Therapeutic strategies in multiple sclerosis. I. Immunotherapy

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1390, 1999, Pages 1697-1710

  Hohlfeld, Reinhard ^a,b,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Autoimmunity; Immunotherapy; Multiple sclerosis; T lymphocytes

Indexed keywords

EID: 0033615465     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0513     Document Type: Article

References (87)

1. Aharoni, R., Teitelbaum, D., Sela, M. & Arnon, R. 1998 Bystander suppression of experimental autoimmune encephalomyelitis by T cell lines and clones of the Th2 type induced by copolymer 1. J. Neuroimmunol. 91, 135-146.
2. Aharoni, R., Teitelbaum, D., Arnon, R. & Sela, M. 1999 Copolymer 1 acts against the immunodominant epitope 82-100 of myelin basic protein by T cell receptor antagonism in addition to major histocompatibility complex blocking. Proc. Natl Acad. Sci. USA 96, 634-639.
3. Arnason, B. G. W. & Reder, A. T. 1994 Interferons and multiple sclerosis. Clin. Neuropharmacol. 17, 495-547.
4. Arnon, R., Sela, M. & Teitelbaum, D. 1996 New insights into the mechanism of action of copolymer 1 in experimental allergic encephalomyelitis and multiple sclerosis. J. Neurol. 243(Suppl. 1), S8-S13.
5. Ben-Nun, A., Mendel, I., Bakimer, R., Fridkis-Hareli, M., Teitelbaum, D., Arnon, R., Sela, M. & Kerlero de Rosbo, N. 1996 The autoimmune reactivity to myelin oligodendrocyte glycoprotein (MOG) in multiple sclerosis is potentially pathogenic: effect of copolymer 1 on MOG-induced disease. J. Neurol. 243(Suppl. 1), S14-S22.
6. Bendtzen, K., Hansen, M. B., Ross, C., Poulsen, L. K. & Svenson, M. 1995 Cytokines and autoantibodies to cytokines. Stem Cells 13, 206-222.
7. Bornstein, M. B. (and 14 others) 1987 A pilot trial of Cop-1 in exacerbating remitting multiple sclerosis. N. Engl. J. Med. 317, 408-414.
8. Bornstein, M. B. (and 15 others) 1991 A placebo-controlled, double-blind, randomized, two-center, pilot trial of COP-1 in chronic progressive multiple sclerosis. Neurology 41, 533-539.
9. Boutros, T., Croze, E. & Yong, V. W. 1997 Interferon-β is a potent promoter of nerve growth factor production by astrocytes. J. Neurochem. 69, 939-946.
10. Briscoe, J., Kohlhuber, F. & Müller, M. 1996 JAKs and STATs branch out. Trends Cell Biol. 6, 336-340.
11. 1b treatment decreases tumor necrosis factor-α and increases interleukin-6 production in multiple sclerosis. Neurology 46, 1633-1638.
12. Calabresi, P. A., Pelfrey, C. M., Tranquill, L. R., Maloni, H. & McFarland, H. F. 1997a VLA-4 expression on peripheral blood lymphocytes is downregulated after treatment of multiple sclerosis with interferon-beta. Neurology 49, 1111-1116.
13. Calabresi, P. A., Tranquill, L. R., Dambrosia, J. M., Stone, L. A., Maloni, H., Bash, C. N., Frank, J. A. & McFarland, H. F. 1997b Increases in soluble VCAM-1 correlate with a decrease in MRI lesions in multiple sclerosis treated with interferon β-1b. Ann. Neurol. 41, 669-674.
14. Chabot, S., Williams, G. & Yong, V. W. 1997 Microglial production of TNF-α is induced by activated T lymphocytes. Involvement of VLA-4 and inhibition by interferon-β1b. J. Clin. Invest. 100, 604-612.
15. Compston, A. 1998 Treatment and management of multiple sclerosis. In McAlpine's multiple sclerosis (ed. A. Compston, G. Ebers, H. Lassmann, W. I. McDonald, B. Matthews & H. Wekerle), pp. 437-498. London: Churchill Livingstone.
16. Darnell, J. E., Kerr, I. M. & Stark, G. R. 1994 JAK-STAT pathways and transciptional activation in response to interferons and other extracellular signaling proteins. Science 264, 1415-1421.
17. Dayal, A. S., Jensen, M. A., Lledo, A. & Arnason, B. G. W. 1995 Interferon-gamma secreting cells in multiple sclerosis patients treated with interferon beta-1b. Neurology 45, 2173-2177.
