Anti-B-Cell Therapies in Autoimmune Neurological Diseases: Rationale and Efficacy Trials

Neurotherapeutics

Volumn 13, Issue 1, 2016, Pages 20-33

  Alexopoulos, Harry ^a   Biba, Angie ^a   Dalakas, Marinos C ^b  

^a UNIVERSITY OF ATHENS   (Greece)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

autoantibodies; autoimmunity; B cells; monoclonal antibodies; neurological disorders; rituximab

Indexed keywords

B CELL ACTIVATING FACTOR; B CELL MATURATION ANTIGEN; B LYMPHOCYTE ANTIBODY; CD19 ANTIGEN; CD20 ANTIGEN; CD27 ANTIGEN; CXCL13 CHEMOKINE; EARLY ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HYBRID PROTEIN; IMMUNOGLOBULIN LIGHT CHAIN; LIGAND; STROMAL CELL DERIVED FACTOR 1; SYNDECAN 1; TUMOR NECROSIS FACTOR ALPHA;

ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTATION; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BRAIN DISEASE; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CHRONIC INFLAMMATORY DEMYELINATING POLYNEUROPATHY; CYTOKINE PRODUCTION; DEMYELINATING NEUROPATHY; EXPANDED DISABILITY STATUS SCALE; GUILLAIN BARRE SYNDROME; HUMAN; HUMORAL IMMUNE DEFICIENCY; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY CELL; MULTICENTER STUDY (TOPIC); MULTIPLE SCLEROSIS; MYOSITIS; NEUROLOGIC DISEASE; OVARY FOLLICLE CELL; PATHOGENESIS; PHASE 2 CLINICAL TRIAL (TOPIC); PLASMABLAST; PLASMAPHERESIS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; REVIEW; SOMATIC HYPERMUTATION; T LYMPHOCYTE ACTIVATION; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLASMA CELL;

AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; B-LYMPHOCYTES; B-LYMPHOCYTES, REGULATORY; CLINICAL TRIALS AS TOPIC; HUMANS; PLASMA CELLS;

EID: 84955411826     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-015-0402-6     Document Type: Review

References (155)

1. Eibel H, Kraus H, Sic H, Kienzler AK, Rizzi M. B cell biology: an overview. Curr Allergy Asthma Rep 2014;14:434.
2. Pieper K, Grimbacher B, Eibel H. B-cell biology and development. J Allergy Clin Immunol 2013;131:959-971.
3. Weinstein E, Peeva E, Putterman C, Diamond B. B-cell biology. Rheum Dis Clin North Am 2004;30:159-174.
4. Kitano M, Moriyama S, Ando Y, et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 2011;34:961-972.
5. O’Connor BP, Vogel LA, Zhang W, et al. Imprinting the fate of antigen-reactive B cells through the affinity of the B cell receptor. J Immunol 2006;177:7723-7732.
6. Kurosaki T, Kometani K, Ise W. Memory B cells. Nat Rev Immunol 2015;15:149-159.
7. Nutt SL, Hodgkin PD, Tarlinton DM, Corcoran LM. The generation of antibody-secreting plasma cells. Nat Rev Immunol 2015;15:160-171.
8. Anolik JH, Barnard J, Owen T, et al. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum 2007;56:3044-3056.
9. Dass S, Rawstron AC, Vital EM, Henshaw K, McGonagle D, Emery P. Highly sensitive B cell analysis predicts response to rituximab therapy in rheumatoid arthritis. Arthritis Rheum 2008;58:2993-2999.
10. Palanichamy A, Barnard J, Zheng B, et al. Novel human transitional B cell populations revealed by B cell depletion therapy. J Immunol 2009;182:5982-5993.
11. Roll P, Dorner T, Tony HP. Anti-CD20 therapy in patients with rheumatoid arthritis: predictors of response and B cell subset regeneration after repeated treatment. Arthritis Rheum 2008;58:1566-1575.
