Novel immunomodulatory approaches for the management of multiple sclerosis

Clinical Pharmacology and Therapeutics

Volumn 95, Issue 1, 2014, Pages 32-44

  Kantarci, O H ^a   Pirko, I ^a   Rodriguez, M ^b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; BETA INTERFERON; DACLIZUMAB; FINGOLIMOD; FUMARIC ACID DIMETHYL ESTER; GLATIRAMER; IMMUNOMODULATING AGENT; MITOXANTRONE; NATALIZUMAB; PLASMA SUBSTITUTE; RITUXIMAB; TERIFLUNOMIDE;

ANEMIA; CHILDHOOD DISEASE; CORTICOSTEROID THERAPY; DEMYELINATION; DISEASE COURSE; DRUG TREATMENT FAILURE; HUMAN; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; MEDICAL DECISION MAKING; MULTICENTER STUDY (TOPIC); MULTIPLE SCLEROSIS; NERVE FIBER; NERVE REGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NUCLEAR MAGNETIC RESONANCE IMAGING; ORAL PARESTHESIA; PERSONALIZED MEDICINE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLASMAPHERESIS; PRIORITY JOURNAL; REMYELINIZATION; REVIEW;

EID: 84890911043     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1038/clpt.2013.196     Document Type: Review

References (98)

1. Noseworthy, J.H., Lucchinetti, C., Rodriguez, M. & Weinshenker, B.G. Multiple sclerosis. N. Engl. J. Med. 343, 938-952 (2000).
2. Lassmann, H., Brück, W. & Lucchinetti, C. Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy. Trends Mol. Med. 7, 115-121 (2001). (Pubitemid 32201673)
3. McDonald, W.I. et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann. Neurol. 50, 121-127 (2001).
4. Polman, C.H. et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann. Neurol. 69, 292-302 (2011).
5. Polman, C.H. et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann. Neurol. 58, 840-846 (2005). (Pubitemid 41746873)
6. Engell, T. A clinical patho-anatomical study of clinically silent multiple sclerosis. Acta Neurol. Scand. 79, 428-430 (1989). (Pubitemid 19129066)
7. Mews, I., Bergmann, M., Bunkowski, S., Gullotta, F. & Brück, W. Oligodendrocyte and axon pathology in clinically silent multiple sclerosis lesions. Mult. Scler. 4, 55-62 (1998). (Pubitemid 28197347)
8. Lebrun, C. et al.; CFSEP. Unexpected multiple sclerosis: follow-up of 30 patients with magnetic resonance imaging and clinical conversion profile. J. Neurol. Neurosurg. Psychiatr. 79, 195-198 (2008). (Pubitemid 351236555)
9. Okuda, D.T. et al. Incidental MRI anomalies suggestive of multiple sclerosis: the radiologically isolated syndrome. Neurology 72, 800-805 (2009).
10. Siva, A., Saip, S., Altintas, A., Jacob, A., Keegan, B.M. & Kantarci, O.H. Multiple sclerosis risk in radiologically uncovered asymptomatic possible inflammatory-demyelinating disease. Mult. Scler. 15, 918-927 (2009).
11. CHAMPS Study Group. Interferon beta-1a for optic neuritis patients at high risk for multiple sclerosis. Am. J. Ophthalmol. 132, 463-471 (2001).
12. Anonymous. Predictors of short-term disease activity following a first clinical demyelinating event: analysis of the CHAMPS placebo group. Mult. Scler. 8, 405-409 (2002).
13. Anonymous. Baseline MRI characteristics of patients at high risk for multiple sclerosis: results from the CHAMPS trial. Controlled High-Risk Subjects Avonex Multiple Sclerosis Prevention Study. Mult. Scler. 8, 330-338 (2002).
14. Tutuncu, M. et al. Onset of progressive phase is an age-dependent clinical milestone in multiple sclerosis. Mult. Scler. 19, 188-198 (2013).
15. Chrousos, G.A., Kattah, J.C., Beck, R.W. & Cleary, P.A. Side effects of glucocorticoid treatment. Experience of the Optic Neuritis Treatment Trial. JAMA 269, 2110-2112 (1993). (Pubitemid 23112630)
16. Séguin, C. et al. Non-traumatic necrosis of bone (osteonecrosis) is associated with endothelial cell activation but not thrombophilia. Rheumatology (Oxford). 47, 1151-1155 (2008). (Pubitemid 352038218)
17. Li, W. et al. Distribution of TRAP-positive cells and expression of HIF-1alpha, VEGF, and FGF-2 in the reparative reaction in patients with osteonecrosis of the femoral head. J. Orthop. Res. 27, 694-700 (2009).
