Axonal loss results in spinal cord atrophy, electrophysiological abnormalities and neurological deficits following demyelination in a chronic inflammatory model of multiple sclerosis

Brain

Volumn 123, Issue 3, 2000, Pages 519-531

  McGavern, Dorian B ^a   Murray, Paul D ^a   Rivera Quiñones, Cynthia ^a   Schmelzer, James D ^a   Low, Phillip A ^a   Rodriguez, Moses ^a  

^a MAYO CLINIC   (United States)

Author keywords

Conduction; Inflammation; Neuropathology; Rotarod; Theiler's virus

Indexed keywords

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LOSS; CONTROLLED STUDY; COORDINATION; DEMYELINATION; DISEASE COURSE; DISEASE SEVERITY; ELECTROPHYSIOLOGY; EVOKED MUSCLE RESPONSE; MOUSE; MULTIPLE SCLEROSIS; MYELINATED NERVE; NERVE FIBER; NEUROLOGY; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROPRIOCEPTION; SPINAL CORD ATROPHY;

EID: 0033975629     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/123.3.519     Document Type: Article

References (45)

1. Adams RD, Victor M, Ropper AH. Multiple sclerosis and allied demyelinative diseases. In: Adams RD, Victor M, Ropper AH. Principles of neurology. 6th edn. New York: McGraw-Hill; 1997. p. 902-27.
2. Blight AR. Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line-sampling. Neuroscience 1983; 10: 521-43.
3. Blight AR, Decrescito V. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 1986; 19: 321-41.
4. Charcot JM. Histologie de la sclerose en plaques. Gaz Hop (Paris) 1868; 41: 554-5, 557-8; 566.
5. Dal Canto MC, Lipton HL. Multiple sclerosis. Animal model: Theiler's virus infection in mice. Am J Pathol 1977; 88: 497-500.
6. Dal Canto MC, Lipton HL. Recurrent demyelination in chronic central nervous system infection produced by Theiler's murine encephalomyelitis virus. J Neurol Sci 1979; 42: 391-405.
7. Dal Canto MC, Lipton HL. Ultrastructural immunohistochemical localization of virus in acute and chronic demyelinating Theiler's virus infection. Am J Pathol 1982; 106: 20-9.
8. Davie CA, Barker GJ, Webb S, Tofts PS, Thompson AJ, Harding AE, et al. Persistent functional deficit in multiple sclerosis and autosomal dominant cerebellar ataxia is associated with axon loss. Brain 1995; 118: 1583-92.
9. 1H magnetic resonance spectroscopy of chronic cerebral white matter lesions and normal appearing white matter in multiple sclerosis. J Neurol Neurosurg Psychiatry 1997; 63: 736-42.
10. De Stefano N, Matthews PM, Fu L, Narayanan S, Stanley J, Francis GS, et al. Axonal damage correlates with disability in patients with relapsing-remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study. Brain 1998; 121: 1469-77.
11. De Stefano N, Matthews PM, Narayanan S, Francis GS, Antel JP, Arnold DL. Axonal dysfunction and disability in a relapse of multiple sclerosis: longitudinal study of a patient. Neurology 1997; 49: 1138-41.
12. Fehlings MG, Tator CH. The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp Neurol 1995; 132: 220-8.
13. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997; 120: 393-9.
14. Filippi M, Paty DW, Kappos L, Barkhof F, Compston DA, Thompson AJ, et al. Correlations between changes in disability and T2-weighted brain MRI activity in multiple sclerosis: a follow-up study. Neurology 1995; 45: 255-60.
15. Filippi M, Campi A, Colombo B, Pereira C, Martinelli V, Baratti C, et al. A spinal cord MRI study of benign and secondary progressive multiple sclerosis. J Neurol 1996; 243: 502-5.
16. Fu L, Matthews PM, De Stefano N, Worsley KJ, Narayanan S, Francis GS, et al. Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 1998; 121: 103-13.
17. Griffiths IR, Klugmann M, Anderson T, Yool D, Thomson S, Schwab MH, et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 1998; 280: 1610-3.
18. Iuliano BA, Schmelzer JD, Thiemann RL, Low PA, Rodriguez M. Motor and somatosensory evoked potentials in mice infected with Theiler's murine encephalomyelitis virus. J Neurol Sci 1994; 123: 186-94.
19. Kidd D, Thorpe JW, Thompson AJ, Kendall BE, Moseley IF, MacManus DG, et al. Spinal cord MRI using multi-array coils and fast spin echo. II. Findings in multiple sclerosis. Neurology 1993; 43: 2632-7.
