Treatment of neuromyelitis optica: State-of-the-art and emerging therapies

Nature Reviews Neurology

Volumn 10, Issue 9, 2014, Pages 493-506

  Papadopoulos, Marios C ^a   Bennett, Jeffrey L ^b   Verkman, Alan S ^c  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; AZATHIOPRINE; BEVACIZUMAB; CD19 ANTIGEN; CETIRIZINE; COMPLEMENT COMPONENT C1S INHIBITOR; CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; CYTOKINE RECEPTOR ANTAGONIST; ECULIZUMAB; FINGOLIMOD; IMMUNOGLOBULIN; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 6; KETOTIFEN; METHOTREXATE; METHYLPREDNISOLONE; MITOXANTRONE; MYCOPHENOLATE MOFETIL; MYCOPHENOLIC ACID; NATALIZUMAB; PREDNISOLONE; RECOMBINANT BETA INTERFERON; RITUXIMAB; SA 237; SIVELESTAT; TOCILIZUMAB; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADD ON THERAPY; ANTIBODY DETECTION; AUTOIMMUNE DISEASE; BLINDNESS; BLOOD BRAIN BARRIER; CARDIOVASCULAR DISEASE; CELL DAMAGE; CELL INFILTRATION; CLINICAL TRIAL (TOPIC); COMPLEMENT DEPENDENT CYTOTOXICITY; DEMYELINATING DISEASE; DIFFERENTIAL DIAGNOSIS; DISEASE EXACERBATION; DRUG EFFICACY; DRUG INDICATION; DRUG MECHANISM; DRUG REPOSITIONING; DRUG SAFETY; DRUG TARGETING; DRUG WITHDRAWAL; EVIDENCE BASED MEDICINE; EXPANDED DISABILITY STATUS SCALE; GRANULOCYTE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INFECTION; INFLAMMATION; LEUKEMIA; LYMPHOCYTE DEPLETION; LYMPHOMA; MACROPHAGE; MULTIPLE CYCLE TREATMENT; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; NONHUMAN; OLIGODENDROGLIA; PARALYSIS; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLASMA EXCHANGE; PREGNANCY; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC DISEASE; UNSPECIFIED SIDE EFFECT;

HUMANS; NEUROMYELITIS OPTICA;

EID: 84908082962     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2014.141     Document Type: Review

References (184)

1. Lennon, V. A. et al. A serum autoantibody marker of neuromyelitis optica: Distinction from multiple sclerosis. Lancet 364, 2106-2112 (2004).
2. Lennon, V. A., Kryzer, T. J., Pittock, S. J., Verkman, A. S. & Hinson, S. R. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J. Exp. Med. 202, 473-477 (2005).
3. Hinson, S. R. et al. Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology 69, 2221-2231 (2007).
4. Wingerchuk, D. M., Lennon, V. A., Pittock, S. J., Lucchinetti, C. F. & Weinshenker, B. G. Revised diagnostic criteria for neuromyelitis optica. Neurology 66, 1485-1489 (2006).
5. Cabre, P. et al. MS and neuromyelitis optica in Martinique (French West Indies). Neurology 56, 507-514 (2001).
6. Cabrera-Gomez, J. A., Kurtzke, J. F., Gonzalez-Quevedo, A. & Lara-Rodriguez, R. An epidemiological study of neuromyelitis optica in Cuba. J. Neurol. 256, 35-44 (2009).
7. Asgari, N. et al. A population-based study of neuromyelitis optica in Caucasians. Neurology 76, 1589-1595 (2011).
8. Banwell, B. et al. Neuromyelitis optica-IgG in childhood inflammatory demyelinating CNS disorders. Neurology 70, 344-352 (2008).
9. Nagaishi, A. et al. Clinical features of neuromyelitis optica in a large Japanese cohort: Comparison between phenotypes. J. Neurol. Neurosurg. Psychiatry 82, 1360-1364 (2011).
10. Jarius, S. et al. Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: A multicentre study of 175 patients. J. Neuroinflammation 9, 14 (2012).
11. Jacob, A. et al. Current concept of neuromyelitis optica (NMO) and NMO spectrum disorders. J. Neurol. Neurosurg. Psychiatry 84, 922-930 (2013).
12. Papadopoulos, M. C. & Verkman, A. S. Aquaporin 4 and neuromyelitis optica. Lancet Neurol. 11, 535-544 (2012).
13. Iyer, A., Elsone, L., Appleton, R. & Jacob, A. A review of the current literature and a guide to the early diagnosis of autoimmune disorders associated with neuromyelitis optica. Autoimmunity 47, 154-161 (2014).
