The relevance of animal models in multiple sclerosis research

Pathophysiology

Volumn 18, Issue 1, 2011, Pages 21-29

  Denic, Aleksandar ^a   Johnson, Aaron J ^b   Bieber, Allan J ^a   Warrington, Arthur E ^a   Rodriguez, Moses ^a,c   Pirko, Istvan ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

Cuprizone; Demyelination; EAE; Experimental autoimmune encephalomyelitis; Lyso phosphatidyl choline; Multiple sclerosis; Remyelination; Theiler's murine encephalomyelitis virus; TMEV; Toxic demyelination

Indexed keywords

BETA INTERFERON; CUPRIZONE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; GAMMA INTERFERON; GLATIRAMER; IMMUNOGLOBULIN; LYSOPHOSPHATIDYLCHOLINE; MINOCYCLINE; MITOXANTRONE; MYELIN; NATALIZUMAB; ROQUINIMEX; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ACUTE DISSEMINATED ENCEPHALOMYELITIS; ALLERGIC ENCEPHALOMYELITIS; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; DEMYELINATION; DISEASE MODEL; DRUG EFFICACY; EPSTEIN BARR VIRUS INFECTION; HUMAN; MEDICAL RESEARCH; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; MYELOOPTIC NEUROPATHY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

EID: 78650573911     PISSN: 09284680     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pathophys.2010.04.004     Document Type: Article

References (71)