12. Adlowitz DG, Barnard J, Biear JN, et al. Expansion of activated peripheral blood memory B cells in rheumatoid arthritis, impact of B cell depletion therapy, and biomarkers of response. PLoS One 2015;10:e0128269.
13. Moore PA, Belvedere O, Orr A, et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 1999;285:260-263.
14. Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med 1999;189:1747-1756.
15. Hahne M, Kataoka T, Schroter M, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med 1998;188:1185-1190.
16. Cachero TG, Schwartz IM, Qian F, et al. Formation of virus-like clusters is an intrinsic property of the tumor necrosis factor family member BAFF (B cell activating factor). Biochemistry 2006;45:2006-2013.
17. Liu Y, Xu L, Opalka N, Kappler J, Shu HB, Zhang G. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 2002;108:383-394.
18. Lopez-Fraga M, Fernandez R, Albar JP, Hahne M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep 2001;2:945-951.
19. Lavie F, Miceli-Richard C, Ittah M, Sellam J, Gottenberg JE, Mariette X. B-cell activating factor of the tumour necrosis factor family expression in blood monocytes and T cells from patients with primary Sjogren’s syndrome. Scand J Immunol 2008;67:185-192.
20. Moreaux J, Legouffe E, Jourdan E, et al. BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood 2004;103:3148-3157.
21. Suzuki K, Setoyama Y, Yoshimoto K, Tsuzaka K, Abe T, Takeuchi T. Effect of interleukin-2 on synthesis of B cell activating factor belonging to the tumor necrosis factor family (BAFF) in human peripheral blood mononuclear cells. Cytokine 2008;44:44-48.
22. Bossen C, Cachero TG, Tardivel A, et al. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 2008;111:1004-1012.
23. Day ES, Cachero TG, Qian F, et al. Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry 2005;44:1919-1931.
24. Zhang L, Zheng S, Wu H, et al. Identification of BLyS (B lymphocyte stimulator), a non-myelin-associated protein, as a functional ligand for Nogo-66 receptor. J Neurosci 2009;29:6348-6352.
25. Ingold K, Zumsteg A, Tardivel A, et al. Identification of proteoglycans as the APRIL-specific binding partners. J Exp Med 2005;201:1375-1383.
26. Mihalcik SA, Huddleston PM, 3rd, Wu X, Jelinek DF. The structure of the TNFRSF13C promoter enables differential expression of BAFF-R during B cell ontogeny and terminal differentiation. J Immunol 2010;185:1045-1054.
27. Yan M, Brady JR, Chan B, et al. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr Biol 2001;11:1547-1552.
28. Lougaris V, Gallizzi R, Vitali M, et al. A novel compound heterozygous TACI mutation in an autosomal recessive common variable immunodeficiency (CVID) family. Hum Immunol 2012;73:836-839.
29. Martinez-Gallo M, Radigan L, Almejun MB, Martinez-Pomar N, Matamoros N, Cunningham-Rundles C. TACI mutations and impaired B-cell function in subjects with CVID and healthy heterozygotes. J Allergy Clin Immunol 2013;131:468-476.
30. O’Connor BP, Raman VS, Erickson LD, et al. BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med 2004;199:91-98.
31. Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity 2015;42:607-612.
32. van de Veen W, Stanic B, Yaman G, et al. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol 2013;131:1204-1212.
33. Mauri C, Menon M. The expanding family of regulatory B cells. Int Immunol 2015;27:479-486.
34. Duddy M, Niino M, Adatia F, et al. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol 2007;178:6092-6099.
35. Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014;507:366-370.
36. Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011;117:530-541.
37. Miyagaki T, Fujimoto M, Sato S. Regulatory B cells in human inflammatory and autoimmune diseases: from mouse models to clinical research. Int Immunol 2015;27:495-504.
38. Tussiwand R, Bosco N, Ceredig R, Rolink AG. Tolerance checkpoints in B-cell development: Johnny B good. Eur J Immunol 2009;39:2317-2324.
