Emerging therapeutic targets for neuromyelitis optica spectrum disorder

References

• Kitley J, Palace J. Therapeutic options in neuromyelitis optica spectrum disorders. Expert Rev Neurother. 2016;16(3):319–329.
   PubMed Web of Science ®Google Scholar
• Papadopoulos MC, Bennett JL, Verkman AS. Treatment of neuromyelitis optica: state-of-the-art and emerging therapies. Nat Rev Neurol. 2014 Sep;10(9):493–506.
   PubMed Web of Science ®Google Scholar
• Pittock SJ, Berthele A, Fujihara K, et al. Eculizumab in aquaporin-4-positive neuromyelitis optica spectrum disorder. N Engl J Med. 2019 Aug 15;381(7):614–625.
   PubMed Web of Science ®Google Scholar
• Yamamura T, Kleiter I, Fujihara K, et al. Trial of satralizumab in neuromyelitis optica spectrum disorder. N Engl J Med. 2019 Nov 28;381(22):2114–2124.
   PubMed Web of Science ®Google Scholar
• Cree BAC, Bennett JL, Kim HJ, et al. Inebilizumab for the treatment of neuromyelitis optica spectrum disorder (N-MOmentum): a double-blind, randomized placebo-controlled phase 2/3 trial. Lancet. 2019 Oct 12;394(10206):1352–1363.
   PubMed Web of Science ®Google Scholar
• Damato V, Evoli A, Iorio R. Efficacy and safety of rituximab therapy in neuromyelitis optica spectrum disorders, a systematic review and meta-analysis. JAMA Neurol. 2016;73(11):1342–1348.
   PubMed Web of Science ®Google Scholar
• Jarius S, Wildemann B, Paul F. Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin Exp Immunol. 2014 May;176(2):149–164.
   PubMed Web of Science ®Google Scholar
• Hinson SR, Lennon VA, Pittock SJ. Autoimmune AQP4 channelopathies and neuromyelitis optica spectrum disorders. Handb Clin Neurol. 2016;133:377–403.
   PubMedGoogle Scholar
• Wu Y, Zhong L, Geng J. Neuromyelitis optica spectrum disorder: pathogenesis, treatment, and experimental models. Mult Scler Relat Disord. 2019 Jan;27:412–418.
   PubMed Web of Science ®Google Scholar
• Papadopoulos MC, Verkman AS. Aquaporin-4 and neuromyelitis optica. Lancet. 2012;11:535–544.
   PubMed Web of Science ®Google Scholar
• Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci. 2013;14:265–277.
   PubMed Web of Science ®Google Scholar
• Crane JM, Lamm C, Rossi A, et al. Binding and specificity of neuromyelitis optica autoantibodies to M1/M23 isoforms and orthogonal arrays. J Biol Chem. 2011;286:16516–16524.
   PubMed Web of Science ®Google Scholar
• Phuan PW, Ratelade J, Rossi A, et al. Complement-dependent cytotoxicity in neuromyelitis optica requires aquaporin-4 protein assembly in orthogonal arrays. J Biol Chem. 2012 Apr 20;287(17):13829–13839.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Yao X, Su T, et al. Bystander mechanism for complement-initiated early oligodendrocyte injury in neuromyelitis optica. Acta Neuropathol. 2017 Jul;134(1):35–44.
   PubMed Web of Science ®Google Scholar
• Duan T, Smith AJ, Verkman AS. Complement-dependent bystander injury to neurons in AQP4-IgG seropositive neuromyelitis optica. J Neuroinflammation. 2018 Oct 22;15(1):294.
   PubMedGoogle Scholar
• Duan T, Smith AJ, Verkman AS. Complement-independent bystander injury in AQP4-IgG seropositive neuromyelitis optica produced by antibody-dependent cellular cytotoxicity. Acta Neuropathol Commun. 2019 Jul 11;7(1):112.
   PubMedGoogle Scholar
• Hinson SR, Romero MF, Popescu BF, et al. Molecular outcomes of neuromyelitis otica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1245–1250.