18. Radke, S., Battmann, A., Jatzke, S., Eulert, J., Jakob, F. & Schütze, N. Expression of the angiomatrix and angiogenic proteins CYR61, CTGF, and VEGF in osteonecrosis of the femoral head. J. Orthop. Res. 24, 945-952 (2006). (Pubitemid 43804929)
19. Ciccone, A., Beretta, S., Brusaferri, F., Galea, I., Protti, A. & Spreafico, C. Corticosteroids for the long-term treatment in multiple sclerosis. Cochrane Database Syst. Rev. CD006264 (2008).
20. Beck, R.W. et al. A randomized, controlled trial of corticosteroids in the treatment of acute optic neuritis. The Optic Neuritis Study Group. N. Engl. J. Med. 326, 581-588 (1992).
21. Beck, R.W. & Gal, R.L. Treatment of acute optic neuritis: a summary of findings from the optic neuritis treatment trial. Arch. Ophthalmol. 126, 994-995 (2008). (Pubitemid 352008387)
22. Katz, B., Trobe, J.D. & Beck, R.W. The optic neuritis treatment trial: implications for clinicians. Semin. Ophthalmol. 10, 214-220 (1995).
23. Corbett, J.J. What have the optic neuritis treatment trial and the longitudinal optic neuritis study shown us? J. Neurol. Sci. 125, 1-2 (1994). (Pubitemid 24240179)
24. Beck, R.W. & Cleary, P.A. Optic neuritis treatment trial. One-year follow-up results. Arch. Ophthalmol. 111, 773-775 (1993). (Pubitemid 23170588)
25. Weinshenker, B.G. et al. A randomized trial of plasma exchange in acute central nervous system inflammatory demyelinating disease. Ann. Neurol. 46, 878-886 (1999).
26. Keegan, M., Pineda, A.A., McClelland, R.L., Darby, C.H., Rodriguez, M. & Weinshenker, B.G. Plasma exchange for severe attacks of CNS demyelination: predictors of response. Neurology 58, 143-146 (2002).
27. Magaña, S.M. et al. Beneficial plasma exchange response in central nervous system inflammatory demyelination. Arch. Neurol. 68, 870-878 (2011).
28. Keegan, M. et al. Relation between humoral pathological changes in multiple sclerosis and response to therapeutic plasma exchange. Lancet 366, 579-582 (2005). (Pubitemid 41140333)
29. Elkhalifa, A. & Weiner, H. Cyclophosphamide Treatment of MS: Current Therapeutic Approaches and Treatment Regimens. Int. MS J. 17, 12-18 (2010).
30. Weiner, H.L., Hauser, S.L., Hafler, D.A., Fallis, R.J., Lehrich, J.R. & Dawson, D.M. The use of cyclophosphamide in the treatment of multiple sclerosis. Ann. N. Y. Acad. Sci. 436, 373-381 (1984). (Pubitemid 15102060)
31. Costelloe, L., Jones, J. & Coles, A. Secondary autoimmune diseases following alemtuzumab therapy for multiple sclerosis. Expert Rev. Neurother. 12, 335-341 (2012).
32. Perumal, J.S., Foo, F., Cook, P. & Khan, O. Subcutaneous administration of alemtuzumab in patients with highly active multiple sclerosis. Mult. Scler. 18, 1197-1199 (2012).
33. Coles, A.J. et al. Alemtuzumab vs. interferon beta-1a in early multiple sclerosis. N. Engl. J. Med. 359, 1786-1801 (2008).
34. Noseworthy, J.H. et al. IV immunoglobulin does not reverse established weakness in MS. Neurology 55, 1135-1143 (2000).
35. Ghatak, N.R., Leshner, R.T., Price, A.C. & Felton, W.L. 3rd. Remyelination in the human central nervous system. J. Neuropathol. Exp. Neurol. 48, 507-518 (1989). (Pubitemid 19220607)
36. Lucchinetti, C., Brück, W., Parisi, J., Scheithauer, B., Rodriguez, M. & Lassmann, H. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 122 (Pt 12), 2279-2295 (1999).