39. Dalakas MC. B cells as therapeutic targets in autoimmune neurological disorders. Nat Clin Pract Neurol 2008;4:557-567.
40. Frischer JM, Bramow S, Dal-Bianco A, et al. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 2009;132:1175-1189.
41. Ozawa K, Suchanek G, Breitschopf H, et al. Patterns of oligodendroglia pathology in multiple sclerosis. Brain 1994;117:1311-1322.
42. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol 2015;15:545-558.
43. Corcione A, Casazza S, Ferretti E, et al. Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis. Proc Natl Acad Sci U S A 2004;101:11064-11069.
44. Harp CT, Ireland S, Davis LS, et al. Memory B cells from a subset of treatment-naive relapsing-remitting multiple sclerosis patients elicit CD4(+) T-cell proliferation and IFN-gamma production in response to myelin basic protein and myelin oligodendrocyte glycoprotein. Eur J Immunol 2010;40:2942-2956.
45. Niino M, Hirotani M, Miyazaki Y, Sasaki H. Memory and naive B-cell subsets in patients with multiple sclerosis. Neurosci Lett 2009;464:74-78.
46. Habib J, Deng J, Lava N, Tyor W, Galipeau J. Blood B cell and regulatory subset content in multiple sclerosis patients. J Mult Scler (Foster City) 2015;2.
47. Knippenberg S, Peelen E, Smolders J, et al. Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J Neuroimmunol 2011;239:80-86.
48. Michel L, Chesneau M, Manceau P, et al. Unaltered regulatory B-cell frequency and function in patients with multiple sclerosis. Clin Immunol 2014;155:198-208.
49. Quan C, Yu H, Qiao J, et al. Impaired regulatory function and enhanced intrathecal activation of B cells in neuromyelitis optica: distinct from multiple sclerosis. Mult Scler 2013;19:289-298.
50. Hirotani M, Niino M, Fukazawa T, et al. Decreased IL-10 production mediated by Toll-like receptor 9 in B cells in multiple sclerosis. J Neuroimmunol 2010;221:95-100.
51. Quan C, ZhangBao J, Lu J, et al. The immune balance between memory and regulatory B cells in NMO and the changes of the balance after methylprednisolone or rituximab therapy. J Neuroimmunol 2015;282:45-53.
52. Myers KJ, Sprent J, Dougherty JP, Ron Y. Synergy between encephalitogenic T cells and myelin basic protein-specific antibodies in the induction of experimental autoimmune encephalomyelitis. J Neuroimmunol 1992;41:1-8.
53. Willenborg DO, Prowse SJ. Immunoglobulin-deficient rats fail to develop experimental allergic encephalomyelitis. J Neuroimmunol 1983;5:99-109.
54. Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol 2010;185:2240-2252.
55. Brilot F, Dale RC, Selter RC, et al. Antibodies to native myelin oligodendrocyte glycoprotein in children with inflammatory demyelinating central nervous system disease. Ann Neurol 2009;66:833-842.
56. Chalmoukou K, Alexopoulos H, Akrivou S, Stathopoulos P, Reindl M, Dalakas MC. Anti-MOG antibodies are frequently associated with steroid-sensitive recurrent optic neuritis. Neurol Neuroimmunol Neuroinflamm 2015;2:e131.
57. Waters P, Woodhall M, O’Connor KC, et al. MOG cell-based assay detects non-MS patients with inflammatory neurologic disease. Neurol Neuroimmunol Neuroinflamm 2015;2:e89.
58. Wang H, Wang K, Zhong X, et al. Cerebrospinal fluid BAFF and APRIL levels in neuromyelitis optica and multiple sclerosis patients during relapse. J Clin Immunol 2012;32:1007-1011.
59. Krumbholz M, Faber H, Steinmeyer F, et al. Interferon-beta increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain 2008;131:1455-1463.