18. Durelli, L. (and 11 others) 1994 Chronic systemic high-dose recombinant interferon alfa-2a reduces exacerbation rate, MRI signs of disease activity, and lymphocyte interferon gamma production in relapsing remitting multiple sclerosis. Neurology 44, 406-413.
19. Ebers, G. C. & PRISM (Prevention of Relapses and Disability by Interferon beta-1a Subcutaneously in Multiple Sclerosis) 1998 Randomised double-blind placebo-controlled study of interferon β-1a in relapsing/remitting multiple sclerosis. Lancet 352, 1498-1504.
20. Fierlbeck, G., Schreiner, T., Schaber, B., Walser, A. & Rassner, G. 1994 Neutralizing interferon β antibodies in melanoma patients treated with recombinant and natural Interferon β. Cancer Immunol. Immunother. 39, 263-268.
21. Fridkis-Hareli, M. & Strominger, J. L. 1998 Promiscuous binding of synthetic copolymer 1 to purified HLA-DR molecules. J. Immunol. 160, 4386-4397.
22. Genain, C. P., Nguyen, M.-H., Letvin, N. L., Pearl, R., Davis, R. L., Adelmann, M., Lees, M. B., Linington, C. & Hauser, S. L. 1995 Antibody facilitation of multiple sclerosis-like lesions in a nonhuman primate. J. Clin. Invest. 96, 2966-2974.
23. Genain, C. P., Abel, K., Belmar, N., Villinger, F., Rosenberg, D. P., Linington, C., Raine, C. S. & Hauser, S. L. 1996 Late complications of immune deviation therapy in a nonhuman primate. Science 274, 2054-2057.
24. Genain, C. P., Cannella, B., Hauser, S. L. & Raine, C. S. 1999 Identification of autoantibodies associated with myelin damage in multiple sclerosis. Nature Med. 5, 170-175.
25. + B cells in active multiple sclerosis and reversal by interferon-β-1b therapy. J. Clin. Invst. 99, 2664-2761.
26. Guthikonda, P., Baker, J. & Mattson, D. H. 1998 Interferon-beta1-b (IFN-B) decreases induced nitric oxide (NO) production by a human astrocytoma line. J. Neuroimmunol. 82, 133-139.
27. Hall, G. L., Compston, A. & Scolding, N. J. 1997 Beta-interferon and multiple sclerosis. Trends Neurosci. 20, 63-67.
28. Hofer, M., Pagliusi, S. R., Hohn, A., Leibrock, A. & Barde, Y.-A. 1990 Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9, 2459-2464.
29. Hohlfeld, R. 1989 Neurological autoimmune disease and the trimolecular complex of T-lymphocytes. Ann. Neurol. 25, 531-538.
30. Hohlfeld, R. 1997 Biotechnological agents for the immunotherapy of multiple sclerosis. Principles, problems and perspectives. Brain 120, 865-916.
31. IFNB (Interferon beta) Multiple Sclerosis Study Group 1995 Interferon beta-1b in the treatment of multiple sclerosis: final outcome of the randomized controlled trial. Neurology 45, 1277-1285.
32. IFNB (Interferon beta) Multiple Sclerosis Study Group and UBC MS/MRI Analysis Group 1996 Neutralizing antibodies during treatment of multiple sclerosis with interferon beta-1b: experience during the first three years. Neurology 47, 889-894.
33. Jacobs, L. & Johnson, K. P. 1994 A brief history of the use of interferons as treatment of multiple sclerosis. Arch. Neurol. 51, 1240-1251.
34. Jacobs, L. D (and 25 others and The Multiple Sclerosis Collaborative Research Group (MSCRG)) 1990 Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. Ann. Neurol. 39, 285-294.
35. Johnson, K. P (and 12 others and The Copolymer 1 Multiple Sclerosis Study Group) 1995 Copolymer 1 reduces relapse rate and improves disability in relapsing remitting multiple sclerosis. Results of a phase III multicenter, double-blind, placebo-controlled trial. Neurology 45, 1268-1276.
36. Johnson, K. P. (and 12 others and The Copolymer 1 Multiple Sclerosis Study Group) 1998 Extended use of glatiramer acetate (Copaxone) is well tolerated and maintains its clinical effect on multiple sclerosis relapse rate and degree of disability. Neurology 50, 701-708.