37. Weiner, L.P., Waxman, S.G., Stohlman, S.A. & Kwan, A. Remyelination following viral-induced demyelination: ferric ion-ferrocyanide staining of nodes of Ranvier within the CNS. Ann. Neurol. 8, 580-583 (1980). (Pubitemid 11213501)
38. Murray, P.D., McGavern, D.B., Sathornsumetee, S. & Rodriguez, M. Spontaneous remyelination following extensive demyelination is associated with improved neurological function in a viral model of multiple sclerosis. Brain 124, 1403-1416 (2001). (Pubitemid 32606101)
39. Bieber, A.J., Kerr, S. & Rodriguez, M. Efficient central nervous system remyelination requires T cells. Ann. Neurol. 53, 680-684 (2003). (Pubitemid 36529446)
40. Kotter, M.R., Setzu, A., Sim, F.J., Van Rooijen, N. & Franklin, R.J. Macrophage depletion impairs oligodendrocyte remyelination following lysolecithininduced demyelination. Glia 35, 204-212 (2001). (Pubitemid 32827763)
41. Yamamura, T., Sun, D., Aloisi, F., Klinkert, W.E. & Wekerle, H. Interaction between oligodendroglia and immune cells: mitogenic effect of an oligodendrocyte precursor cell line on syngeneic T lymphocytes. J. Neurosci. Res. 32, 178-189 (1992).
42. Asakura, K., Miller, D.J., Pease, L.R. & Rodriguez, M. Targeting of IgMkappa antibodies to oligodendrocytes promotes CNS remyelination. J. Neurosci. 18, 7700-7708 (1998). (Pubitemid 28441011)
43. Miller, D.J., Bright, J.J., Sriram, S. & Rodriguez, M. Successful treatment of established relapsing experimental autoimmune encephalomyelitis in mice with a monoclonal natural autoantibody. J. Neuroimmunol. 75, 204-209 (1997). (Pubitemid 27170321)
44. Ciric, B., VanKeulen, V., Rodriguez, M., Kyle, R.A., Gertz, M.A. & Pease, L.R. Clonal evolution in Waldenstrom macroglobulinemia highlights functional role of B-cell receptor. Blood 97, 321-323 (2001). (Pubitemid 32061276)
45. Warrington, A.E. et al. Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis. Proc. Natl. Acad. Sci. USA 97, 6820-6825 (2000). (Pubitemid 30412798)
46. Watzlawik, J. et al. Human remyelination promoting antibody inhibits apoptotic signaling and differentiation through Lyn kinase in primary rat oligodendrocytes. Glia 58, 1782-1793 (2010).
47. Kantarci, O. et al. Survival and predictors of disability in Turkish MS patients. Turkish Multiple Sclerosis Study Group (TUMSSG). Neurology 51, 765-772 (1998). (Pubitemid 28449257)
48. Runmarker, B. & Andersen, O. Prognostic factors in a multiple sclerosis incidence cohort with twenty-five years of follow-up. Brain 116 (Pt 1), 117-134 (1993). (Pubitemid 23087038)
49. Weinshenker, B.G., Rice, G.P., Noseworthy, J.H., Carriere, W., Baskerville, J. & Ebers, G.C. The natural history of multiple sclerosis: a geographically based study. 3. Multivariate analysis of predictive factors and models of outcome. Brain 114 (Pt 2), 1045-1056 (1991).
50. Rodriguez, M., Siva, A., Ward, J., Stolp-Smith, K., O'Brien, P. & Kurland, L. Impairment, disability, and handicap in multiple sclerosis: a population-based study in Olmsted County, Minnesota. Neurology 44, 28-33 (1994).
51. Pittock, S.J. et al. Change in MS-related disability in a population-based cohort: a 10-year follow-up study. Neurology 62, 51-59 (2004). (Pubitemid 38082870)
52. Benedikz, J. et al. The natural history of untreated multiple sclerosis in Iceland. A total population-based 50 year prospective study. Clin. Neurol. Neurosurg. 104, 208-210 (2002). (Pubitemid 34799912)
53. Confavreux, C., Aimard, G. & Devic, M. Course and prognosis of multiple sclerosis assessed by the computerized data processing of 349 patients. Brain 103, 281-300 (1980). (Pubitemid 10046624)
54. Levic, Z.M. et al. Prognostic factors for survival in multiple sclerosis. Mult. Scler. 5, 171-178 (1999). (Pubitemid 29290446)
55. Myhr, K.M. et al. Disability and prognosis in multiple sclerosis: demographic and clinical variables important for the ability to walk and awarding of disability pension. Mult. Scler. 7, 59-65 (2001). (Pubitemid 32396580)
56. Pittock, S.J. et al. Clinical implications of benign multiple sclerosis: a 20-year population-based follow-up study. Ann. Neurol. 56, 303-306 (2004). (Pubitemid 39037929)
57. Riise, T. et al. Early prognostic factors for disability in multiple sclerosis, a European multicenter study. Acta Neurol. Scand. 85, 212-218 (1992).