14. Matiello, M. et al. Genetic analysis of aquaporin-4 in neuromyelitis optica. Neurology 77, 1149-1155 (2011).
15. Matsushita, T. et al. Association of the HLA-DPB1∗0501 allele with anti-aquaporin-4 antibody positivity in Japanese patients with idiopathic central nervous system demyelinating disorders. Tissue Antigens 73, 171-176 (2009).
16. Brum, D. G. et al. HLA-DRB association in neuromyelitis optica is different from that observed in multiple sclerosis. Mult. Scler. 16, 21-29 (2010).
17. Deschamps, R. et al. Different HLA class II (DRB1 and DQB1) alleles determine either susceptibility or resistance to NMO and multiple sclerosis among the French Afro-Caribbean population. Mult. Scler. 17, 24-31 (2011).
18. Zephir, H. et al. Is neuromyelitis optica associated with human leukocyte antigen? Mult. Scler. 15, 571-579 (2009).
19. Matiello, M. et al. Familial neuromyelitis optica. Neurology 75, 310-315 (2010).
20. Matsuoka, T. et al. Heterogeneity of aquaporin-4 autoimmunity and spinal cord lesions in multiple sclerosis in Japanese. Brain 130, 1206-1223 (2007).
21. Nakashima, I. et al. Clinical and MRI features of Japanese patients with multiple sclerosis positive for NMO-IgG. J. Neurol. Neurosurg. Psychiatry 77, 1073-1075 (2006).
22. Wu, J. S., Zhang, M. N., Carroll, W. M. & Kermode, A. G. Characterisation of the spectrum of demyelinating disease in Western Australia. J. Neurol. Neurosurg. Psychiatry 79, 1022-1026 (2008).
23. Weinshenker, B. G. & Wingerchuk, D. M. The two faces of neuromyelitis optica. Neurology 82, 466-467 (2014).
24. Jarius, S. & Wildemann, B. AQP4 antibodies in neuromyelitis optica: Diagnostic and pathogenetic relevance. Nat. Rev. Neurol. 6, 383-392 (2010).
25. Jarius, S. et al. Mechanisms of disease: Aquaporin-4 antibodies in neuromyelitis optica. Nat. Clin. Pract. Neurol. 4, 202-214 (2008).
26. Varrin-Doyer, M. et al. Aquaporin 4-specific T cells in neuromyelitis optica exhibit a Th17 bias and recognize Clostridium ABC transporter. Ann. Neurol. 72, 53-64 (2012).
27. Koga, M., Takahashi, T., Kawai, M., Fujihara, K. & Kanda, T. A serological analysis of viral and bacterial infections associated with neuromyelitis optica. J. Neurol. Sci. 300, 19-22 (2011).
28. Shimizu, F. et al. Sera from neuromyelitis optica patients disrupt the blood-brain barrier. J. Neurol. Neurosurg. Psychiatry 83, 288-297 (2012).
29. Jarius, S. et al. Cerebrospinal fluid antibodies to aquaporin-4 in neuromyelitis optica and related disorders: Frequency, origin, and diagnostic relevance. J. Neuroinflammation 7, 52 (2010).
30. Kalluri, S. R. et al. Quantification and functional characterization of antibodies to native aquaporin 4 in neuromyelitis optica. Arch. Neurol. 67, 1201-1208 (2010).
31. Chihara, N. et al. Plasmablasts as migratory IgG-producing cells in the pathogenesis of neuromyelitis optica. PLoS ONE 8, e83036 (2013).
32. Bradl, M. & Lassmann, D. H. Anti-aquaporin-4 antibodies in neuromyelitis optica: How to prove their pathogenetic relevance? Int. MS J. 15, 75-78 (2008).
33. Saadoun, S. et al. Intra-cerebral injection of neuromyelitis optica immunoglobulin G. and human complement produces neuromyelitis optica lesions in mice. Brain 133, 349-361 (2010).
34. Bennett, J. L. et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann. Neurol. 66, 617-629 (2009).
35. Zhang, H., Bennett, J. L. & Verkman, A. S. Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann. Neurol. 70, 943-954 (2011).
36. Ratelade, J. et al. Neuromyelitis optica IgG and natural killer cells produce NMO lesions in mice without myelin loss. Acta Neuropathol. 123, 861-872 (2012).
37. Saadoun, S. et al. Neutrophil protease inhibition reduces neuromyelitis optica-immunoglobulin G-induced damage in mouse brain. Ann. Neurol. 71, 323-333 (2012).
38. Ratelade, J. et al. Involvement of antibody-dependent cell-mediated cytotoxicity in inflammatory demyelination in a mouse model of neuromyelitis optica. Acta Neuropathol. 126, 699-709 (2013).