60. Krumbholz M, Theil D, Derfuss T, et al. BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma. J Exp Med 2005;201:195-200.
61. Kim SH, Kim W, Li XF, Jung IJ, Kim HJ. 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 2011;68:1412-1420.
62. Pellkofer HL, Krumbholz M, Berthele A, et al. Long-term follow-up of patients with neuromyelitis optica after repeated therapy with rituximab. Neurol 2011;76:1310-1315.
63. Radaelli M, Moiola L, Sangalli F, et al. Neuromyelitis optica spectrum disorders: long-term safety and efficacy of rituximab in Caucasian patients. Mult Scler 2015.
64. Satoh J, Onoue H, Arima K, Yamamura T. Nogo-A and nogo receptor expression in demyelinating lesions of multiple sclerosis. J Neuropathol Exp Neurol 2005;64:129-138.
65. Dalakas MC. Autoimmune peripheral neuropathies. In: Rich RR, Fleisher TA, Shearer WT (eds.). Clinical immunology: principles and practice. Philadelphia, PA: Mosby Elsevier, 2011, pp. 977-994.
66. Kusunoki S, Kaida K. Antibodies against ganglioside complexes in Guillain-Barre syndrome and related disorders. J Neurochem 2011;116:828-832.
67. Willison HJ, Yuki N. Peripheral neuropathies and anti-glycolipid antibodies. Brain 2002;125:2591-2625.
68. Yuki N, Hartung HP. Guillain-Barré syndrome. N Engl J Med 2012;366:2294-2304.
69. Dalakas MC. Advances in the diagnosis, pathogenesis and treatment of CIDP. Nat Rev Neurol 2011;7:507-517.
70. Dalakas MC, Engel WK. Immunoglobulin and complement deposits in nerves of patients with chronic relapsing polyneuropathy. Arch Neurol 1980;37:637-640.
71. Dalakas MC, Houff SA, Engel WK, Madden DL, Sever JL. CSF “monoclonal” bands in chronic relapsing polyneuropathy. Neurology 1980;30:864-867.
72. Stathopoulos P, Alexopoulos H, Dalakas MC. Autoimmune antigenic targets at the node of Ranvier in demyelinating disorders. Nat Rev Neurol 2015;11:143-156.
73. Tackenberg B, Jelcic I, Baerenwaldt A, et al. Impaired inhibitory Fcγ receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci U S A 2009;106:4788-4792.
74. Ritter C, Forster D, Albrecht P, Hartung HP, Kieseier BC, Lehmann HC. IVIG regulates BAFF expression in patients with chronic inflammatory demyelinating polyneuropathy (CIDP). J Neuroimmunol 2014;274:225-229.
75. Monaco S, Bonetti B, Ferrari S, et al. Complement-mediated demyelination in patients with IgM monoclonal gammopathy and polyneuropathy. N Engl J Med 1990;322:649-652.
76. Lombardi R, Erne B, Lauria G, et al. IgM deposits on skin nerves in anti-myelin-associated glycoprotein neuropathy. Ann Neurol 2005;57:180-187.
77. Campagnolo M, Ferrari S, Dalla Torre C, et al. Polyneuropathy with anti-sulfatide and anti-MAG antibodies: clinical, neurophysiological, pathological features and response to treatment. J Neuroimmunol 2015;281:1-4.
78. Dalakas MC, Rakocevic G, Salajegheh M, et al. Placebo-controlled trial of rituximab in IgM anti-myelin-associated glycoprotein antibody demyelinating neuropathy. Ann Neurol 2009;65:286-293.
79. Maurer MA, Rakocevic G, Leung CS, et al. Rituximab induces sustained reduction of pathogenic B cells in patients with peripheral nervous system autoimmunity. J Clin Invest 2012;122:1393-1402.
80. Rizzi M, Knoth R, Hampe CS, et al. Long-lived plasma cells and memory B cells produce pathogenic anti-GAD65 autoantibodies in Stiff Person Syndrome. PLoS One 2010;5:e10838.