37. Kappos, L. & European Study Group on Interferon-beta in Secondary Progressive MS 1998 Placebo-controlled multicenter randomized trial of Interferon β-1b in treatment of secondary progressive multiple sclerosis. Lancet 352, 1491-1497.
38. Kappos, L. (and 10 others and the Gadolinium MRI Meta-Analysis Study Group) 1999 Predictive value of gadolinium enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis. Lancet 353, 964-969.
39. Karni, A., Bakimer-Kleiner, R., Abramsky, O. & Ben-Nun, A. 1999 Elevated levels of antibody to myelin-oligodendrocyte glycoprotein is not specific for patients with multiple sclerosis. Arch. Neural. 56, 311-315.
40. Kerschensteiner, M., Gallmeier, E., Behrens, L., Klinkert, W. E. F., Kolbeck, R., Hoppe, E., Stadelmann, C., Lassmann, H., Wekerle, H. & Hohlfeld, R. 1999 Activated human T cells, B cells and monocytes produce brain-derived neurotrophic factor (BDNF) in vitro and in brain lesions: a neuroprotective role of inflammation? J. Exp. Med. 189, 865-870.
41. Khan, O. A. & Dhib-Jalbut, S. S. 1998 Neutralizing antibodies to interferon β-1a and interferon β-1b in MS patients are cross-reactive. Neurology 51, 1698-1702.
42. Kojima, K., Berger, T., Lassmann, H., Hinze-Selch, D., Zhang, Y., Gehrmann, J., Wekerle, H. & Linington, C. 1994 Experimental autoimmune panencephalitis and uvcoretinitis in the Lewis rat transferred by T lymphocytes specific for the S100β molecule, a calcium binding protein of astroglia. J. Exp. Med. 180, 817-829.
43. Lassmann, H. & Wekerle, H. 1998 Experimental models of multiple sclerosis. In McAlpine's multiple sclerosis (ed. A. Compston, G. Ebers, H. Lassmann, W. I. McDonald, B. Matthews & H. Wekerle), pp. 409-434. London: Churchill Livingstone.
44. Lassmann, H., Raine, C. S., Antel, J. & Princas, J. W. 1998 Immnopathology of multiple sclerosis: report on an international meeting held at the Institute of Neurology of the University of Vienna. J. Neuroimmunol. 86, 213-217.
45. Leppert, D., Waubant, E., Bürk, M. R., Oksenberg, J. R. & Hauser, S. L. 1996 Interferon-beta-1b inhibits gelatinase secretion and in vitro migration of human T cells: a possible mechanism for treatment efficacy in multiple sclerosis. Ann. Neurol. 40, 846-854.
46. Lewin, G. R. & Barde, Y.-A. 1996 Physiology of the neurotrophins. A. Rev. Neurosci. 19, 289-317.
47. Lindert, R.-B., Haase, C. G., Brehm, U., Linington, C., Wekerle, H. & Hohlfeld, R. 1999 Multiple sclerosis: B and T cell responses to the extracellular domain of the myelin oligodendrocyte glycoprotein (MOG). Brain (In the press.)
48. Linington, C., Bradl, M., Lassmann, H., Brunner, C. & Vass, K. 1988 Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am. J. Pathol. 130, 443-454.
49. Linington, C., Berger, T., Perry, L., Weerth, S., Hinze-Selch, D., Zhang, Y., Lu, H.-C., Lassmann, H. & Wekerle, H. 1993 T cells specific for the myelin oligodendrocyte glycoprotein (MOG) mediate an unusual autoimmune inflammatory response in the central nervous system. Eur. J. Immunol. 23, 1364-1372.
50. Lu, H.-T., Riley, J. L., Babcock, G. T., Huston, M., Stark, G. R., Boss, J. M. & Ransohoff, R. M. 1995 Interferon (IFN) β acts downstream of IFN-γ-induced class II transactivator messenger RNA accumulation to block histocompatibility complex class II gene expression and requires the 48-kD DNA-binding protein, ISGF3-g. J. Exp. Med. 182, 1517-1525.
51. Lucchinetti, C. F., Brück, W., Rodriguez, M. & Lassmann, H. 1996 Dístinct patterns of multiple sclerosis pathology indicates heterogeneity in pathogenesis. Brain Pathol. 6, 259-274.
52. McDonald, W. I. 1998 Diagnostic methods investigation in multiple sclerosis. In McAlpine's multiple sclerosis (ed. A. Compston, G. Ebers, H. Lassmann, W. I. McDonald, B. Matthews & H. Wekerle), pp. 251-279. London: Churchill Livingstone.