39. Wrzos, C. et al. Early loss of oligodendrocytes in human and experimental neuromyelitis optica lesions. Acta Neuropathol. 127, 523-538 (2014).
40. Pohl, M. et al. T cell-activation in neuromyelitis optica lesions plays a role in their formation. Acta Neuropathol. Commun. 1, 85 (2013).
41. Saadoun, S., Bridges, L. R., Verkman, A. S. & Papadopoulos, M. C. Paucity of natural killer and cytotoxic T cells in human neuromyelitis optica lesions. Neuroreport 23, 1044-1047 (2012).
42. Saadoun, S. et al. T cell deficiency does not reduce lesions in mice produced by intracerebral injection of NMO-IgG and complement. J. Neuroimmunol. 235, 27-32 (2011).
43. Hinson, S. R. et al. Aquaporin-4-binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by down-regulating EAAT2. J. Exp. Med. 205, 2473-2481 (2008).
44. Hinson, S. R. et al. Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc. Natl Acad. Sci. USA 109, 1245-1250 (2012).
45. Rossi, A., Ratelade, J., Papadopoulos, M. C., Bennett, J. L. & Verkman, A. S. Neuromyelitis optica IgG does not alter aquaporin-4 water permeability, plasma membrane M1/M23 isoform content, or supramolecular assembly. Glia 60, 2027-2039 (2012).
46. Ratelade, J., Bennett, J. L. & Verkman, A. S. Evidence against cellular internalization in vivo of NMO-IgG, aquaporin-4, and excitatory amino acid transporter 2 in neuromyelitis optica. J. Biol. Chem. 286, 45156-45164 (2011).
47. Faulkner, J. R. et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24, 2143-2155 (2004).
48. Voskuhl, R. R. et al. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J. Neurosci. 29, 11511-11522 (2009).
49. Trebst, C. et al. Update on the diagnosis and treatment of neuromyelitis optica: Recommendations of the Neuromyelitis Optica Study Group (NEMOS). J. Neurol. 261, 1-16 (2014).
50. Kimbrough, D. J. et al. Treatment of neuromyelitis optica: Review and recommendations. Mult. Scler. Relat. Disord. 1, 180-187 (2012).
51. Wingerchuk, D. M., Pittock, S. J., Lucchinetti, C. F., Lennon, V. A. & Weinshenker, B. G. A secondary progressive clinical course is uncommon in neuromyelitis optica. Neurology 68, 603-605 (2007).
52. Barnes, P. J. Corticosteroids: The drugs to beat. Eur. J. Pharmacol. 533, 2-14 (2006).
53. Linhares, U. C. et al. The ex vivo production of IL-6 and IL-21 by CD4+ T cells is directly associated with neurological disability in neuromyelitis optica patients. J. Clin. Immunol. 33, 179-189 (2013).
54. Wang, H. H. et al. Interleukin-17-secreting T cells in neuromyelitis optica and multiple sclerosis during relapse. J. Clin. Neurosci. 18, 1313-1317 (2011).
55. Muls, N. et al. Upregulation of IL-17, but not of IL-9, in circulating cells of CIS and relapsing MS patients. Impact of corticosteroid therapy on the cytokine network. J. Neuroimmunol. 243, 73-80 (2012).
56. Reeves, H. M. & Winters, J. L. The mechanisms of action of plasma exchange. Br. J. Haematol. 164, 342-351 (2014).
57. Bonnan, M. & Cabre, P. Plasma exchange in severe attacks of neuromyelitis optica. Mult. Scler. Int. 2012, 787630 (2012).
58. Bonnan, M. et al. Plasma exchange in severe spinal attacks associated with neuromyelitis optica spectrum disorder. Mult. Scler. 15, 487-492 (2009).
59. Keegan, M. et al. Plasma exchange for severe attacks of CNS demyelination: Predictors of response. Neurology 58, 143-146 (2002).
60. Merle, H. et al. Treatment of optic neuritis by plasma exchange (add-on) in neuromyelitis optica. Arch. Ophthalmol. 130, 858-862 (2012).
61. Elsone, L. et al. Role of intravenous immunoglobulin in the treatment of acute relapses of neuromyelitis optica: Experience in 10 patients. Mult. Scler. 20, 501-504 (2014).
62. Greenberg, B. M. et al. Idiopathic transverse myelitis: Corticosteroids, plasma exchange, or cyclophosphamide. Neurology 68, 1614-1617 (2007).