   PubMed Web of Science ®Google Scholar
• Rossi A, Ratelade J, Papadopoulos MC, et al. Neuromyelitis optica IgG does not alter aquaporin-4 water permeability, plasma membrane M1/M23 isoform content, or supramolecular assembly. Glia. 2012 Dec;60(12):2027–2039.
   PubMed Web of Science ®Google Scholar
• Hillebrand S, Schanda K, Nigritinou M, et al. Circulating AQP4-specific auto-antibodies alone can induce neuromyelitis optica spectrum disorder in the rat. Acta Neuropathol. 2019 Mar;137(3):467–485.
   PubMed Web of Science ®Google Scholar
• Shimizu F, Schaller KL, Owens GP, et al. Glucose-regulated protein 78 autoantibody associates with blood-brain barrier disruption in neuromyelitis optica. Sci Transl Med. 2017Jul 5;9:397.
   Web of Science ®Google Scholar
• Duan T, Verkman AS. Experimental animal models of aquaporin-4-IgG-seropositive neuromyelitis optica spectrum disorders: progress and shortcomings. Brain Pathol. 2020 Jan;30(1):13–25.
   PubMed Web of Science ®Google Scholar
• Cree BA, Spencer CM, Varrin-Doyer M, et al. Gut microbiome analysis in neuromyelitis optica reveals overabundance of Clostridium perfringens. Ann Neurol. 2016 Sep;80(3):443–447.
   PubMed Web of Science ®Google Scholar
• Collin M, Olsen A. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. Embo J. 2001 Jun 15;20(12):3046–3055.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Ratelade J, Zhang H, et al. Enzymatic deglycosylation converts pathogenic neuromyelitis optica anti-aquaporin-4 immunoglobulin G into therapeutic antibody. Ann Neurol. 2013 Jan;73(1):77–85.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Asavapanumas N, Verkman AS. Therapeutic cleavage of anti-aquaporin-4 autoantibody in neuromyelitis optica by an IgG-selective proteinase. Mol Pharmacol. 2013 Jun;83(6):1268–1275.
   PubMed Web of Science ®Google Scholar
• Collin M, Bjorck L. Toward clinical use of the IgG specific enzymes IdeS and EndoS against antibody-mediated diseases. Methods Mol Biol. 2017;1535:339–351.
   PubMedGoogle Scholar
• Lonze BE, Tatapudi VS, Weldon EP, et al. IdeS (imlifidase): A novel agent that cleaves human IgG and permits successful kidney transplantation across high-strength donor-specific antibody. Ann Surg. 2018 Sep;268(3):488–496.
   PubMed Web of Science ®Google Scholar
• Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol. 2007 Sep;7(9):715–725.
   PubMed Web of Science ®Google Scholar
• Kiessling P, Lledo-Garcia R, Watanabe S, et al. The FcRn inhibitor rozanolixizumab reduces human serum IgG concentration: A randomized phase 1 study. Sci Transl Med. 2017 Nov 1;9:414.
   Web of Science ®Google Scholar
• Lipphardt M, Muhlhausen J, Kitze B, et al. Immunoadsorption or plasma exchange in steroid-refractory multiple sclerosis and neuromyelitis optica. J Clin Apher. 2019 Aug;34(4):381–391.
   PubMed Web of Science ®Google Scholar
• Kleiter I, Gahlen A, Borisow N, et al. Apheresis therapies for NMOSD attacks: A restrospective study of 207 therapeutic interventions. Neurol Neuroimmunol Neuroinflamm. 2018 Sep 26;5(6):e504.
   PubMed Web of Science ®Google Scholar
• Liu S, Zhou J, Liu Q, et al. HA208 immunoadsorption, an alternative treatment for neuromyelitis optica spectrum disorders? Mult Scler Relat Disord. 2019 Oct;30(37):101480.
