Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis

The Lancet Neurology

Volumn 8, Issue 3, 2009, Pages 280-291

  Trapp, Bruce D ^a   Stys, Peter K ^b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; CALPAIN; CALPASTATIN; CARBAMAZEPINE; FLECAINIDE; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR ANTAGONIST; IONOTROPIC RECEPTOR; LAMOTRIGINE; MEMANTINE; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PHENYTOIN; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CHANNEL BLOCKING AGENT; VOLTAGE GATED SODIUM CHANNEL;

ALLERGIC ENCEPHALITIS; ALLERGIC ENCEPHALOMYELITIS; AXONAL INJURY; AXOPLASM; CALCIUM TRANSPORT; CELL DEATH; CELL ENERGY; CELL HYPOXIA; CLINICAL TRIAL; CYTOPATHOLOGY; DEMYELINATION; DISABILITY; DISEASE ACTIVITY; DRUG WITHDRAWAL; ENERGY CONSUMPTION; ENERGY YIELD; EXCITOTOXICITY; HUMAN; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MITOCHONDRION; MULTIPLE SCLEROSIS; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE CONDUCTION; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RECEPTOR BLOCKING; REMYELINIZATION; REVIEW; SODIUM CALCIUM EXCHANGE; SODIUM TRANSPORT;

ANOXIA; AXONS; HUMANS; MODELS, BIOLOGICAL; MULTIPLE SCLEROSIS; NECROSIS; NEURAL CONDUCTION;

EID: 59949106172     PISSN: 14744422     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1474-4422(09)70043-2     Document Type: Review

References (109)