63. Kitley, J. et al. Prognostic factors and disease course in aquaporin-4 antibody-positive patients with neuromyelitis optica spectrum disorder from the United Kingdom and Japan. Brain 135, 1834-1849 (2012).
64. Watanabe, S. et al. Low-dose corticosteroids reduce relapses in neuromyelitis optica: A retrospective analysis. Mult. Scler. 13, 968-974 (2007).
65. Miyamoto, K. & Kusunoki, S. Intermittent plasmapheresis prevents recurrence in neuromyelitis optica. Ther. Apher. Dial. 13, 505-508 (2009).
66. Costanzi, C. et al. Azathioprine: Tolerability, efficacy, and predictors of benefit in neuromyelitis optica. Neurology 77, 659-666 (2011).
67. Bichuetti, D. B., Lobato de Oliveira, E. M., Oliveira, D. M., Amorin de Souza, N. & Gabbai, A. A. Neuromyelitis optica treatment: Analysis of 36 patients. Arch. Neurol. 67, 1131-1136 (2010).
68. Sahraian, M. A., Moinfar, Z., Khorramnia, S. & Ebrahim, M. M. Relapsing neuromyelitis optica: Demographic and clinical features in Iranian patients. Eur. J. Neurol. 17, 794-799 (2010).
69. Jacob, A. et al. Treatment of neuromyelitis optica with mycophenolate mofetil: Retrospective analysis of 24 patients. Arch. Neurol. 66, 1128-1133 (2009).
70. Kitley, J. et al. Methotrexate is an alternative to azathioprine in neuromyelitis optica spectrum disorders with aquaporin-4 antibodies. J. Neurol. Neurosurg. Psychiatry 84, 918-921 (2013).
71. Kim, S.-H. et al. Efficacy and safety of mitoxantrone in patients with highly relapsing neuromyelitis optica. Arch. Neurol. 68, 473-479 (2010).
72. Yaguchi, H. et al. Efficacy of intravenous cyclophosphamide therapy for neuromyelitis optica spectrum disorder. Intern. Med. 52, 969-972 (2013).
73. Bichuetti, D. B., Oliveira, E. M., Boulos Fde, C. & Gabbai, A. A. Lack of response to pulse cyclophosphamide in neuromyelitis optica: Evaluation of 7 patients. Arch. Neurol. 69, 938-939 (2012).
74. Cree, B. A. et al. An open label study of the effects of rituximab in neuromyelitis optica. Neurology 64, 1270-1272 (2005).
75. Jacob, A. et al. Treatment of neuromyelitis optica with rituximab: Retrospective analysis of 25 patients. Arch. Neurol. 65, 1443-1448 (2008).
76. Kim, S.-H., Kim, W., Li, X. F., Jung, I.-J. & Kim, H. J. Repeated treatment with rituximab based on the assessment of peripheral circulating memory B cells in patients with relapsing neuromyelitis optica over 2 years. Arch. Neurol. 68, 1412-1420 (2011).
77. Bedi, G. S. et al. Impact of rituximab on relapse rate and disability in neuromyelitis optica. Mult. Scler. 17, 1225-1230 (2011).
78. Kim, S.-H., Huh, S.-Y., Lee, S. J., Joung, A. & Kim, H. J. A 5-year follow-up of rituximab treatment in patients with neuromyelitis optica spectrum disorder. JAMA Neurol. 70, 1110-1117 (2013).
79. Greenberg, B. M. et al. Rituximab dosing and monitoring strategies in neuromyelitis optica patients: Creating strategies for therapeutic success. Mult. Scler. 18, 1022-1026 (2012).
80. Jarius, S. et al. Antibody to aquaporin-4 in the long-term course of neuromyelitis optica. Brain 131, 3072-3080 (2008).
81. Pellkofer, H. L. et al. Long-term follow-up of patients with neuromyelitis optica after repeated therapy with rituximab. Neurology 76, 1310-1315 (2011).
82. Kim, S. H., Huh, S. Y., Lee, S. J., Joung, A. & Kim, H. J. A 5-year follow-up of rituximab treatment in patients with neuromyelitis optica spectrum disorder. JAMA Neurol. 70, 1110-1117 (2013).
83. Carson, K. R. et al. Monoclonal antibody-associated progressive multifocal leucoencephalopathy in patients treated with rituximab, natalizumab, and efalizumab: A Review from the Research on Adverse Drug Events and Reports (RADAR) Project. Lancet Oncol. 10, 816-824 (2009).
84. Kageyama, T. et al. Combination of cyclosporine A with corticosteroids is effective for the treatment of neuromyelitis optica. J. Neurol. 260, 627-634 (2013).