   Google Scholar
• Faer S, Nikolayczik J, Chan A, et al. Immunoadsorption in patients with neuromyelitis optica spectrum disorder. Ther Adv Neurol Disord. 2016 July;9(4):281–286.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Zhang H, Anderson MO, et al. Small-molecule inhibitors of NMO-IgG binding to aquaporin-4 reduce astrocyte cytotoxicity in neuromyelitis optica. Faseb J. 2012 May;26(5):2197–2208.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Zhang H, Saadoun S, et al. Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. Ann Neurol. 2012 Mar;71(3):314–322.
   PubMed Web of Science ®Google Scholar
• Bennett JL, Lam C, Kalluri SR, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009 Nov;66(5):617–629.
   PubMed Web of Science ®Google Scholar
• Duan T, Tradtrantip L, Phuan PW, et al. Affinity-matured ‘aquaporumab’ anti-aquaporin-4 antibody for therapy of seropositive neuromyelitis optica spectrum disorders. Neuropharmacology. 2020 Jan 1;162:107827.
   PubMed Web of Science ®Google Scholar
• Zhang H, Verkman AS. Longitudinally extensive NMO spinal cord pathology produced by passive transfer of NMO-IgG in mice lacking complement inhibitor CD59. J Autoimmun. 2014 Sep;53:67–77.
   PubMed Web of Science ®Google Scholar
• Yao X, Verkman AS. Marked central nervous system pathology in CD59 knockout rats following passive transfer of neuromyelitis optica immunoglobulin G. Acta Neuropathol Commun. 2017 Feb 17;5(1):15.
   PubMedGoogle Scholar
• Zelek WM, Xie L, Morgan BP, et al. Compendium of current complement therapeutics. Mol Immunol. 2019;114:341–352.
   PubMed Web of Science ®Google Scholar
• Phuan PW, Zhang H, Asavapanumas N, et al. C1q-targeted monoclonal antibody prevents complement-dependent cytotoxicity and neuropathology in in vitro and mouse models of neuromyelitis optica. Acta Neuropathol. 2013 Jun;125(6):829–840.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Duan T, Yeaman MR, et al. CD55 upregulation in astrocytes by statins as potential therapy for AQP4-IgG seropositive neuromyelitis optica. J Neuroinflammation. 2019 Mar 9;16(1):57.
   PubMedGoogle Scholar
• Wingerchuk DM. Neuromyelitis optica: potential roles for intravenous immunoglobulin. J Clin Immunol. 2013 Jan;33(Suppl 1):S33–S37.
   PubMedGoogle Scholar
• Absoud M, Brex P, Ciccarelli O, et al. A multicentre randomised controlled trial of intravenous immunoglobulin compared with standard therapy for the treatment of transverse myelitis in adults and children (STRIVE). Health Technol Assess. 2017 May;21(31):1–50.
   PubMed Web of Science ®Google Scholar
• Lunemann JD, Nimmerjahn F, Dalakas MC. Intravenous immunoglobulin in neurology–mode of action and clinical efficacy. Nat Rev Neurol. 2015 Feb;11(2):80–89.
   PubMed Web of Science ®Google Scholar
• Ratelade J, Smith AJ, Verkman AS. Human immunoglobulin G reduces the pathogenicity of aquaporin-4 autoantibodies in neuromyelitis optica. Exp Neurol. 2014 May;255:145–153.
   PubMed Web of Science ®Google Scholar
• Grunewald B, Bennett JL, Toyka KV, et al. Efficacy of polyvalent human immunoglobulins in an animal model of neuromyelitis optica evoked by intrathecal anti-aquaporin 4 antibodies. Int J Mol Sci. 2016 Aug 26;17:9.
   Web of Science ®Google Scholar
• Zuercher AW, Spirig R, Baz Morelli A, et al. Next-generation Fc receptor-targeting biologics for autoimmune diseases. Autoimmun Rev. 2019 Oct;18(10):102366.
   PubMed Web of Science ®Google Scholar
• Spirig R, Campbell IK, Koernig S, et al. rIgG1 Fc hexamer inhibits antibody-mediated autoimmune disease via effects on complement and FcgammaRs. J Immunol. 2018 Apr 15;200(8):2542–2553.