81. Dalakas MC, Li M, Fujii M, Jacobowitz DM. Stiff person syndrome: quantification, specificity, and intrathecal synthesis of GAD65 antibodies. Neurology 2001;57:780-784.
82. Geis C, Weishaupt A, Hallermann S, et al. Stiff person syndrome-associated autoantibodies to amphiphysin mediate reduced GABAergic inhibition. Brain 2010;133:3166-3180.
83. Cohen-Kaminsky S, Delattre RM, Devergne O, et al. High IL-6 gene expression and production by cultured human thymic epithelial cells from patients with myasthenia gravis. Ann N Y Acad Sci 1993;681:97-99.
84. Huang D, Pirskanen R, Hjelmstrom P, Lefvert AK. Polymorphisms in IL-1beta and IL-1 receptor antagonist genes are associated with myasthenia gravis. J Neuroimmunol 1998;81:76-81.
85. Huang YM, Kivisakk P, Ozenci V, Pirskanen R, Link H. Increased levels of circulating acetylcholine receptor (AChR)-reactive IL-10-secreting cells are characteristic for myasthenia gravis (MG). Clin Exp Immunol 1999;118:304-308.
86. Ragheb S, Lisak R, Lewis R, Van Stavern G, Gonzales F, Simon K. A potential role for B-cell activating factor in the pathogenesis of autoimmune myasthenia gravis. Arch Neurol 2008;65:1358-1362.
87. Dalakas MC. Inflammatory myopathies: management of steroid resistance. Curr Opin Neurol 2011;24:457-462.
88. Greenberg SA, Pinkus GS, Amato AA, Pinkus JL. Myeloid dendritic cells in inclusion-body myositis and polymyositis. Muscle Nerve 2007;35:17-23.
89. Salajegheh M, Kong SW, Pinkus JL, et al. Interferon-stimulated gene 15 (ISG15) conjugates proteins in dermatomyositis muscle with perifascicular atrophy. Ann Neurol 2010;67:53-63.
90. Dalakas MC. Inflammatory muscle diseases. N Engl J Med 2015;373:393-394.
91. Aggarwal R, Bandos A, Reed AM, et al. Predictors of clinical improvement in rituximab-treated refractory adult and juvenile dermatomyositis and adult polymyositis. Arthritis Rheumatol 2014;66:740-749.
92. Chung L, Genovese MC, Fiorentino DF. A pilot trial of rituximab in the treatment of patients with dermatomyositis. Arch Dermatol 2007;143:763-767.
93. Haroon M, Devlin J. Rituximab as a first-line agent for the treatment of dermatomyositis. Rheumatol Int 2012;32:1783-1784.
94. Levine TD. Rituximab in the treatment of dermatomyositis: an open-label pilot study. Arthritis Rheum 2005;52:601-607.
95. Rios Fernandez R, Callejas Rubio JL, Sanchez Cano D, Saez Moreno JA, Ortego Centeno N. Rituximab in the treatment of dermatomyositis and other inflammatory myopathies. A report of 4 cases and review of the literature. Clin Exp Rheumatol 2009;27:1009-1016.
96. Leone A, Sciascia S, Kamal A, Khamashta M. Biologicals for the treatment of systemic lupus erythematosus: current status and emerging therapies. Exp Rev Clin Immunol 2015;11:109-116.
97. Luhder F, Gold R. Trial and error in clinical studies: lessons from ATAMS. Lancet Neurol 2014;13:340-341.
98. Fujimoto M, Poe JC, Hasegawa M, Tedder TF. CD19 regulates intrinsic B lymphocyte signal transduction and activation through a novel mechanism of processive amplification. Immunol Res 2000;22:281-298.
99. Herbst R, Wang Y, Gallagher S, et al. B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. J Pharmacol Exp Ther 2010;335:213-222.