85. Bourre, B. et al. Neuromyelitis optica and pregnancy. Neurology 78, 875-879 (2012).
86. Kim, W. et al. Influence of pregnancy on neuromyelitis optica spectrum disorder. Neurology 78, 1264-1267 (2012).
87. Ringelstein, M. et al. Neuromyelitis optica and pregnancy during therapeutic B cell depletion: Infant exposure to anti-AQP4 antibody and prevention of rebound relapses with low-dose rituximab postpartum. Mult. Scler. 19, 1544-1547 (2013).
88. Wen, H. et al. Ontogeny of water transport in rat brain: Postnatal expression of the aquaporin-4 water channel. Eur. J. Neurosci. 11, 935-945 (1999).
89. Gomori, E. et al. Fetal development of membrane water channel proteins aquaporin-1 and aquaporin-4 in the human brain. Int. J. Dev. Neurosci. 24, 295-305 (2006).
90. Saadoun, S. et al. Neuromyelitis optica IgG causes placental inflammation and fetal death. J. Immunol. 191, 2999-3005 (2013).
91. Damiano, A. E. Review: Water channel proteins in the human placenta and fetal membranes. Placenta 32 (Suppl. 2), S207-S211 (2011).
92. De Falco, M. et al. Down-regulation of aquaporin 4 in human placenta throughout pregnancy. In Vivo 21, 813-817 (2007).
93. Reuss, R. et al. A woman with acute myelopathy in pregnancy: Case outcome. BMJ 339, b4026 (2009).
94. Fragoso, Y. D. et al. Neuromyelitis optica and pregnancy. J. Neurol. 260, 2614-2619 (2013).
95. Pellkofer, H. L., Suessmair, C., Schulze, A., Hohlfeld, R. & Kuempfel, T. Course of neuromyelitis optica during inadvertent pregnancy in a patient treated with rituximab. Mult. Scler. 15, 1006-1008 (2009).
96. Yuksel, D., Senbil, N., Yilmaz, D. & Yavuz Gurer, Y. K. Devic's neuromyelitis optica in an infant case. J. Child. Neurol. 22, 1143-1146 (2007).
97. Tillema, J. M. & McKeon, A. The spectrum of neuromyelitis optica (NMO) in childhood. J. Child. Neurol. 27, 1437-1447 (2012).
98. McKeon, A. et al. CNS aquaporin-4 autoimmunity in children. Neurology 71, 93-100 (2008).
99. Lotze, T. E. et al. Spectrum of pediatric neuromyelitis optica. Pediatrics 122, e1039-e1047 (2008).
100. Huppke, P. et al. Neuromyelitis optica and NMO-IgG in European pediatric patients. Neurology 75, 1740-1804 (2010).
101. Kim, S.-H., Kim, W., Li, X. F., Jung, I.-J. & Kim, H. J. Does interferon beta treatment exacerbate neuromyelitis optica spectrum disorder? Mult. Scler. 18, 1480-1483 (2012).
102. Palace, J., Leite, M. I., Nairne, A. & Vincent, A. Interferon beta treatment in neuromyelitis optica: Increase in relapses and aquaporin 4 antibody titers. Arch. Neurol. 67, 1016-1017 (2010).
103. Shimizu, J. et al. IFNβ-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 75, 1423-1427 (2010).
104. Warabi, Y., Matsumoto, Y. & Hayashi, H. Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J. Neurol. Sci. 252, 57-61 (2007).
105. Axtell, R. C., Raman, C. & Steinman, L. Type I interferons: Beneficial in Th1 and detrimental in Th17 autoimmunity. Clin. Rev. Allergy Immunol. 44, 114-120 (2012).
106. Kleiter, I. et al. Failure of natalizumab to prevent relapses in neuromyelitis optica. Arch. Neurol. 69, 239-245 (2012).
107. Barnett, M., Prineas, J., Buckland, M., Parratt, J. & Pollard, J. Massive astrocyte destruction in neuromyelitis optica despite natalizumab therapy. Mult. Scler. 18, 108-112 (2012).
108. Kitley, J. et al. Catastrophic brain relapse in seronegative NMO after a single dose of natalizumab. J. Neurol. Sci. 339, 223-225 (2014).
109. Kleiter, I. et al. Failure of natalizumab to prevent relapses in neuromyelitis optica. Arch. Neurol. 69, 239-245 (2012).
110. Polman, C. H. et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med. 354, 899-910 (2006).
111. Lucchinetti, C. F. et al. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125, 1450-1461 (2002).
112. Zhang, H. & Verkman, A. S. Eosinophil pathogenicity mechanisms and therapeutics in neuromyelitis optica. J. Clin. Invest. 123, 2306-2316 (2013).