   PubMed Web of Science ®Google Scholar
• Bosques CJ, Manning AM. Fc-gamma receptors: attractive targets for autoimmune drug discovery searching for intelligent therapeutic designs. Autoimmun Rev. 2016 Nov;15(11):1081–1088.
   PubMed Web of Science ®Google Scholar
• Tradtrantip L, Felix CM, Spirig R, et al. Recombinant IgG1 Fc hexamers block cytotoxicity and pathological changes in experimental in vitro and rat models of neuromyelitis optica. Neuropharmacology. 2018 May 1;133:345–353.
   PubMed Web of Science ®Google Scholar
• Saadoun S, Waters P, MacDonald C, et al. Neutrophil protease inhibition reduces neuromyelitis optica-immunoglobulin G-induced damage in mouse brain. Ann Neurol. 2012 Mar;71(3):323–333.
   PubMed Web of Science ®Google Scholar
• Zhang H, Verkman AS. Eosinophil pathogenicity mechanisms and therapeutics in neuromyelitis optica. J Clin Invest. 2013 May;123(5):2306–2316.
   PubMed Web of Science ®Google Scholar
• Katz Sand I, Fabian MT, Telford R, et al. Open-label, add-on trial of cetirizine for neuromyelitis optica. Neurol Neuroimmunol Neuroinflamm. 2018 Mar;5(2):e441.
   PubMed Web of Science ®Google Scholar
• Caminati M, Cegolon L, Vianello A, et al. Mepolizumab for severe eosinophilic asthma: a real-world snapshot on clinical markers and timing of response. Expert Rev Respir Med. 2019;16:1–8.
   Google Scholar
• Valesini G, Alessandri C, Celestino D, et al. Anti-endothelial antibodies and neuropsychiatric systemic lupus erythematosus. Ann N Y Acad Sci. 2006;1069:118–128.
   PubMed Web of Science ®Google Scholar
• Guilpain P, Mouthon L. Antiendothelial cells autoantibodies in vasculitis-associated systemic diseases. Clin Rev Allergy Immunol. 2008 Oct;35(1–2):59–65.
   PubMed Web of Science ®Google Scholar
• Del Papa N, Raschi E, Moroni G, et al. Anti-endothelial cell IgG fractions from systemic lupus erythematosus patients bind to human endothelial cells and induce a pro-adhesive and a pro-inflammatory phenotype in vitro. Lupus. 1999;8(6):423–429.
   PubMed Web of Science ®Google Scholar
• Minagar A, Long A, Ma T, et al. Interferon (IFN)-beta 1a and IFN-beta 1b block IFN-gamma-induced disintegration of endothelial junction integrity and barrier. Endothelium. 2003;10(6):299–307.
   PubMedGoogle Scholar
• Shimizu F, Sano Y, Takahashi T, et al. Sera from neuromyelitis optica patients disrupt the blood-brain barrier. J Neurol Neurosurg Psychiatry. 2012 Mar;83(3):288–297.
   PubMed Web of Science ®Google Scholar
• Mealy MA, Shin K, John G, et al. Bevacizumab is safe in acute relapses of neuromyelitis optica. Clin Exp Neuroimmunol. 2015 Nov 1;6(4):413–418.
   PubMedGoogle Scholar
• Nishihara H, Shimizu F, Sano Y, et al. Fingolimod prevents blood-brain barrier disruption induced by the sera from patients with multiple sclerosis. PLoS One. 2015;10(3):e0121488.
   PubMed Web of Science ®Google Scholar
• Trinka E, Steinhoff BJ, Nikanorova M, et al. Perampanel for focal epilepsy: insights from early clinical experience. Acta Neurol Scand. 2016 Mar;133(3):160–172.
   PubMed Web of Science ®Google Scholar
• Shimizu F, Nishihara H, Kanda T. Blood-brain barrier dysfunction in immuno-mediated neurological diseases. Immunol Med. 2018 Sep;41(3):120–128.