100. Tedder TF, Poe JC, Haas KM. CD22: a multifunctional receptor that regulates B lymphocyte survival and signal transduction. Adv Immunol 2005;88:1-50.
101. Goede V, Klein C, Stilgenbauer S. Obinutuzumab (GA101) for the treatment of chronic lymphocytic leukemia and other B-cell non-hodgkin’s lymphomas: a glycoengineered type II CD20 antibody. Oncol Res Treat 2015;38:185-192.
102. Robak P, Smolewski P, Robak T. Emerging immunological drugs for chronic lymphocytic leukemia. Exp Opin Emerg Drugs 2015;20:423-447.
103. Teo EC, Chew Y, Phipps C. A review of monoclonal antibody therapies in lymphoma. Crit Rev Oncol Hematol 2015.
104. Palanichamy A, Jahn S, Nickles D, et al. Rituximab efficiently depletes increased CD20-expressing T cells in multiple sclerosis patients. J Immunol 2014;193:580-586.
105. Petereit HF, Rubbert-Roth A. Rituximab levels in cerebrospinal fluid of patients with neurological autoimmune disorders. Mult Scler 2009;15:189-192.
106. Cross AH, Stark JL, Lauber J, Ramsbottom MJ, Lyons JA. Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J Neuroimmunol 2006;180:63-70.
107. Bar-Or A, Calabresi PA, Arnold D, et al. Rituximab in relapsing-remitting multiple sclerosis: a 72-week, open-label, phase I trial. Ann Neurol 2008;63:395-400
108. Hauser SL, Waubant E, Arnold DL, et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008;358:676-688.
109. Nielsen AS, Miravalle A, Langer-Gould A, Cooper J, Edwards KR, Kinkel RP. Maximally tolerated versus minimally effective dose: the case of rituximab in multiple sclerosis. Mult Scler 2012;18:377-378.
110. Cross AH, Klein RS, Piccio L. Rituximab combination therapy in relapsing multiple sclerosis. Ther Adv Neurol Disord 2012;5:311-319.
111. Evdoshenko E, Maslyanskiy A, Lapin S, et al. Dynamics of B-cell populations in CSF and blood in patients treated with a combination of rituximab and mitoxantrone. ISRN Neurol 2013;2013:748127.
112. Hawker K, O’Connor P, Freedman MS, et al. Rituximab in patients with primary progressive multiple sclerosis: results of a randomized double-blind placebo-controlled multicenter trial. Ann Neurol 2009;66:460-471.
113. Bedi GS, Brown AD, Delgado SR, Usmani N, Lam BL, Sheremata WA. Impact of rituximab on relapse rate and disability in neuromyelitis optica. Mult Scler 2011;17:1225-1230.
114. Cree BA, Lamb S, Morgan K, Chen A, Waubant E, Genain C. An open label study of the effects of rituximab in neuromyelitis optica. Neurology 2005;64:1270-1272.
115. Ip VH, Lau AY, Au LW, et al. Rituximab reduces attacks in Chinese patients with neuromyelitis optica spectrum disorders. J Neurol Sci 2013;324:38-39.
116. Jacob A, Weinshenker BG, Violich I, et al. Treatment of neuromyelitis optica with rituximab: retrospective analysis of 25 patients. Arch Neurol 2008;65:1443-1448.
117. Mahmood NA, Silver K, Onel K, Ko M, Javed A. Efficacy and safety of rituximab in pediatric neuromyelitis optica. J Child Neurol 2011;26:244-247.
118. Gredler V, Mader S, Schanda K, et al. Clinical and immunological follow-up of B-cell depleting therapy in CNS demyelinating diseases. J Neurol Sci 2013;328:77-82.
119. Kim SH, Jeong IH, Hyun JW, et al. Treatment outcomes with rituximab in 100 patients with neuromyelitis optica: influence of FCGR3A polymorphisms on the therapeutic response to rituximab. JAMA Neurol 2015;72:989-995.