113. Chu, V. T. et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12, 151-159 (2011).
114. Min, J. H., Kim, B. J. & Lee, K. H. Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult. Scler. 18, 113-115 (2012).
115. Izaki, S. et al. A case of neuromyelitis optica spectrum disorder developing a fulminant course with multiple white-matter lesions following fingolimod treatment [Japanese]. Rinsho Shinkeigaku 53, 513-517 (2013).
116. Sugita, K. et al. FTY720 regulates bone marrow egress of eosinophils and modulates late-phase skin reaction in mice. Am. J. Pathol. 177, 1881-1887 (2010).
117. Pittock, S. J. et al. Eculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: An open-label pilot study. Lancet Neurol. 12, 554-562 (2013).
118. Chihara, N. et al. Interleukin 6 signaling promotes anti-aquaporin 4 autoantibody production from plasmablasts in neuromyelitis optica. Proc. Natl Acad. Sci. USA 108, 3701-3706 (2011).
119. Uzawa, A. et al. Cerebrospinal fluid interleukin-6 and glial fibrillary acidic protein levels are increased during initial neuromyelitis optica attacks. Clin. Chim. Acta 421, 181-183 (2013).
120. Wang, H. et al. Notable increased cerebrospinal fluid levels of soluble interleukin-6 receptors in neuromyelitis optica. Neuroimmunomodulation 19, 304-308 (2012).
121. Araki, M. et al. Clinical improvement in a patient with neuromyelitis optica following therapy with the anti-IL-6 receptor monoclonal antibody tocilizumab. Mod. Rheumatol 23, 827-831 (2013).
122. Ayzenberg, I. et al. Interleukin 6 receptor blockade in patients with neuromyelitis optica nonresponsive to anti-CD20 therapy. JAMA Neurol. 70, 394-397 (2013).
123. Kieseier, B. C. et al. Disease amelioration with tocilizumab in a treatment-resistant patient with neuromyelitis optica: Implication for cellular immune responses. JAMA Neurol. 70, 390-393 (2013).
124. Komai, T. et al. Neuromyelitis optica spectrum disorder complicated with Sjogren syndrome successfully treated with tocilizumab: A case report. Mod. Rheumatol http://dx.doi.org/10.3109/14397595.2013.861333.
125. Asavapanumas, N., Ratelade, J. & Verkman, A. S. Unique neuromyelitis optica pathology produced in naive rats by intracerebral administration of NMO-IgG. Acta Neuropathol. 127, 539-551 (2014).
126. Jarius, S. et al. Cerebrospinal fluid findings in aquaporin-4 antibody positive neuromyelitis optica: Results from 211 lumbar punctures. J. Neurol. Sci. 306, 82-90 (2011).
127. Jacob, A. et al. Detrimental role of granulocyte-colony stimulating factor in neuromyelitis optica: Clinical case and histological evidence. Mult. Scler. 18, 1801-1803 (2012).
128. Young, R. E. et al. Neutrophil elastase (NE)-deficient mice demonstrate a nonredundant role for NE in neutrophil migration, generation of proinflammatory mediators, and phagocytosis in response to zymosan particles in vivo. J. Immunol. 172, 4493-4502 (2004).
129. Papayannopoulos, V., Metzler, K. D., Hakkim, A. & Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191, 677-691 (2010).
130. Iwata, K. et al. Effect of neutrophil elastase inhibitor (sivelestat sodium) in the treatment of acute lung injury (ALI) and acute respiratory distress syndrome (ARDS): A systematic review and meta-analysis. Intern. Med. 49, 2423-2432 (2010).
131. Kawabata, K. et al. ONO-5046, a novel inhibitor of human neutrophil elastase. Biochem. Biophys. Res. Commun. 177, 814-820 (1991).
132. Kita, H. Eosinophils: Multifaceted biological properties and roles in health and disease. Immunol. Rev. 242, 161-177 (2011).
133. Imbach, P. et al. High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet 1, 1228-1231 (1981).
134. Gelfand, E. W. Intravenous immune globulin in autoimmune and inflammatory diseases. N. Engl. J. Med. 367, 2015-2025 (2012).
135. Jacob, S. & Rajabally, Y. A. Current proposed mechanisms of action of intravenous immunoglobulins in inflammatory neuropathies. Curr. Neuropharmacol. 7, 337-342 (2009).
136. Magraner, M. J., Coret, F. & Casanova, B. The effect of intravenous immunoglobulin on neuromyelitis optica. Neurologia 28, 65-72 (2013).
137. Bakker, J. & Metz, L. Devic's neuromyelitis optica treated with intravenous gamma globulin (IVIG). Can. J. Neurol. Sci. 31, 265-267 (2004).
