibition of nerve conduction by T lymphocytes reactive to basic protein of myelin. Nature 303:246-247.
155. Youl BD, Turano G, Miller DH, Towell AD, Macmanus DG, Moore SG, Barrett G, Kendall BE, Moseley IF, Tofts PS, Halliday AM, McDonald WI (1991) The pathophysiology of acute optic neuritis. An association of gadolinium leakage with clinical and electrophysiological deficits. Brain 114:2437-2450.
156. Zhou ZH, Bubien JK (2002) ENaC plays a role in regulated antibody secretion by hybridomas. Am J Physiol Cell Physiol 283:C1480-C1491.