120. Mealy MA, Wingerchuk DM, Palace J, Greenberg BM, Levy M. Comparison of relapse and treatment failure rates among patients with neuromyelitis optica: multicenter study of treatment efficacy. JAMA Neurol 2014;71:324-330.
121. Nakashima I, Takahashi T, Cree BA, et al. Transient increases in anti-aquaporin-4 antibody titers following rituximab treatment in neuromyelitis optica, in association with elevated serum BAFF levels. J Clin Neurosci 2011;18:997-998.
122. Perumal JS, Kister I, Howard J, Herbert J. Disease exacerbation after rituximab induction in neuromyelitis optica. Neurol Neuroimmunol Neuroinflamm 2015;2:e61.
123. Karenfort M, Kieseier BC, Tibussek D, Assmann B, Schaper J, Mayatepek E. Rituximab as a highly effective treatment in a female adolescent with severe multiple sclerosis. Develop Med Child Neurol 2009;51:159-161.
124. Tzaribachev N, Koetter I, Kuemmerle-Deschner JB, Schedel J. Rituximab for the treatment of refractory pediatric autoimmune diseases: a case series. Cases J 2009;2:6609
125. Beres SJ, Graves J, Waubant E. Rituximab use in pediatric central demyelinating disease. Pediatr Neurol 2014;51:114-118.
126. Bacorro EA, Tehrani R. Stiff-person syndrome: persistent elevation of glutamic acid decarboxylase antibodies despite successful treatment with rituximab. J Clin Rheumatol 2010;16:237-239.
127. Lobo ME, Araujo ML, Tomaz CA, Allam N. Stiff-person syndrome treated with rituximab. BMJ Case Rep 2010;2010.
128. Dupond JL, Essalmi L, Gil H, Meaux-Ruault N, Hafsaoui C. Rituximab treatment of stiff-person syndrome in a patient with thymoma, diabetes mellitus and autoimmune thyroiditis. J Clin Neurosci 2010;17:389-391.
129. Katoh N, Matsuda M, Ishii W, Morita H, Ikeda S. Successful treatment with rituximab in a patient with stiff-person syndrome complicated by dysthyroid ophthalmopathy. Intern Med 2010;49:237-241.
130. Qureshi A, Hennessy M. Stiff person syndrome (SPS) complicated by respiratory failure: successful treatment with rituximab. J Neurol 2012;259:180-181.
131. Zdziarski P. A case of stiff person syndrome: immunomodulatory effect of benzodiazepines: successful rituximab and tizanidine therapy. Medicine 2015;94:e954.
132. Dalakas MC, Rakocevic G, Dambrosia J, McElroy B. A double-blind, placebo-cotrolled study of rituximab in patients with stiff-person syndrome (SPS). Ann Neurol 2009;66:S20.
133. Nowak RJ, Dicapua DB, Zebardast N, Goldstein JM. Response of patients with refractory myasthenia gravis to rituximab: a retrospective study. Ther Adv Neurol Disord 2011;4:259-266.
134. Keung B, Robeson KR, DiCapua DB, et al. Long-term benefit of rituximab in MuSK autoantibody myasthenia gravis patients. J Neurol Neurosurg Psychiatry 2013;84:1407-1409.
135. Iorio R, Damato V, Alboini PE, Evoli A. Efficacy and safety of rituximab for myasthenia gravis: a systematic review and meta-analysis. J Neurol 2015;262:1115-1119.
136. Oddis CV, Reed AM, Aggarwal R, et al. Rituximab in the treatment of refractory adult and juvenile dermatomyositis and adult polymyositis: a randomized, placebo-phase trial. Arthritis Rheum 2013;65:314-324.
137. Martin Mdel P, Cravens PD, Winger R, et al. Depletion of B lymphocytes from cerebral perivascular spaces by rituximab. Arch Neurol 2009;66:1016-1020.