58. Weinshenker, B.G. et al. The natural history of multiple sclerosis: a geographically based study. 2. Predictive value of the early clinical course. Brain 112 (Pt 6), 1419-1428 (1989). (Pubitemid 20024212)
59. Kantarci, O.H. & Weinshenker, B.G. Natural history of multiple sclerosis. Neurol. Clin. 23, 17-38, v (2005).
60. Confavreux, C. & Vukusic, S. Natural history of multiple sclerosis: a unifying concept. Brain 129, 606-616 (2006). (Pubitemid 43278223)
61. Wolinsky, J.S.; PROMiSe Study Group. The diagnosis of primary progressive multiple sclerosis. J. Neurol. Sci. 206, 145-152 (2003). (Pubitemid 36143719)
62. Jacobs, L.D. et al. Intramuscular interferon beta-1a therapy initiated during a first demyelinating event in multiple sclerosis. CHAMPS Study Group. N. Engl. J. Med. 343, 898-904 (2000).
63. Beck, R.W. et al. Interferon beta-1a for early multiple sclerosis: CHAMPS trial subgroup analyses. Ann. Neurol. 51, 481-490 (2002). (Pubitemid 34260778)
64. Comi, G., Filippi, M. & Wolinsky, J.S. European/Canadian multicenter, doubleblind, randomized, placebo-controlled study of the effects of glatiramer acetate on magnetic resonance imaging-measured disease activity and burden in patients with relapsing multiple sclerosis. European/Canadian Glatiramer Acetate Study Group. Ann. Neurol. 49, 290-297 (2001). (Pubitemid 32202781)
65. Comi, G. et al.; PreCISe study group. Effect of glatiramer acetate on conversion to clinically definite multiple sclerosis in patients with clinically isolated syndrome (PreCISe study): a randomised, double-blind, placebo-controlled trial. Lancet 374, 1503-1511 (2009).
66. Paty, D.W. & Li, D.K. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. II. MRI analysis results of a multicenter, randomized, double-blind, placebo-controlled trial. UBC MS/MRI Study Group and the IFNB Multiple Sclerosis Study Group. Neurology 43, 662-667 (1993). (Pubitemid 23121952)
67. Jacobs, L.D. et al. Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann. Neurol. 39, 285-294 (1996). (Pubitemid 26100751)
68. Antonelli, G. et al. Further study on the specificity and incidence of neutralizing antibodies to interferon (IFN) in relapsing remitting multiple sclerosis patients treated with IFN beta-1a or IFN beta-1b. J. Neurol. Sci. 168, 131-136 (1999). (Pubitemid 29467431)
69. Waubant, E. et al. Clinical characteristics of responders to interferon therapy for relapsing MS. Neurology 61, 184-189 (2003). (Pubitemid 36875298)
70. Johnson, K.P. et al. Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: results of a phase III multicenter, double-blind placebo-controlled trial. The Copolymer 1 Multiple Sclerosis Study Group. Neurology 45, 1268-1276 (1995).
71. Ge, Y. et al. Glatiramer acetate (Copaxone) treatment in relapsing-remitting MS: quantitative MR assessment. Neurology 54, 813-817 (2000). (Pubitemid 30111334)
72. Wolinsky, J.S., Narayana, P.A. & Johnson, K.P.; Multiple Sclerosis Study Group and the MRI Analysis Center. United States open-label glatiramer acetate extension trial for relapsing multiple sclerosis: MRI and clinical correlates. Multiple Sclerosis Study Group and the MRI Analysis Center. Mult. Scler. 7, 33-41 (2001). (Pubitemid 32396577)
73. Noseworthy, J.H. & Kirkpatrick, P. Natalizumab. Nat. Rev. Drug Discov. 4, 101-102 (2005).
74. Miller, D.H. et al.; International Natalizumab Multiple Sclerosis Trial Group. A controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med. 348, 15-23 (2003). (Pubitemid 36026342)
75. Langer-Gould, A., Atlas, S.W., Green, A.J., Bollen, A.W. & Pelletier, D. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 353, 375-381 (2005). (Pubitemid 41132342)
76. Kleinschmidt-DeMasters, B.K. & Tyler, K.L. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N. Engl. J. Med. 353, 369-374 (2005). (Pubitemid 41132341)
77. Kappos, L. et al.; FREEDOMS Study Group. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N. Engl. J. Med. 362, 387-401 (2010).
78. Cohen, J.A. et al.; TRANSFORMS Study Group. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N. Engl. J. Med. 362, 402-415 (2010).