   PubMedGoogle Scholar
• Baldassari LE, Feng J, Clayton BLL, et al. Developing therapeutic strategies to promote myelin repair in multiple sclerosis. Expert Rev Neurother. 2019 Oct;19(10):997–1013.
   PubMed Web of Science ®Google Scholar
• Bove RM, Green AJ. Remyelinating pharmacotherapies in multiple sclerosis. Neurotherapeutics. 2017 Oct;14(4):894–904.
   PubMed Web of Science ®Google Scholar
• Yao X, Su T, Verkman AS. Clobetasol promotes remyelination in a mouse model of neuromyelitis optica. Acta Neuropathol Commun. 2016 Apr 26;4(1):42.
   PubMedGoogle Scholar
• Bennett JL, O’Connor KC, Bar-Or A, et al. B lymphocytes in neuromyelitis optica. Neurol Neuroimmunol Neuroinflamm. 2015 Jun;2(3):e104.
   PubMed Web of Science ®Google Scholar
• de Romeuf C, Dutertre CA, Le Garff-Tavernier M, et al. Chronic lymphocytic leukaemia cells are efficiently killed by an anti-CD20 monoclonal antibody selected for improved engagement of FcgammaRIIIA/CD16. Br J Haematol. 2008 Mar;140(6):635–643.
   PubMed Web of Science ®Google Scholar
• Alexopoulos H, Biba A, Dalakas MC. Anti-B-cell therapies in autoimmune neurological diseases: rationale and efficacy trials. Neurotherapeutics. 2016 Jan;13(1):20–33.
   PubMed Web of Science ®Google Scholar
• Leone A, Sciascia S, Kamal A, et al. Biologicals for the treatment of systemic lupus erythematosus: current status and emerging therapies. Expert Rev Clin Immunol. 2015 Jan;11(1):109–116.
   PubMed Web of Science ®Google Scholar
• Kansal R, Richardson N, Neeli I, et al. Sustained B cell depletion by CD19-targeted CAR T cells is a highly effective treatment for murine lupus. Sci Transl Med. 2019 Mar 6;11:482.
   Web of Science ®Google Scholar
• Kalampokis I, Yoshizaki A, Tedder TF. IL-10-producing regulatory B cells (B10 cells) in autoimmune disease. Arthritis Res Ther. 2013;15(Suppl 1):S1.
   PubMed Web of Science ®Google Scholar
• Yu M, Song Y, Zhu MX, et al. B10 cells ameliorate the progression of lupus nephritis by attenuating glomerular endothelial cell injury. Cell Physiol Biochem. 2015;36(6):2161–2169.
   PubMedGoogle Scholar
• 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 Mar;19(3):289–298.
   PubMed Web of Science ®Google Scholar
• Cho EB, Cho HJ, Seok JM, et al. The IL-10-producing regulatory B cells (B10 cells) and regulatory T cell subsets in neuromyelitis optica spectrum disorder. Neurol Sci. 2018 Mar;39(3):543–549.
   PubMed Web of Science ®Google Scholar
• Lucchinetti CF, Mandler RN, McGavern D, et al. A role for humoral mechanisms in the pathogenesis of Devic’s neuromyelitis optica. Brain. 2002 Jul;125(Pt 7):1450–1461.
   PubMed Web of Science ®Google Scholar
• Lin J, Li X, Xia J. Th17 cells in neuromyelitis optica spectrum disorder: a review. Int J Neurosci. 2016 Dec;126(12):1051–1060.
   PubMed Web of Science ®Google Scholar
• Cruz-Herranz A, Sagan SA, Sobel RA, et al. T cells targeting neuromyelitis optica autoantigen aquaporin-4 cause paralysis and visual system injury. J Nat Sci. 2017 May;3(5):e358.