1. Noseworthy J.H., Lucchinetti C., Rodriguez M., and Weinshenker B.G. Multiple sclerosis. N Engl J Med 343 (2000) 938-952
2. Weinshenker B.G. Epidemiology of multiple sclerosis. Neurol Clin 14 (1996) 291-308
3. Waxman S.G. Multiple sclerosis as a neuronal disease (2005), Elsevier Academic Press, Burlington, MA
4. Trapp B.D., and Nave K.-A. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci 31 (2008) 247-269
5. Peru R.L., Mandrycky N., Nait-Oumesmar B., and Lu Q.R. Paving the axonal highway: from stem cells to myelin repair. Stem Cell Rev 4 (2008) 304-318
6. Kornek B., and Lassmann H. Axonal pathology in multiple sclerosis. A historical note. Brain Pathol 9 (1999) 651-656
7. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., and Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338 (1998) 278-285
8. Ganter P., Prince C., and Esiri M.M. Spinal cord axonal loss in multiple sclerosis: a post-mortem study. Neuropathol Appl Neurobiol 25 (1999) 459-467
9. Lovas G., Szilagyi N., Majtenyi K., Palkovits M., and Komoly S. Axonal changes in chronic demyelinated cervical spinal cord plaques. Brain 123 (2000) 308-317
10. Bjartmar C., Kinkel R.P., Kidd G., Rudick R.A., and Trapp B.D. Axonal loss in normal-appearing white matter in a patient with acute MS. Neurology 57 (2001) 1248-1252
11. Rudick R.A., Fisher E., Lee J.C., Simon J., and Jacobs L. Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 53 (1999) 1698-1704
12. Simon J.H., Jacobs L.D., Campion M.K., et al. A longitudinal study of brain atrophy in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Neurology 53 (1999) 139-148
13. Arnold D.L., Riess G.T., Matthews P.M., et al. Use of proton magnetic resonance spectroscopy for monitoring disease progression in multiple sclerosis. Ann Neurol 36 (1994) 76-82
14. Matthews P.M., Pioro E., Narayanan S., et al. Assessment of lesion pathology in multiple sclerosis using quantitative MRI morphometry and magnetic resonance spectroscopy. Brain 119 (1996) 715-722
15. Bjartmar C., Kidd G., Mork S., Rudick R., and Trapp B.D. Neurological disability correlates with spinal cord axonal loss and reduce N-acetyl aspartate in chronic multiple sclerosis patients. Ann Neurol 48 (2000) 893-901
16. Griffiths I., Klugmann M., Anderson T., et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280 (1998) 1610-1613
17. Lappe-Siefke C., Goebbels S., Gravel M., et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33 (2003) 366-374
18. Yin X., Crawford T.O., Griffin J.W., et al. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18 (1998) 1953-1962
19. Trapp B.D., Ransohoff R., and Rudick R. Axonal pathology in multiple sclerosis: relationship to neurologic disability. Curr Opin Neurol 12 (1999) 295-302
20. Trapp B.D., Ransohoff R.M., Fisher E., and Rudick R.A. Neurodegeneration in multiple sclerosis: relationship to neurological disability. Neuroscientist 5 (1999) 48-57
21. Bjartmar C., Yin X., and Trapp B.D. Axonal pathology in myelin disorders. J Neurocytol 28 (1999) 383-395
22. Reddy H., Narayanan S., Arnoutelis R., et al. Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 123 (2000) 2314-2320
23. Rocca M.A., Mezzapesa D.M., Falini A., et al. Evidence for axonal pathology and adaptive cortical reorganization in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage 18 (2003) 847-855
24. Pantano P., Iannetti G.D., Caramia F., et al. Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 125 (2002) 1607-1615
25. Parry A.M., Scott R.B., Palace J., Smith S., and Matthews P.M. Potentially adaptive functional changes in cognitive processing for patients with multiple sclerosis and their acute modulation by rivastigmine. Brain 126 (2003) 2750-2760
26. Nave K.-A., and Trapp B.D. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31 (2008) 535-561
27. Kornek B., Storch M.K., Weissert R., et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 157 (2000) 267-276
28. Smith K.J., and Lassmann H. The role of nitric oxide in multiple sclerosis. Lancet Neurol 1 (2002) 232-241
29. Bechtold D.A., and Smith K.J. Sodium-mediated axonal degeneration in inflammatory demyelinating disease. J Neurol Sci 233 (2005) 27-35
30. Dutta R., McDonough J., Yin X., et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59 (2006) 478-489
31. Mahad D., Ziabreva I., Lassmann H., and Turnbull D. Mitochondrial defects in acute multiple sclerosis lesions. Brain 131 (2008) 1722-1735
32. 2+ exchanger. Proc Natl Acad Sci USA 101 (2004) 8168-8173
33. Stys P.K. Axonal degeneration in multiple sclerosis: is it time for neuroprotective strategies?. Ann Neurol 55 (2004) 601-603
34. Ouardouz M, Coderre E, Basak A, et al. Glutamate receptors on myelinated spinal cord axons: I) GluR6 kainate receptors. Ann Neurol (in press).
35. Ouardouz M, Coderre E, Zamponi GW, et al. Glutamate receptors on myelinated spinal cord axons: II) AMPA and GluR5 receptors. Ann Neurol (in press).
36. + ATPase in chronic MS lesions. Ann Neurol 63 (2008) 428-435
37. Black J.A., Newcombe J., Trapp B.D., and Waxman S.G. Sodium channel expression within chronic multiple sclerosis plaques. J Neuropathol Exp Neurol 66 (2007) 828-837