20. Kidd D, Thorpe JW, Kendall BE, Barker GJ, Miller DH, McDonald WI, et al. MRI dynamics of brain and spinal cord in progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 1996; 60: 15-9.
21. Klugmann M, Schwab MH, Puhlhofer A, Schneider A, Zimmermann F, Griffiths IR, et al. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 1997; 18: 59-70.
22. Kuhn PL, Petroulakis E, Zazanis GA, McKinnon RD. Motor function analysis of myelin mutant mice using a rotarod. Int J Dev Neurosci 1995; 13: 715-22.
23. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status score (EDSS). Neurology 1983; 33: 1444-52.
24. Lehrich JR, Amason BG, Hochberg FH. Demyelinative myelopathy in mice induced by the DA virus. J Neurol Sci 1976; 29: 149-60.
25. Lipton HL. Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect Immun 1975; 11: 1147-55.
26. Lipton HL, Dal Canto MC. Chronic neurologic disease in Theiler's virus infection of SJL/J mice. J Neurol Sci 1976a; 30: 201-7.
27. Lipton HL, Dal Canto MC. Theiler's virus-induced demyelination: prevention by immunosuppression. Science 1976b; 192: 62-4.
28. Losseff NA, Webb SL, O'Riordan JI, Page R, Wang L, Barker GJ, et al. Spinal cord atrophy and disability in multiple sclerosis. Brain 1996; 119: 701-8.
29. Lycklama a Nijeholt GJ, van Walderveen MA, Castelijns JA, van Waesberghe JH, Polman C, Scheltens P, et al. Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. Brain 1998; 121: 687-97.
30. McDonald WI, Sears TA. The effects of experimental demyelination on conduction in the central nervous system. Brain 1970; 93: 583-98.
31. McGavern DB, Murray PD, Rodriguez M. Quantitation of spinal cord demyelination, remyelination, atrophy, and axonal loss in a model of progressive neurologic injury. J Neurosci Res 1999a. In press.
32. McGavern DB, Zoecklein L, Drescher KM, Rodriguez M. Quantitative assessment of neurologic deficits in a chronic progressive murine model of CNS demyelination. Exp Neurol 1999b; 158: 171-81.
33. Narayanan S, Fu L, Pioro E, De Stefano N, Collins DL, Francis GS, et al. Imaging of axonal damage in multiple sclerosis: spatial distribution of magnetic resonance imaging lesions. Ann Neurol 1997; 41: 385-91.
34. Oppenheimer DR. The cervical cord in multiple sclerosis. Neuropathol Appl Neurobiol 1978; 4: 151-62.
35. Paya CV, Leibson PJ, Patick AK, Rodriguez M. Inhibition of Theiler's virus-induced demyelination in vivo by tumor necrosis factor alpha. Im Immunol 1990; 2: 909-13.
36. Riahi F, Zijdenbos A, Narayanan S, Arnold D, Francis G, Antel J, et al. Improved correlation between scores on the expanded disability status scale and cerebral lesion load in relapsing-remitting multiple sclerosis. Brain 1998; 121: 1305-12.
37. Rivera-Quiñones C, McGavern D, Schmelzer JD, Hunter SF, Low PA, Rodriguez M. Absence of neurological deficits following extensive demyelination in a class I-deficient murine model of multiple sclerosis. Nature Med 1998; 4: 187-93.
38. Rodriguez M, David CS. Demyelination induced by Theiler's virus: influence of the H-2 haplotype. J Immunol 1985; 135: 2145-8.
39. Rodriguez M, Leibowitz JL, Lampert PW. Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann Neurol 1983; 13: 426-33.
40. Rodriguez M, Oleszak E, Leibowitz J. Theiler's murine encephalomyelitis: a model of demyelination and persistence of virus. [Review]. Crit Rev Immunol 1987; 7: 325-65.
41. Rosenberg LJ, Wrathall JR. Quantitative analysis of acute axonal pathology in experimental spinal cord contusion. J Neurotrauma 1997; 14: 823-38.
42. Rozas G, Labandeira Garcia JL. Drug-free evaluation of rat models of parkinsonism and nigral grafts using a new automated rotarod test. Brain Res 1997; 749: 188-99.
43. Stevenson VL, Leary SM, Losseff NA, Parker GJ, Barker GJ, Husmani, Y, et al. Spinal cord atrophy and disability in MS. A longitudinal study. Neurology 1998; 51: 234-8.
44. 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: 278-85.
45. Urenjak J, Williams SR, Gadian DG, Noble M. Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci 1993; 13: 981-9.