138. Carson KR, Focosi D, Major EO, 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 2009;10:816-824.
139. De Palma R, Sementa A. Rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008;358:2645-2646.
140. Shetty S, Ahmed AR. Preliminary analysis of mortality associated with rituximab use in autoimmune diseases. Autoimmunity 2013;46:487-496.
141. Kim SH, Huh SY, Lee SJ, Joung A, Kim HJ. A 5-year follow-up of rituximab treatment in patients with neuromyelitis optica spectrum disorder. JAMA Neurol 2013;70:1110-1117.
142. Weinfurtner K, Graves J, Ness J, Krupp L, Milazzo M, Waubant E. Prolonged remission in neuromyelitis optica following cessation of rituximab treatment. J Child Neurol 2015;30:1366-1370.
143. Svenningsson A, Bergman J, Dring A, et al. Rapid depletion of B lymphocytes by ultra-low-dose rituximab delivered intrathecally. Neurol Neuroimmunol Neuroinflamm 2015;2:e79.
144. Marnetto F, Granieri L, Valentino P, Capobianco M, Pautasso M, Bertolotto A. CD19 mRNA quantification improves rituximab treatment-to-target approach: a proof of concept study. J Neuroimmunol 2014;277:127-133.
145. Stork AC, Notermans NC, van den Berg LH, et al. Fcgamma receptor IIIA genotype is associated with rituximab response in antimyelin-associated glycoprotein neuropathy. J Neurol Neurosurg Psychiatry 2014;85:918-920.
146. Emery P, Rigby W, Tak PP, et al. Safety with ocrelizumab in rheumatoid arthritis: results from the ocrelizumab phase III program. PLoS One 2014;9:e87379.
147. Harigai M, Tanaka Y, Maisawa S. Safety and efficacy of various dosages of ocrelizumab in Japanese patients with rheumatoid arthritis with an inadequate response to methotrexate therapy: a placebo-controlled double-blind parallel-group study. J Rheumatol 2012;39:486-495.
148. Mysler EF, Spindler AJ, Guzman R, et al. Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from a randomized, double-blind, phase III study. Arthritis Rheum 2013;65:2368-2379.
149. Rigby W, Tony HP, Oelke K, et al. Safety and efficacy of ocrelizumab in patients with rheumatoid arthritis and an inadequate response to methotrexate: results of a forty-eight-week randomized, double-blind, placebo-controlled, parallel-group phase III trial. Arthritis Rheum 2012;64:350-359.
150. Stohl W, Gomez-Reino J, Olech E, et al. Safety and efficacy of ocrelizumab in combination with methotrexate in MTX-naive subjects with rheumatoid arthritis: the phase III FILM trial. Ann Rheum Dis 2012;71:1289-1296.
151. Tak PP, Mease PJ, Genovese MC, et al. Safety and efficacy of ocrelizumab in patients with rheumatoid arthritis and an inadequate response to at least one tumor necrosis factor inhibitor: results of a forty-eight-week randomized, double-blind, placebo-controlled, parallel-group phase III trial. Arthritis Rheum 2012;64:360-370.
152. Kappos L, Li D, Calabresi PA, et al. Ocrelizumab in relapsing-remitting multiple sclerosis: a phase 2, randomised, placebo-controlled, multicentre trial. Lancet 2011;378:1779-1787.
153. Sorensen PS, Lisby S, Grove R, et al. Safety and efficacy of ofatumumab in relapsing-remitting multiple sclerosis: a phase 2 study. Neurology 2014;82:573-581.
154. Ketterl TG, Messinger YH, Niess DR, Gilles E, Engel WK, Perkins JL. Ofatumumab for refractory opsoclonus-myoclonus syndrome following treatment of neuroblastoma. Pediatr Blood Cancer 2013;60:E163-E165.
155. Pranzatelli MR, Tate ED, Shenoy S, Travelstead AL. Ofatumumab for a rituximab-allergic child with chronic-relapsing paraneoplastic opsoclonus-myoclonus. Pediatr Blood Cancer 2012;58:988-991.