38. Stys P.K., Lehning E., Saubermann A.J., and Lopachin Jr. R.M. Intracellular concentrations of major ions in rat myelinated axons and glia: calculations based on electron probe X-ray microanalyses. J Neurochem 68 (1997) 1920-1928
39. 2+ channel activation of ryanodine receptors. Neuron 40 (2003) 53-63
40. Fern R., Ransom B.R., and Waxman S.G. Voltage-gated calcium channels in CNS white matter: role in anoxic injury. J Neurophysiol 74 (1995) 369-377
41. 2+ stores during ischaemia in rat spinal cord white matter. J Physiol 577 (2006) 191-204
42. Ferguson B., Matyszak M.K., Esiri M.M., and Perry V.H. Axonal damage in acute multiple sclerosis lesions. Brain 120 (1997) 393-399
43. Sanchez I., Hassinger L., Paskevich P.A., Shine H.D., and Nixon R.A. Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J Neurosci 16 (1996) 5095-5105
44. Strack S., Westphal R.S., Colbran R.J., Ebner F.F., and Wadzinski B.E. Protein serine/threonine phosphatase 1 and 2A associate with and dephosphorylate neurofilaments. Brain Res Mol Brain Res 49 (1997) 15-28
45. Kornek B., Storch M.K., Bauer J., et al. Distribution of a calcium channel subunit in dystrophic axons in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 124 (2001) 1114-1124
46. Bitsch A., Schuchardt J., Bunkowski S., Kuhlmann T., and Bruck W. Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 123 (2000) 1174-1183
47. Stys P.K., and Jiang Q. Calpain-dependent neurofilament breakdown in anoxic and ischemic rat central axons. Neurosci Lett 328 (2002) 150-154
48. Shields D.C., Schaecher K.E., Saido T.C., and Banik N.L. A putative mechanism of demyelination in multiple sclerosis by a proteolytic enzyme, calpain. Proc Natl Acad Sci USA 96 (1999) 11486-11491
49. Povlishock J.T., and Christman C.W. The pathobiology of traumatically induced axonal injury in animals and humans: a review of current thoughts. J Neurotrauma 12 (1995) 555-564
50. Yam P.S., Dewar D., and McCulloch J. Axonal injury caused by focal cerebral ischemia in the rat. J Neurotrauma 15 (1998) 441-450
51. Smith K.J. Sodium channels and multiple sclerosis: roles in symptom production, damage and therapy. Brain Pathol 17 (2007) 230-242
52. + conductance in rat optic nerve axons. Proc Natl Acad Sci USA 90 (1993) 6976-6980
53. + currents that fail to inactivate. Trends Neurosci 16 (1993) 455-460
54. Bo L., Dawson T.M., Wesselingh S., et al. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36 (1994) 778-786
55. Pacher P., Beckman J.S., and Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87 (2007) 315-424
56. Redford E.J., Kapoor R., and Smith K.J. Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120 (1997) 2149-2157
57. Smith K.J., Kapoor R., Hall S.M., and Davies M. Electrically active axons degenerate when exposed to nitric oxide. Ann Neurol 49 (2001) 470-476
58. Kapoor R., Davies M., Blaker P.A., Hall S.M., and Smith K.J. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 53 (2003) 174-180
59. Waxman S.G. Ions, energy and axonal energy: towards a molecular neurology of multiple sclerosis. Trends Mol Med 12 (2006) 192-195
60. Lipton S.A., and Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330 (1994) 613-622
61. Matute C., Alberdi E., Domercq M., Perez-Cerda F., Perez-Samartin A., and Sanchez-Gomez M.V. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci 24 (2001) 224-230
62. Steinman L. Multiple sclerosis: a two-stage disease. Nat Immunol 2 (2001) 762-764
63. Lassmann H. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci 206 (2003) 187-191
64. Ye Z.C., Wyeth M.S., Baltan-Tekkok S., and Ransom B.R. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 23 (2003) 3588-3596
65. Parpura V., Scemes E., and Spray D.C. Mechanisms of glutamate release from astrocytes: gap junction "hemichannels", purinergic receptors and exocytotic release. Neurochem Int 45 (2004) 259-264
66. Ziskin J.L., Nishiyama A., Rubio M., Fukaya M., and Bergles D.E. Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10 (2007) 321-330
67. +-dependent glutamate transport. J Neurosci 19 (1999) RC16
68. Tekkök S.B., Ye Z., and Ransom B.R. Excitotoxic mechanisms of ischemic injury in myelinated white matter. J Cereb Blood Flow Metab 27 (2007) 1540-1552
69. Karadottir R., Cavelier P., Bergersen L.H., and Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438 (2005) 1162-1166
70. Salter M.G., and Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438 (2005) 1167-1171
71. Micu I., Jiang Q., Coderre E., et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439 (2006) 988-992
72. Srinivasan R., Sailasuta N., Hurd R., Nelson S., and Pelletier D. Evidence of elevated glutamate in multiple sclerosis using magnetic resonance spectroscopy at 3 T. Brain 128 (2005) 1016-1025
73. Srinivasan R., Cunningham C., Chen A., et al. TE-averaged two-dimensional proton spectroscopic imaging of glutamate at 3 T. Neuroimage 30 (2006) 1171-1178
74. Matute C., Domercq M., and Sanchez-Gomez M.V. Glutamate-mediated glial injury: mechanisms and clinical importance. Glia 53 (2006) 212-224
75. Wosik K., Ruffini F., Almazan G., Olivier A., Nalbantoglu J., and Antel J.P. Resistance of human adult oligodendrocytes to AMPA/kainate receptor-mediated glutamate injury. Brain 127 (2004) 2636-2648