138. Okada, K., Tsuji, S. & Tanaka, K. Intermittent intravenous immunoglobulin successfully prevents relapses of neuromyelitis optica. Intern. Med. 46, 1671-1672 (2007).
139. Ratelade, J., Smith, A. J. & Verkman, A. S. Intravenous immunoglobulin (IVIg) reduces the pathogenicity of aquaporin-4 autoantibodies in neuromyelitis optica. Exp. Neurol. 255, 145-153 (2014).
140. Tedder, T. F. CD19: A promising B cell target for rheumatoid arthritis. Nat. Rev. Rheumatol. 5, 572-577 (2009).
141. Hammer, O. CD19 as an attractive target for antibody-based therapy. MAbs 4, 571-577 (2012).
142. Kim, S., Steelman, A. J., Koito, H. & Li, J. Astrocytes promote TNF-mediated toxicity to oligodendrocyte precursors. J. Neurochem. 116, 53-66 (2011).
143. Pentsn-Rol, G. et al. TNF-α and IL-10 downregulation and marked oxidative stress in neuromyelitis optica. J. Inflamm. (Lond.) 6, 18 (2009).
144. Tradtrantip, L. et al. Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. Ann. Neurol. 71, 314-322 (2012).
145. Tradtrantip, L. et al. Small-molecule inhibitors of NMO-IgG binding to aquaporin-4 reduce astrocyte cytotoxicity in neuromyelitis optica. FASEB J. 26, 2197-2208 (2012).
146. Phuan, P. W. et al. A small-molecule screen yields idiotype-specific blockers of neuromyelitis optica immunoglobulin G binding to aquaporin-4. J. Biol. Chem. 287, 36837-36844 (2012).
147. Crane, J. M. et al. Binding affinity and specificity of neuromyelitis optica autoantibodies to aquaporin-4 M1/M23 isoforms and orthogonal arrays. J. Biol. Chem. 286, 16516-16524 (2011).
148. Phuan, P. W., Ratelade, J., Rossi, A., Tradtrantip, L. & Verkman, A. S. Complement-dependent cytotoxicity in neuromyelitis optica requires aquaporin-4 protein assembly in orthogonal arrays. J. Biol. Chem. 287, 13829-13839 (2012).
149. Jarius, S. & Wildemann, B. Aquaporin-4 antibodies, CNS acidosis and neuromyelitis optica: A potential link. Med. Hypotheses 81, 1090-1095 (2013).
150. Warth, A. Prevention of orthogonal array of particles formation as a treatment approach for neuromyelitis optica. Med. Hypotheses 73, 361-362 (2009).
151. Collin, M. & Olsen, A. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 20, 3046-3055 (2001).
152. Tradtrantip, L., Ratelade, J., Zhang, H. & Verkman, A. S. Enzymatic deglycosylation converts pathogenic neuromyelitis optica anti-aquaporin-4 immunoglobulin G. into therapeutic antibody. Ann. Neurol. 73, 77-85 (2013).
153. Tradtrantip, L., Asavapanumas, N. & Verkman, A. S. Therapeutic cleavage of anti-aquaporin-4 autoantibody in neuromyelitis optica by an IgG-selective proteinase. Mol. Pharmacol. 83, 1268-1275 (2013).
154. Lewis, L. A. & Ram, S. Meningococcal disease and the complement system. Virulence 5, 98-126 (2014).
155. Phuan, P. W. et al. C1q-targeted monoclonal antibody prevents complement-dependent cytotoxicity and neuropathology in in vitro and mouse models of neuromyelitis optica. Acta Neuropathol. 125, 829-840 (2013).
156. Ricklin, D. & Lambris, J. D. Complement-targeted therapeutics. Nat. Biotechnol. 25, 1265-1275 (2007).
157. Ricklin, D. & Lambris, J. D. Progress and trends in complement therapeutics. Adv. Exp. Med. Biol. 735, 1-22 (2013).
158. Davies, A. & Lachmann, P. J. Membrane defence against complement lysis: The structure and biological properties of CD59. Immunol. Res. 12, 258-275 (1993).
159. Zipfel, P. F. & Skerka, C. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729-740 (2009).
160. Botto, M. et al. Complement in human diseases: Lessons from complement deficiencies. Mol. Immunol. 46, 2774-2783 (2009).
161. Asavapanumas, N. et al. Experimental mouse model of optic neuritis with inflammatory demyelination produced by passive transfer of neuromyelitis optica-immunoglobulin G. J. Neuroinflammation 11, 16 (2014).