53. McRac, B. L., Semnani, R. T., Hayes, M. P. & Van Seventer, G. A. 1998 Type I IFNs inhibit human dendritic cell IL-12 production and Th1 cell development. J. Immunol. 160, 4298-4304.
54. Malik, O., Compston, D. A. S. & Scolding, N. J. 1998 Interferon-beta inhibits mitogen induced astrocyte proliferation in vitro, J. Neuroimmunol. 86, 155-162.
55. Martínez-Cáceres, E. M., Río, J., Barrau, M., Durán, I., Borrás, C., Tintoré, M. & Montalban, X. 1998 Amelioration of flu-like symptoms at the onset of interferon β-1β therapy in multiple sclerosis by low-dose oral steroids is related to decrease in interleukin-6 induction. Ann. Neurol. 44, 682-685.
56. Miller, A., Shapiro, S., Gershtein, R., Kinarty, A., Awashdeh, H., Onigman, S. & Hat, N. 1998 Treatment of multiple sclerosis with copolymer-1 (Copaxone): implicating mechanisms of Th1 to Th2/Th3 immune deviation. J. Neuroimmunol. 92, 113-121.
57. Moalem, G., Leibowitz-Amit, R., Yoles, E., Mor, F., Cohen, I. R. & Schwartz, M. 1999 Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nature Med. 5, 49-55.
58. Myhr, K. M. (and 12 others and the Norwegian Study Group on Interferon-α in Multiple Sclerosis) 1999 Interferon-α2a reduces MRI disease activity in relapsing remitting multiple sclerosis. Neurology 52, 1049-1056.
59. Neumann, H. & Wekerle, H. 1998 Neuronal control of the immune response in the central nervous system: linking brain immunity to neurodegeneration. J. Neuropathol. Exp. Neurol. 58, 1-9.
60. Noseworthy, J. H., Gold, R. & Hartung, H.-P. 1999 Treatment of multiple sclerosis: recent trials and future perspectives. Curr. Opin. Neurol. 12, 279-293.
61. Panitch, H. S., Hirsch, R .L., Schindler, J. & Johnson, K. P. 1987 Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system. Neurology 37, 1097-1102.
62. Paty, D. W., Li, D. K. B., UBC MS/MRI Analysis Group & IFNB Multiple Sclerosis Study Group 1993 Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. II. MRI analysis results of a multicenter, randomized, double blind, placebo-controlled trial. Neurology 43, 662-667.
63. Pette, M., Pette, D. F., Muraro, P. A., Martin, R. & McFarland, H. F. 1997 Interferon-β interferes with the proliferation but not with the cytokine secretion of myelin basic protein-specific T-helper type 1 lymphocytes. Neurology 49, 385-392.
64. Reindl, M., Linington, C., Brehm, U., Egg, R., Dilitz, E., Deisenhammer, F., Poewe, W. & Berger, T. 1999 Antibodies against the myelin oligodendrocyte glycoprotein and the myelin basic protein in multiple sclerosis and other neurological diseases: a comparative study. Brain (In the press.)
65. Rep, M. H. G., Hintzen, R. Q., Polman, C. H. & Van Lier, R. A. W. 1996 Recombinant interferon-β blocks proliferation but enhances interleukin-10 secretion by activated human T cells. J. Neuroimmunol. 67, 111-118.
66. Rudick, R. A., Ransohoff, R. M., Peppler, R., Van der Brug, S., Lehmann, P. V. & Alam, J. 1996 Interferon beta induces interleukin-10 expression: relevance to multiple sclerosis. Ann. Neurol. 40, 618-627.
67. Rudick, R. A., Ransohoff, R. M., Lee, J.-C., Peppler, R., Yu, M., Mathisen, P. M. & Tuohy, V. K. 1998a In vivo effects of interferon beta-1a on immunosuppressibe cytokines in multiple sclerosis. Neurology 50, 1294-1300.
68. Rudick, R. A. (and 16 others and The Multiple Sclerosis Collaborative Research Group (MSCRG) 1998b Incidence and significance of neutralizing antibodies to interferon beta-1a in multiple sclerosis. Neurology 50, 1266-1272.
69. Rudick, R. A., Carpenter, C. S., Cookfair, D. L., Tuohy, V. K. & Ransohoff, R. M. 1999a In vitro and in vivo inhibition of mitogen-driven T cell activation by recombinant interferon-beta. Neurology 43, 2080-2087.
