Insights into the molecular pathogenesis of progression in multiple sclerosis: Potential implications for future therapies

Archives of Neurology

Volumn 63, Issue 1, 2006, Pages 25-33

  Imitola, Jaime ^a   Chitnis, Tanuja ^a   Khoury, Samia J ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HIM R710 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASTROCYTE; CONFERENCE PAPER; DEMYELINATION; DISEASE COURSE; EFFECTOR CELL; EVIDENCE BASED MEDICINE; GENE EXPRESSION; HUMAN; MICROENVIRONMENT; MICROGLIA; MOLECULAR DYNAMICS; MULTIPLE SCLEROSIS; NERVE FIBER REGENERATION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL;

BRAIN; CHRONIC DISEASE; DEMYELINATING DISEASES; DISEASE PROGRESSION; HUMANS; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVOUS SYSTEM; NEUROLOGY; TIME FACTORS;

EID: 30344437563     PISSN: 00039942     EISSN: 15383687     Source Type: Journal    
DOI: 10.1001/archneur.63.1.25     Document Type: Conference Paper

References (84)

1. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med. 2000;343:938-952.
2. Weiner HL. Multiple sclerosis is an inflammatory T-cell-mediated autoimmune disease. Arch Neurol. 2004;61:1613-1615.
3. Wolswijk G. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain. 2002;125:338-349.
4. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES. Multiple sclerosis: remyelination of nascent lesions. Ann Neurol. 1993;33:137-151.
5. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci. 2000;20:6404-6412.
6. Traboulsee A, Dehmeshki J, Peters KR, et al. Disability in multiple sclerosis is related to normal appearing brain tissue MTR histogram abnormalities. Mult Scler. 2003;9:566-573.
7. Oh J, Henry RG, Genain C, Nelson SJ, Pelletier D. Mechanisms of normal appearing corpus callosum injury related to pericallosal T1 lesions in multiple sclerosis using directional diffusion tensor and 1H MRS imaging. J Neurol Neurosurg Psychiatry. 2004;75:1281-1286.
8. 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;47:707-717.
9. Baranzini SE, Mousavi P, Rio J, et al. Transcriptionbased prediction of response to IFNbeta using supervised computational methods. PLoS Biol. 2005;3:e2.
10. Frohman EM, Filippi M, Stuve O, et al. Characterizing the mechanisms of progression in multiple sclerosis: evidence and new hypotheses for future directions. Arch Neurol. 2005;62:1345-1356.
11. Frohman EM, Stuve O, Havrdova E, et al. Therapeutic considerations for disease progression in multiple sclerosis: evidence, experience, and future expectations. Arch Neurol. 2005;62:1519-1530.
12. Zamvil SS, Steinman L. Diverse targets for intervention during inflammatory and neurodegenerative phases of multiple sclerosis. Neuron. 2003;38:685-688.
13. Wujek JR, Bjartmar C, Richer E, et al. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J Neuropathol Exp Neurol. 2002;61:23-32.
14. Werner P, Pitt D, Raine CS. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol. 2001;50:169-180.
15. Pitt D, Werner P, Raine CS. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med. 2000;6:67-70.
16. John GR, Shankar SL, Shafit-Zagardo B, et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med. 2002;8:1115-1121.
17. Stidworthy MF, Genoud S, Li WW, et al. Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain. 2004;127:1928-1941.
18. Antony JM, van Marle G, Opii W, et al. Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat Neurosci. 2004;7:1088-1095.
19. Heppner FL, Greter M, Marino D, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med. 2005;11:146-152.
20. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol. 2001;50:389-400.
21. Giuliani F, Goodyer CG, Antel JP, Yong VW. Vulnerability of human neurons to T cell-mediated cytotoxicity. J Immunol. 2003;171:368-379.
22. Ge Y, Law M, Johnson G, et al. Preferential occult injury of corpus callosum in multiple sclerosis measured by diffusion tensor imaging. J Magn Reson Imaging. 2004;20:1-7.
23. Lindberg RL, De Groot CJ, Certa U, et al. Multiple sclerosis as a generalized CNS disease: comparative microarray analysis of normal appearing white matter and lesions in secondary progressive MS. J Neuroimmunol. 2004;152:154-167.
24. Whitney LW, Becker KG, Tresser NJ, et al. Analysis of gene expression in multiple sclerosis lesions using cDNA microarrays. Ann Neurol. 1999;46:425-428.
25. Black JA, Dib-Hajj S, Baker D, Newcombe J, Cuzner ML, Waxman SG. Sensory neuron-specific sodium channel SNS is abnormally expressed in the brains of mice with experimental allergic encephalomyelitis and humans with multiple sclerosis. Proc Natl Acad Sci U S A. 2000;97:11598-11602.