162. Zhang, H. & Verkman, A. S. Longitudinally extensive NMO spinal cord pathology produced by passive transfer of NMO-IgG in mice lacking complement inhibitor CD59. J. Autoimmun. http://dx.doi.org/10.1016/j.jaut.2014.02.011.
163. Vincent, T. et al. Functional consequences of neuromyelitis optica-IgG astrocyte interactions on blood-brain barrier permeability and granulocyte recruitment. J. Immunol. 181, 5730-5737 (2008).
164. Mihai, S. & Nimmerjahn, F. The role of Fc receptors and complement in autoimmunity. Autoimmun. Rev. 12, 657-660 (2013).
165. Hosokawa, T. et al. Increased serum matrix metalloproteinase-9 in neuromyelitis optica: Implication of disruption of blood-brain barrier. J. Neuroimmunol. 236, 81-86 (2011).
166. Bluestone, J. A. & Bour-Jordan, H. Current and future immunomodulation strategies to restore tolerance in autoimmune diseases. Cold Spring Harb. Perspect. Biol. 4 (2012).
167. Bar-Or, A. et al. Induction of antigen-specific tolerance in multiple sclerosis after immunization with DNA encoding myelin basic protein in a randomized, placebo-controlled phase 1/2 trial. Arch. Neurol. 64, 1407-1415 (2007).
168. Faria, A. M. C. & Weiner, H. L. Oral tolerance: Therapeutic implications for autoimmune diseases. Clin. Dev. Immunol. 13, 143-157 (2006).
169. Bielekova, B. et al. Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: Results of a phase II clinical trial with an altered peptide ligand. Nat. Med. 6, 1167-1175 (2000).
170. Fagius, J., Lundgren, J. & Oberg, G. Early highly aggressive MS successfully treated by hematopoietic stem cell transplantation. Mult. Scler. 15, 229-237 (2008).
171. Illei, G. G. et al. Current state and future directions of autologous hematopoietic stem cell transplantation in systemic lupus erythematosus. Ann. Rheum. Dis. 70, 2071-2074 (2011).
172. Mader, S. et al. Complement activating antibodies to myelin oligodendrocyte glycoprotein in neuromyelitis optica and related disorders. J. Neuroinflammation 8, 184 (2011).
173. Kitley, J. et al. Longitudinally extensive transverse myelitis with and without aquaporin 4 antibodies. JAMA Neurol. 70, 1375-1381 (2013).
174. Kitley, J. et al. Neuromyelitis optica spectrum disorders with aquaporin-4 and myelin-oligodendrocyte glycoprotein antibodies: A comparative study. JAMA Neurol. 71, 276-283 (2014).
175. Kitley, J. et al. Myelin-oligodendrocyte glycoprotein antibodies in adults with a neuromyelitis optica phenotype. Neurology 79, 1273-1277 (2012).
176. Rostasy, K. et al. Persisting myelin oligodendrocyte glycoprotein antibodies in aquaporin-4 antibody negative pediatric neuromyelitis optica. Mult. Scler. 19, 1052-1059 (2013).
177. Sato, D. K. et al. Distinction between MOG antibody-positive and AQP4 antibody-positive NMO spectrum disorders. Neurology 82, 474-481 (2014).
178. Reindl, M., Di Pauli, F., Rostasy, K. & Berger, T. The spectrum of MOG autoantibody-associated demyelinating diseases. Nat. Rev. Neurol. 9, 455-461 (2013).
179. Saadoun, S. et al. Neuromyelitis optica MOG-IgG causes reversible lesions in mouse brain. Acta Neuropathol. Commun. 2, 35 (2014).
180. Mealy, M. A., Wingerchuk, D. M., Palace, J., Greenberg, B. M. & Levy, M. Comparison of relapse and treatment failure rates among patients with neuromyelitis optica: Multicenter study of treatment efficacy. JAMA Neurol. 71, 324-330 (2014).
181. Pellkofer, H. L. et al. Long-term follow-up of patients with neuromyelitis optica after repeated therapy with rituximab. Neurology 76, 1310-1315 (2011).
182. Weinstock-Guttman, B. et al. Study of mitoxantrone for the treatment of recurrent neuromyelitis optica (Devic disease). Arch. Neurol. 63, 957-963 (2006).
183. Li, Y., Wang, H., Long, Y., Lu, Z. & Hu, X. Increased memory Th17 cells in patients with neuromyelitis optica and multiple sclerosis. J. Neuroimmunol. 234, 155-160 (2011).
184. Raveendra, B. L. et al. Discovery of peptoid ligands for anti-aquaporin 4 antibodies. Chem. Biol. 20, 351-359 (2013).