76. Tekkok S.B., and Goldberg M.P. AMPA/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 21 (2001) 4237-4248
77. Li S., and Stys P.K. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 20 (2000) 1190-1198
78. Pitt D., Werner P., and Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6 (2000) 67-70
79. Smith T., Groom A., Zhu B., and Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6 (2000) 62-66
80. Groom A.J., Smith T., and Turski L. Multiple sclerosis and glutamate. Ann NY Acad Sci 993 (2003) 229-275
81. Chen H.S., and Lipton S.A. The chemical biology of clinically tolerated NMDA receptor antagonists. J Neurochem 97 (2006) 1611-1626
82. Wallstrom E., Diener P., Ljungdahl A., Khademi M., Nilsson C.G., and Olsson T. Memantine abrogates neurological deficits, but not CNS inflammation, in Lewis rat experimental autoimmune encephalomyelitis. J Neurol Sci 137 (1996) 89-96
83. Fisher E., Lee J.C., Nakamura K., and Rudick R.A. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol 64 (2008) 255-265
84. Fisniku L.K., Chard D.T., Jackson J.S., et al. Grey matter atrophy is related to long-term disability in multiple sclerosis. Ann Neurol 64 (2008) 247-254
85. Fisher E., Chang A., Fox R., et al. Imaging correlates of axonal swelling in chronic multiple sclerosis brains. Ann Neurol 62 (2007) 219-228
86. Lassmann H. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci 206 (2003) 187-191
87. Breij E.C., Brink B.P., Veerhuis R., et al. Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann Neurol 63 (2008) 16-25
88. Rieckmann P., and Maurer M. Anti-inflammatory strategies to prevent axonal injury in multiple sclerosis. Curr Opin Neurol 15 (2002) 361-370
89. Bartt R.E. Multiple sclerosis, natalizumab therapy, and progressive multifocal leukoencephalopathy. Curr Opin Neurol 19 (2006) 341-349
90. Schwartz M., Moalem G., Leibowitz-Amit R., and Cohen I.R. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22 (1999) 295-299
91. Antel J.P., and Bar-Or A. Multiple sclerosis: therapy. In: Lazzarini R. (Ed). Myelin biology and disorders (2004), Elsevier, Amsterdam 791-806
92. Coles A.J., Cox A., Le P.E., et al. The window of therapeutic opportunity in multiple sclerosis: evidence from monoclonal antibody therapy. J Neurol 253 (2006) 98-108
93. Metz I., Lucchinetti C.F., Openshaw H., et al. Autologous haematopoietic stem cell transplantation fails to stop demyelination and neurodegeneration in multiple sclerosis. Brain 130 (2007) 1254-1262
94. Smith M.R., Smith R.D., Plummer N.W., Meisler M.H., and Goldin A.L. Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18 (1998) 6093-6102
95. + channels. Proc Natl Acad Sci USA 93 (1996) 9270-9275
96. Stys P.K., Ransom B.R., and Waxman S.G. Tertiary and quaternary local anesthetics protect CNS white matter from anoxic injury at concentrations that do not block excitability. J Neurophysiol 67 (1992) 236-240
97. 2+ changes in CNS myelin using 2-photon microscopy. Nat Med 13 (2007) 874-879
98. + channel β2 subunits is neuroprotective in a mouse model of multiple sclerosis. Mol Cell Neurosci (2008) 10.1016/j.mcn.2008.10.001 published online Nov 1.
99. Bechtold D.A., Kapoor R., and Smith K.J. Axonal protection using flecainide in experimental autoimmune encephalomyelitis. Ann Neurol 55 (2004) 607-616
100. Lo A.C., Saab C.Y., Black J.A., and Waxman S.G. Phenytoin protects spinal cord axons and preserves axonal conduction and neurological function in a model of neuroinflammation in vivo. J Neurophysiol 90 (2003) 3566-3571
101. Black J.A., Liu S., Carrithers M., Carrithers L.M., and Waxman S.G. Exacerbation of experimental autoimmune encephalomyelitis after withdrawal of phenytoin and carbamazepine. Ann Neurol 62 (2007) 21-33
102. Bechtold D.A., Miller S.J., Dawson A.C., et al. Axonal protection achieved in a model of multiple sclerosis using lamotrigine. J Neurol 253 (2006) 1542-1551
103. Hardin-Pouzet H., Krakowski M., Bourbonniere L., Didier-Bazes M., Tran E., and Owens T. Glutamate metabolism is down-regulated in astrocytes during experimental allergic encephalomyelitis. Glia 20 (1997) 79-85
104. Werner P., Pitt D., and Raine C.S. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol 50 (2001) 169-180
105. Agrawal S.K., and Fehlings M.G. Role of NMDA and non-NMDA ionotropic glutamate receptors in traumatic spinal cord axonal injury. J Neurosci 17 (1997) 1055-1063
106. Wrathall J.R., Teng Y.D., and Marriott R. Delayed antagonism of AMPA/kainate receptors reduces long-term functional deficits resulting from spinal cord trauma. Exp Neurol 145 (1997) 565-573
107. Hassen G.W., Feliberti J., Kesner L., Stracher A., and Mokhtarian F. Prevention of axonal injury using calpain inhibitor in chronic progressive experimental autoimmune encephalomyelitis. Brain Res 1236 (2008) 206-215
108. Jiang Q., and Stys P.K. Calpain inhibitors confer biochemical, but not electrophysiological, protection against anoxia in rat optic nerves. J Neurochem 74 (2000) 2101-2107
109. Lehmann H.C., Lopez P.H., Zhang G., et al. Passive immunization with anti-ganglioside antibodies directly inhibits axon regeneration in an animal model. J Neurosci 27 (2007) 27-34