26. Kornek B, Storch MK, 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. 2000;157:267-276.
27. Graumann U, Reynolds R, Steck AJ, Schaeren-Wiemers N. Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult. Brain Pathol. 2003;13:554-573.
28. Filippi M, Bozzali M, Rovaris M, et al. Evidence for widespread axonal damage at the earliest clinical stage of multiple sclerosis. Brain. 2003;126:433-437.
29. Ge Y, Gonen O, Inglese M, Babb JS, Markowitz CE, Grossman RI. Neuronal cell injury precedes brain atrophy in multiple sclerosis. Neurology. 2004;62:624-627.
30. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain. 1997;120:393-399.
31. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med. 1998;338:278-285.
32. Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. Acute axonal injury in multiple sclerosis: correlation with demyelination and inflammation. Brain. 2000;123:1174-1183.
33. Ganter P, Prince C, Esiri MM. Spinal cord axonal loss in multiple sclerosis: a post-mortem study. Neuropathol Appl Neurobiol. 1999;25:459-467.
34. Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM. Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain. 2000;123:1845-1849.
35. Brady ST, Witt AS, Kirkpatrick LL, et al. Formation of compact myelin is required for maturation of the axonal cytoskeleton. J Neurosci. 1999;19:7278-7288.
36. Redford EJ, Kapoor R, Smith KJ. Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain. 1997;120:2149-2157.
37. Garbern JY, Yool DA, Moore GJ, et al. Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain. 2002;125:551-561.
38. Yin X, Crawford TO, Griffin JW, et al. Myelinassociated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci. 1998;18:1953-1962.
39. Mead RJ, Singhrao SK, Neal JW, Lassmann H, Morgan BP. The membrane attack complex of complement causes severe demyelination associated with acute axonal injury. J Immunol. 2002;168:458-465.
40. Linington C, Morgan BP, Scolding NJ, Wilkins P, Piddlesden S, Compston DA. The role of complement in the pathogenesis of experimental allergic encephalomyelitis. Brain. 1989;112:895-911.
41. Chavany C, Vicario-Abejon C, Miller G, Jendoubi M. Transgenic mice for interleukin 3 develop motor neuron degeneration associated with autoimmune reaction against spinal cord motor neurons. Proc Natl Acad Sci U S A. 1998;95:11354-11359.
42. Campbell IL, Abraham CR, Masliah E, et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A. 1993;90:10061-10065.
43. Alcazar A, Regidor I, Masjuan J, Salinas M, Alvarez-Cermeno JC. Axonal damage induced by cerebrospinal fluid from patients with relapsing-remitting multiple sclerosis. J Neuroimmunol. 2000;104:58-67.
44. Brewer KL, Bethea JR, Yezierski RP. Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp Neurol. 1999;159:484-493.
45. Beattie EC, Stellwagen D, Morishita W, et al. Control of synaptic strength by glial TNFalpha. Science. 2002;295:2282-2285.
46. Ibrahim SM, Mix E, Bottcher T, et al. Gene expression profiling of the nervous system in murine experimental autoimmune encephalomyelitis. Brain. 2001;124:1927-1938.
47. Lu T, Pan Y, Kao SY, et al. Gene regulation and DNA damage in the ageing human brain. Nature. 2004;429:883-891.
48. Andrews T, Zhang P, Bhat NR. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res. 1998;54:574-583.
49. Lenercept Multiple Sclerosis Study Group and University of British Columbia MS/MRI Analysis Group. TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. Neurology. 1999;53:457-465.
50. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci. 2001;4:1116-1122.
51. Brosnan CF, Battistini L, Raine CS, Dickson DW, Casadevall A, Lee SC. Reactive nitrogen intermediates in human neuropathology: an overview. Dev Neurosci. 1994;16:152-161.
52. Vladimirova O, O'Connor J, Cahill A, Alder H, Butunoi C, Kalman B. Oxidative damage to DNA inplaques of MS brains. Mult Scler. 1998;4:413-418.
53. Lu F, Selak M, O'Connor J, et al. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J Neurol Sci. 2000;177:95-103.
54. Smith KJ, Kapoor R, Hall SM, Davies M. Electrically active axons degenerate when exposed to nitric oxide. Ann Neurol. 2001;49:470-476.
55. Lock C, Hermans G, Pedotti R, et al. Genemicroarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med. 2002;8:500-508.