70. Rudick, R. A. (and 28 others and the Multiple Sclerosis Collaborative Research Group (MSCRG) 1999b Cerebrospinal fluid abnormalities in a phase III trial of Avonex® (IFNβ-1a) for relapsing multiple sclerosis. J. Neuroimmunol. 93, 8-14.
71. Schmidt, S., Hertfelder, H.-J., Von Spiegel, T., Hering, R., Harzheim, M., Lassmann, H., Deckert-Schlüter, M. & Schlegel, U. 1999 Lethal capillary leak syndrome after a single administration of interferon beta-1b. Neurology 53, 220-222.
72. Sibley, W. A. & IFNB Multiple Sclerosis Study Group 1993 Interferon beta-1b is effective in relapsing remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 43, 655-661.
73. Sörensen, T. L. (and 11 others) 1999 Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J. Clin. Invest. 103, 807-815.
74. Steinman, L. 1993 Connections between the immune system and the nervous system. Proc. Natl Acad. Sci. USA 90, 7912-7914.
75. Stone, L. A., Frank, J. A., Albert, P. S., Bash, C., Smith, M. E., Maloni, H. & McFarland, H. F. 1995 The effect of interferon-β on blood brain barrier disruptions demonstrated by contrast-enhanced magnetic resonance imaging in relapsing remitting multiple sclerosis. Ann. Neurol. 37, 611-619.
76. Storch, M. K., Stefferl, A., Brehm, U., Weissert, R., Wallström, E., Kerschensteiner, M., Olsson, T., Linington, C. & Lassmann, H. 1998 Autoimmunity to myelin oligodendrocyte glycoprotein in rats mimics the spectrum of multiple sclerosis pathology. Brain Pathol. 8, 681-694.
77. Stüve, O., Dooley N. P., Uhm, J. H., Antel, J. P., Francis, G. S., Williams, G. & Yong, V. W. 1996 Interferon-β-1b decreases the migration of T lymphocytes in vitro: effects on matrix metalloproteinase-9. Ann. Neurol. 40, 853-863.
78. Teitelbaum, D., Fridkis-Hareli, M., Arnon, R. & Sela, M. 1996 Copolymer 1 inhibits chronic relapsing experimental allergic encephalomyelitis induced by protcolipid protein (PLP) peptides in mice and interferes with PLP-specific T cell responses. J. Neuroimmunol. 64, 209-217.
79. Van Weyenbergh, J., Lipinski, P., Abadie, A., Chabas, D., Blank, U., Liblau, R. & Wietzerbin, J. 1998 Antagonistic action of IFN-β and IFN-γ on high affinity Fcg receptor expression in healthy controls and multiple sclerosis patients. J. Immnnol. 161, 1568-1574.
80. Weber, F., Polak, T., Günther, A., Kubuschok, B., Janovskaja, J., Bitsch, A., Poser, S. & Rieckmann, P. 1998 Synergistic immunomodulatory effects of interferon-β1b and the phosphodiesterase inhibitor pentoxifylline in patients with relapsing-remitting multiple sclerosis. Ann. Neurol. 44, 27-34.
81. Weber, F., Janovskaja, J., Polak, T., Poser, S. & Rieckmann, P. 1999 Effect of interferon-β on human myelin basic protein-specific T cell lines: comparison of IFNβ-1a and IFNβ-1b. Neurology 52, 1069-1071.
82. Weilbach, F. X. & Gold, R. 1999 Disease modifying treatments for multiple sclerosis. What is the horizon? CNS Drugs 11, 133-157.
83. Weinstock-Guttman, B., Ransohoff, R. M., Kinkel, R. P. & Rudick, R. A. 1995 The interferons: biological effects, mechanisms of action, and use in multiple sclerosis. Ann. Neurol. 37, 8-15.
84. Wekerle, H., Linington, C., Lassmann, H. & Meyermann, R. 1986 Cellular immune reactivity within the CNS. Trends Neurosci. 9, 271-277.
85. Wekerle, H., Kojima, K., Lannes-Vieira, J., Lassmann, H. & Linington, C. 1994 Animal models. Ann. Neurol. 36, S47-S53.
86. Wraith, D. C., McDevitt, H. O., Steinman, L. & Acha-Orbea, H. 1989 T cell recognition as the target for immune intervention in autoimmune disease. Cell 57, 709-715.
87. Yong, V. W., Chabot, S., Stüve, O. & Williams, G. 1998 Interferon beta in the treatment of multiple sclerosis. Mechanisms of action. Neurology 51, 682-689.