1. Noseworthy J.H., Lucchinetti C., Rodriguez M., Weinshenker B.G. Multiple sclerosis. N. Engl. J. Med. 2000, 343:938-952.
2. 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.
3. Lucchinetti C.F., Parisi J., Bruck W. The pathology of multiple sclerosis. Neurol. Clin. 2005, 23:77-105. vi.
4. Baxter A.G. The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol. 2007, 7:904-912.
5. Rivers T., Sprunt D.H., Berry G.P. Observations on attempts to produce acute disseminated encephalomyelitis in monkeys. J. Exp. Med. 1933, 58:39-53.
6. Stuart G., Krikorian K. A fatal neuro-paralytic accident of antirabies treatment. Lancet 1930, 215:1123-1125.
7. Rivers T., Schwentker F.F. Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys. J. Exp. Med. 1935, 61:689-702.
8. Kabat E.A., Wolf A., Bezer A.E. Rapid production of acute disseminated encephalomyelitis in rhesus monkeys by injection of brain tissue with adjuvants. Science 1946, 104:362-363.
9. Wolf A., Kabat E., Bezer A. The pathology of acute disseminated encephalomyelitis produced experimentally in the rhesus monkey and its resemblance to human demyelinating disease. J. Neuropathol. Exp. Neurol. 1947, 6:333-357.
10. Pettinelli C.B., McFarlin D.E. Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1+ 2- T lymphocytes. J. Immunol. 1981, 127:1420-1423.
11. Bettelli E., Korn T., Oukka M., Kuchroo V.K. Induction and effector functions of T(H)17 cells. Nature 2008, 453:1051-1057.
12. Sun D., Whitaker J.N., Huang Z., Liu D., Coleclough C., Wekerle H., Raine C.S. Myelin antigen-specific CD8+ T cells are encephalitogenic and produce severe disease in C57BL/6 mice. J. Immunol. 2001, 166:7579-7587.
13. Huseby E.S., Liggitt D., Brabb T., Schnabel B., Ohlen C., Goverman J. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J. Exp. Med. 2001, 194:669-676.
14. Segal B.M. Experimental autoimmune encephalomyelitis: cytokines, effector T cells, and antigen-presenting cells in a prototypical Th1-mediated autoimmune disease. Curr. Allergy Asthma Rep. 2003, 3:86-93.
15. Steinman L., Zamvil S.S. How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis. Ann. Neurol. 2006, 60:12-21.
16. Sriram S., Steiner I. Experimental allergic encephalomyelitis: a misleading model of multiple sclerosis. Ann. Neurol. 2005, 58:939-945.
17. Nelson A.L., Bieber A.J., Rodriguez M. Contrasting murine models of MS. Int. MS J. 2004, 11:95-99.
18. Ure D.R., Rodriguez M. Polyreactive antibodies to glatiramer acetate promote myelin repair in murine model of demyelinating disease. FASEB J. 2002, 16:1260-1262.
19. Schwartz R., Datta S. Autoimmunity and autoimmune diseases. Fundamental Immunology 1989, 819-866. Raven Press, Ltd, New York. W.E. Paul (Ed.).
20. Wingerchuk D.M., Lennon V.A., Pittock S.J., Lucchinetti C.F., Weinshenker B.G. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006, 66:1485-1489.
21. Lassmann H., Ransohoff R.M. The CD4-Th1 model for multiple sclerosis: a critical [correction of crucial] re-appraisal. Trends Immunol. 2004, 25:132-137.
22. Neumann H., Medana I.M., Bauer J., Lassmann H. Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases. Trends Neurosci. 2002, 25:313-319.
23. Babbe H., Roers A., Waisman A., Lassmann H., Goebels N., Hohlfeld R., Friese M., Schroder R., Deckert M., Schmidt S., Ravid R., Rajewsky K. Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J. Exp. Med. 2000, 192:393-404.
24. Hauser S.L., Bhan A.K., Gilles F., Kemp M., Kerr C., Weiner H.L. Immunohistochemical analysis of the cellular infiltrate in multiple sclerosis lesions. Ann. Neurol. 1986, 19:578-587.
25. Kornek B., Storch M.K., Weissert R., Wallstroem E., Stefferl A., Olsson T., Linington C., Schmidbauer M., Lassmann H. 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.
26. Howe C.L., Rodriguez M. Remyelination as neuroprotection. Multiple Sclerosis as a Neuronal Disease 2005, 389-419. Elsevier Academic Press, San Diego. S.G. Waxman (Ed.).
27. Poser C.M. Pathogenesis of multiple sclerosis. A critical reappraisal. Acta Neuropathol. 1986, 71:1-10.
28. Dal Canto M.C., Lipton H.L. Multiple sclerosis. Animal model: Theiler's virus infection in mice. Am. J. Pathol. 1977, 88:497-500.
29. McFarlin D.E., McFarland H.F. Multiple sclerosis (first of two parts). N. Engl. J. Med. 1982, 307:1183-1188.
30. Kurtzke J.F. Epidemiologic contributions to multiple sclerosis: an overview. Neurology 1980, 30:61-79.
31. McFarlin D.E., McFarland H.F. Multiple sclerosis (second of two parts). N. Engl. J. Med. 1982, 307:1246-1251.
32. De Jager P.L., Simon K.C., Munger K.L., Rioux J.D., Hafler D.A., Ascherio A. Integrating risk factors: HLA- DRB1*1501 and Epstein-Barr virus in multiple sclerosis. Neurology 2008, 70:1113-1118.
33. Ascherio A., Munger K.L. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann. Neurol. 2007, 61:288-299.
34. Ascherio A., Munger K.L., Lennette E.T., Spiegelman D., Hernan M.A., Olek M.J., Hankinson S.E., Hunter D.J. Epstein-Barr virus antibodies and risk of multiple sclerosis: a prospective study. JAMA 2001, 286:3083-3088.
35. Theiler M. Spontaneous encephalomyelitis of mice-a new virus disease. Science 1934, 80:122.
36. Zoecklein L.J., Pavelko K.D., Gamez J., Papke L., McGavern D.B., Ure D.R., Njenga M.K., Johnson A.J., Nakane S., Rodriguez M. Direct comparison of demyelinating disease induced by the Daniel's strain and BeAn strain of Theiler's murine encephalomyelitis virus. Brain Pathol. 2003, 13:291-308.
37. Dal Canto M.C., Kim B.S., Miller S.D., Melvold R.W. Theiler's murine encephalomyelitis virus (TMEV)-induced demyelination: a model for human multiple sclerosis. Methods 1996, 10:453-461.
38. Lipton H.L. Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect Immun. 1975, 11:1147-1155.