56. Kalkers NF, Barkhof F, Bergers E, van Schijndel R, Polman CH. The effect of the neuroprotective agent riluzole on MRI parameters in primary progressive multiple sclerosis: a pilot study. Mult Scler. 2002;8:532-533.
57. Steinman L. Multiple sclerosis: a two-stage disease. Nat Immunol. 2001;2:762-764.
58. Simmons ML, Frondoza CG, Coyle JT. Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience. 1991;45:37-45.
59. De Stefano N, Narayanan S, Francis GS, et al. Evidence of axonal damage in the early stages of multiple sclerosis and its relevance to disability. Arch Neurol. 2001;58:65-70.
60. Li LM, Cendes F, Andermann F, Dubeau F, Arnold DL. Spatial extent of neuronal metabolic dysfunction measured by proton MR spectroscopic imaging in patients with localization-related epilepsy. Epilepsia. 2000;41:666-674.
61. De Stefano N, Narayanan S, Matthews PM, Francis GS, Antel JP, Arnold DL. In vivo evidence for axonal dysfunction remote from focal cerebral demyelination of the type seen in multiple sclerosis. Brain. 1999;122:1933-1939.
62. Lassmann H. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci. 2003;206:187-191.
63. Sim FJ, Zhao C, Penderis J, Franklin RJ. The agerelated decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci. 2002;22:2451-2459.
64. Confavreux C, Vukusic S, Moreau T, Adeleine P. Relapses and progression of disability in multiple sclerosis. N Engl J Med. 2000;343:1430-1438.
65. Liguori M, Marrosu MG, Pugliatti M, et al. Age at onset in multiple sclerosis. Neurol Sci. 2000;21(suppl 2):S825-S829.
66. Enzinger C, Ropele S, Smith S, et al. Accelerated evolution of brain atrophy and "black holes" in MS patients with APOE-epsilon 4. Ann Neurol. 2004;55:563-569.
67. Nishie M, Mori F, Ogawa M, et al. Multinucleated astrocytes in old demyelinated plaques in a patient with multiple sclerosis. Neuropathology. 2004;24:248-253.
68. Clarke G, Collins RA, Leavitt BR, et al. A one-hit model of cell death in inherited neuronal degenerations. Nature. 2000;406:195-199.
69. D'Intino G, Paradisi M, Fernandez M, et al. Cognitive deficit associated with cholinergic and nerve growth factor down-regulation in experimental allergic encephalomyelitis in rats. Proc Natl Acad Sci U S A. 2005;102:3070-3075.
70. Linker RA, Maurer M, Gaupp S, et al. CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat Med. 2002;8:620-624.
71. Maier K, Rau CR, Storch MK, et al. Ciliary neurotrophic factor protects retinal ganglion cells from secondary cell death during acute autoimmune optic neuritis in rats. Brain Pathol. 2004;14:378-387.
72. Butzkueven H, Zhang JG, Soilu-Hanninen M, et al. LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat Med. 2002;8:613-619.
73. Imitola J, Snyder EY, Khoury SJ. Genetic programs and responses of neural stem/progenitor cells during demyelination: potential insights into repair mechanisms in multiple sclerosis. Physiol Genomics. 2003;14:171-197.
74. Cannella B, Hoban CJ, Gao YL, et al. The neuregulin, glial growth factor 2, diminishes autoimmune demyelination and enhances remyelination in a chronic relapsing model for multiple sclerosis. Proc Natl Acad Sci U S A. 1998;95:10100-10105.
75. Calza L, Fernandez M, Giuliani A, Aloe L, Giardino L. Thyroid hormone activates oligodendrocyte precursors and increases a myelin-forming protein and NGF content in the spinal cord during experimental allergic encephalomyelitis. Proc Natl Acad Sci U S A. 2002;99:3258-3263.
76. Stolt CC, Rehberg S, Ader M, et al. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 2002;16:165-170.
77. Fancy SP, Zhao C, Franklin RJ. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci. 2004;27:247-254.
78. Arnett HA, Fancy SP, Alberta JA, et al. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science. 2004;306:2111-2115.
79. GrandPre T, Nakamura F, Vartanian T, Strittmatter SM. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature. 2000;403:439-444.
80. Yamashita T, Tucker KL, Barde YA. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron. 1999;24:585-593.
81. Karnezis T, Mandemakers W, McQualter JL, et al. The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyelination. Nat Neurosci. 2004;7:736-744.
82. Fontoura P, Ho PP, DeVoss J, et al. Immunity to the extracellular domain of Nogo-A modulates experimental autoimmune encephalomyelitis. J Immunol. 2004;173:6981-6992.
83. Sivasankaran R, Pei J, Wang KC, et al. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci. 2004;7:261-268.
84. Kutzelnigg A, Lucchinetti CF, Stadelmann C, et al. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain. 2005;128:2705-2712.