   PubMedGoogle Scholar
• Waisman A, Ruiz PJ, Hirschberg DL, et al. Suppressive vaccination with DNA encoding a variable region gene of the T-cell receptor prevents autoimmune encephalomyelitis and activates Th2 immunity. Nat Med. 1996 Aug;2(8):899–905.
   PubMed Web of Science ®Google Scholar
• Garren H, Robinson WH, Krasulova E, et al. Phase 2 trial of a DNA vaccine encoding myelin basic protein for multiple sclerosis. Ann Neurol. 2008 May;63(5):611–620.
   PubMed Web of Science ®Google Scholar
• Steinman L, Bar-Or A, Behne JM, et al. Restoring immune tolerance in neuromyelitis optica: part I. Neurol Neuroimmunol Neuroinflamm. 2016 Oct;3(5):e276.
   PubMedGoogle Scholar
• Bar-Or A, Steinman L, Behne JM, et al. Restoring immune tolerance in neuromyelitis optica: part II. Neurol Neuroimmunol Neuroinflamm. 2016 Oct;3(5):e277.
   PubMedGoogle Scholar
• Kohm AP, Carpentier PA, Anger HA, et al. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol. 2002 Nov 1;169(9):4712–4716.
   PubMed Web of Science ®Google Scholar
• Marek-Trzonkowska N, Mysliwiec M, Dobyszuk A, et al. Therapy of type 1 diabetes with CD4+CD25highCD127-regulatory T cells prolongs survival of pancreatic islets - results of one year follow-up. Clin Immunol. 2014 Jul;153(1):23–30.
   PubMed Web of Science ®Google Scholar
• Di Ianni M, Falzetti F, Carotti A, et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood. 2011 Apr 7;117(14):3921–3928.
   PubMed Web of Science ®Google Scholar
• Moser M. Dendritic cells in immunity and tolerance-do they display opposite functions? Immunity. 2003 Jul;19(1):5–8.
   PubMed Web of Science ®Google Scholar
• Boltjes A, van Wijk F. Human dendritic cell functional specialization in steady-state and inflammation. Front Immunol. 2014;5:131.
   PubMed Web of Science ®Google Scholar
• Florez-Grau G, Zubizarreta I, Cabezon R, et al. Tolerogenic dendritic cells as a promising antigen-specific therapy in the treatment of multiple sclerosis and neuromyelitis optica from preclinical to clinical trials. Front Immunol. 2018;9:1169.
   PubMed Web of Science ®Google Scholar
• Papenfuss TL, Powell ND, McClain MA, et al. Estriol generates tolerogenic dendritic cells in vivo that protect against autoimmunity. J Immunol. 2011 Mar 15;186(6):3346–3347155.
   PubMed Web of Science ®Google Scholar
• Zubizarreta I, Florez-Grau G, Vila G, et al. Immune tolerance in multiple sclerosis and neuromyelitis optica with peptide-loaded tolerogenic dendritic cells in a phase 1b trial. Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8463–8470.
   PubMed Web of Science ®Google Scholar
• Burt RK, Balabanov R, Han X, et al. Autologous nonmyeloablative hematopoietic stem cell transplantation for neuromyelitis optica. Neurology. 2019 Oct 29;93(18):e1732–e1741.
   PubMed Web of Science ®Google Scholar
• Soltys J, Liu Y, Ritchie A, et al. Membrane assembly of aquaporin-4 autoantibodies regulates classical complement activation in neuromyelitis optica. J Clin Invest. 2019 Apr 8;129(5):2000–2013.
   PubMed Web of Science ®Google Scholar
• Zhang C, Tian DC, Yang CS, et al. Safety and efficacy of bortezomib in patients with highly relapsing neuromyelitis optica spectrum disorder. JAMA Neurol. 2017 Aug 1;74(8):1010–1012.
   PubMed Web of Science ®Google Scholar
• Weinshenker BG, Barron G, Behne JM, et al. Challenges and opportunities in designing clinical trials for neuromyelitis optica. Neurology. 2015 Apr 28;84(17):1805–1815.
   PubMed Web of Science ®Google Scholar