39. Lipton H.L., Dal Canto M.C. The TO strains of Theiler's viruses cause "slow virus-like" infections in mice. Ann Neurol. 1979, 6:25-28.
40. Rodriguez M., Oleszak E., Leibowitz J. Theiler's murine encephalomyelitis: a model of demyelination and persistence of virus. Crit. Rev. Immunol. 1987, 7:325-365.
41. Katz-Levy Y., Neville K.L., Girvin A.M., Vanderlugt C.L., Pope J.G., Tan L.J., Miller S.D. Endogenous presentation of self myelin epitopes by CNS-resident APCs in Theiler's virus-infected mice. J. Clin. Investig. 1999, 104:599-610.
42. Miller S.D., Vanderlugt C.L., Begolka W.S., Pao W., Yauch R.L., Neville K.L., Katz-Levy Y., Carrizosa A., Kim B.S. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 1997, 3:1133-1136.
43. Bieber A.J.a.R. M. Experimental models of virus-induced demyelination. Myelin Biology and Disorders 2004, 1073-1100. Elsevier Academic Press, San Diego, CA. R.A. Lazzarini (Ed.).
44. Bieber A.J., Ure D.R., Rodriguez M. Genetically dominant spinal cord repair in a murine model of chronic progressive multiple sclerosis. J. Neuropathol. Exp. Neurol. 2005, 64:46-57.
45. Sibley W.A., Bamford C.R., Clark K. Clinical viral infections and multiple sclerosis. Lancet 1985, 1:1313-1315.
46. Sarchielli P., Trequattrini A., Usai F., Murasecco D., Gallai V. Role of viruses in the etiopathogenesis of multiple sclerosis. Acta Neurol. (Napoli) 1993, 15:363-381.
47. Rodriguez M., David C.S. Demyelination induced by Theiler's virus: influence of the H-2 haplotype. J. Immunol. 1985, 135:2145-2148.
48. Rodriguez M., Leibowitz J.L., Lampert P.W. Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann Neurol. 1983, 13:426-433.
49. Lipton H.L., Twaddle G., Jelachich M.L. The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Virol. 1995, 69:2525-2533.
50. Lipton H.L., Dal Canto M.C. Theiler's virus-induced demyelination: prevention by immunosuppression. Science 1976, 192:62-64.
51. McGavern D.B., Murray P.D., Rivera-Quinones C., Schmelzer J.D., Low P.A., Rodriguez M. Axonal loss results in spinal cord atrophy, electrophysiological abnormalities and neurological deficits following demyelination in a chronic inflammatory model of multiple sclerosis. Brain 2000, 123(Pt 3):519-531.
52. Howe C.L., Adelson J.D., Rodriguez M. Absence of perforin expression confers axonal protection despite demyelination. Neurobiol. Dis. 2007, 25:354-359.
53. Rivera-Quinones C., McGavern D., Schmelzer J.D., Hunter S.F., Low P.A., Rodriguez M. Absence of neurological deficits following extensive demyelination in a class I-deficient murine model of multiple sclerosis. Nat. Med. 1998, 4:187-193.
54. Olson J.K., Eagar T.N., Miller S.D. Functional activation of myelin-specific T cells by virus-induced molecular mimicry. J. Immunol. 2002, 169:2719-2726.
55. Olson J.K., Croxford J.L., Calenoff M.A., Dal Canto M.C., Miller S.D. A virus-induced molecular mimicry model of multiple sclerosis. J. Clin. Investig. 2001, 108:311-318.
56. Tsunoda I., Fujinami R.S. Inside-out versus outside-in models for virus induced demyelination: axonal damage triggering demyelination. Springer Semin. Immunopathol. 2002, 24:105-125.
57. Pirko I., Gamez J., Johnson A.J., Macura S.I., Rodriguez M. Dynamics of MRI lesion development in an animal model of viral-induced acute progressive CNS demyelination. Neuroimage 2004, 21:576-582.
58. Pirko I., Ciric B., Gamez J., Bieber A.J., Warrington A.E., Johnson A.J., Hanson D.P., Pease L.R., Macura S.I., Rodriguez M. A human antibody that promotes remyelination enters the CNS and decreases lesion load as detected by T2-weighted spinal cord MRI in a virus-induced murine model of MS. FASEB J. 2004, 18:1577-1579.
59. Pirko I., Nolan T.K., Holland S.K., Johnson A.J. Multiple sclerosis: pathogenesis and MR imaging features of hypointensities in a [corrected] murine model. Radiology 2008, 246:790-795.
60. Pirko I., Johnson A.J., Lohrey A.K., Chen Y., Ying J. Deep gray matter T2 hypointensity correlates with disability in a murine model of MS. J. Neurol. Sci. 2009, 282:34-38.
61. Pirko I., Suidan G.L., Rodriguez M., Johnson A.J. Acute hemorrhagic demyelination in a murine model of multiple sclerosis. J. Neuroinflamm. 2008, 5:31.
62. Blakemore W.F., Franklin R.J. Remyelination in experimental models of toxin-induced demyelination. Curr. Top. Microbiol. Immunol. 2008, 318:193-212.
63. Jeffery N.D., Blakemore W.F. Remyelination of mouse spinal cord axons demyelinated by local injection of lysolecithin. J. Neurocytol. 1995, 24:775-781.
64. Hall S.M. The effect of injections of lysophosphatidyl choline into white matter of the adult mouse spinal cord. J. Cell Sci. 1972, 10:535-546.
65. Bieber A.J., Kerr S., Rodriguez M. Efficient central nervous system remyelination requires T cells. Ann. Neurol. 2003, 53:680-684.
66. Shields S.A., Gilson J.M., Blakemore W.F., Franklin R.J. Remyelination occurs as extensively but more slowly in old rats compared to young rats following gliotoxin-induced CNS demyelination. Glia 1999, 28:77-83.
67. Suzuki K., Kikkawa Y. Status spongiosus of CNS and hepatic changes induced by cuprizone (biscyclohexanone oxalyldihydrazone). Am. J. Pathol. 1969, 54:307-325.
68. Carlton W.W. Spongiform encephalopathy induced in rats and guinea pigs by cuprizone. Exp. Mol. Pathol. 1969, 10:274-287.
69. Love S. Cuprizone neurotoxicity in the rat: morphologic observations. J. Neurol. Sci. 1988, 84:223-237.
70. Blakemore W.F., Franklin R.J. Advances in Multiple Sclerosis and Experimental Demyelinating Diseases 2008, Springer-Verlag, Berlin Heidelberg.
71. Matsushima G.K., Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 2001, 11:107-116.