79. Hartung, H.P. et al.; Mitoxantrone in Multiple Sclerosis Study Group (MIMS). Mitoxantrone in progressive multiple sclerosis: a placebo-controlled, doubleblind, randomised, multicentre trial. Lancet 360, 2018-2025 (2002).
80. Ghalie, R.G. et al. A study of therapy-related acute leukaemia after mitoxantrone therapy for multiple sclerosis. Mult. Scler. 8, 441-445 (2002).
81. Linker, R.A. et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 134, 678-692 (2011).
82. Kappos, L. et al. Effect of BG-12 on contrast-enhanced lesions in patients with relapsing-remitting multiple sclerosis: subgroup analyses from the phase 2b study. Mult. Scler. 18, 314-321 (2012).
83. MacManus, D.G. et al. BG-12 reduces evolution of new enhancing lesions to T1-hypointense lesions in patients with multiple sclerosis. J. Neurol. 258, 449-456 (2011).
84. Brousil, J.A., Roberts, R.J. & Schlein, A.L. Cladribine: an investigational immunomodulatory agent for multiple sclerosis. Ann. Pharmacother. 40, 1814-1821 (2006). (Pubitemid 44544879)
85. Yang, J.S., Xu, L.Y., Xiao, B.G., Hedlund, G. & Link, H. Laquinimod (ABR- 215062) suppresses the development of experimental autoimmune encephalomyelitis, modulates the Th1/Th2 balance and induces the Th3 cytokine TGF-beta in Lewis rats. J. Neuroimmunol. 156, 3-9 (2004). (Pubitemid 39310510)
86. Comi, G. et al.; ALLEGRO Study Group. Placebo-controlled trial of oral laquinimod for multiple sclerosis. N. Engl. J. Med. 366, 1000-1009 (2012).
87. Bielekova, B. et al. Humanized anti-CD25 (daclizumab) inhibits disease activity in multiple sclerosis patients failing to respond to interferon beta. Proc. Natl. Acad. Sci. U.S.A. 101, 8705-8708 (2004). (Pubitemid 38745835)
88. Paolillo, A. et al. Quantitative MRI in patients with secondary progressive MS treated with monoclonal antibody Campath 1H. Neurology 53, 751-757 (1999). (Pubitemid 29448295)
89. Coles, A.J. et al. Alemtuzumab more effective than interferon ß-1a at 5-year follow-up of CAMMS223 clinical trial. Neurology 78, 1069-1078 (2012).
90. Jones, J.L. et al. Improvement in disability after alemtuzumab treatment of multiple sclerosis is associated with neuroprotective autoimmunity. Brain 133, 2232-2247 (2010).
91. Cossburn, M. et al. Autoimmune disease after alemtuzumab treatment for multiple sclerosis in a multicenter cohort. Neurology 77, 573-579 (2011).
92. Cuker, A. et al. A distinctive form of immune thrombocytopenia in a phase 2 study of alemtuzumab for the treatment of relapsing-remitting multiple sclerosis. Blood 118, 6299-6305 (2011).
93. Calabrese, L.H., Molloy, E.S., Huang, D. & Ransohoff, R.M. Progressive multifocal leukoencephalopathy in rheumatic diseases: evolving clinical and pathologic patterns of disease. Arthritis Rheum. 56, 2116-2128 (2007). (Pubitemid 47173558)
94. Barun, B. & Bar-Or, A. Treatment of multiple sclerosis with anti-CD20 antibodies. Clin. Immunol. 142, 31-37 (2012).
95. Kremenchutzky, M., Rice, G.P., Baskerville, J., Wingerchuk, D.M. & Ebers, G.C. The natural history of multiple sclerosis: a geographically based study 9: observations on the progressive phase of the disease. Brain 129, 584-594 (2006). (Pubitemid 43278221)
96. Kappos, L. et al.; European (EU-SPMS) Interferon beta-1b in Secondary Progressive Multiple Sclerosis Trial Steering Committee and Independent Advisory Board; North American (NA-SPMS) Interferon beta-1b in Secondary Progressive Multiple Sclerosis Trial Steering Committee and Independent Advisory Board. Interferon beta-1b in secondary progressive MS: a combined analysis of the two trials. Neurology 63, 1779-1787 (2004). (Pubitemid 39532369)
97. Julian, L. et al.; Network of Pediatric MS Centers of Excellence. Cognitive impairment occurs in children and adolescents with multiple sclerosis: results from a United States network. J. Child Neurol. 28, 102-107 (2013).
98. Chabas, D. et al.; US Network of Pediatric MS Centers of Excellence. Younger children with MS have a distinct CSF inflammatory profile at disease onset. Neurology 74, 399-405 (2010).