Pathogenesis and advances in monoclonal antibody treatment of neuromyelitis optica spectrum disorder_Chinese Journal of Ocular Fundus Diseases

Authors：

Chang Qiaoqiao ^1,2 ,  Wu Songdi ^1,2

1. Department of Neuro-ophthalmology, The First Affiliated Hospital of Northwest University (Xi'an No.1 Hospital), Xi'an 710002, China;
2. Xi'an Key Laboratory for Innovation and Translation of Neuroimmunological Diseases, Xi'an 710002, China;

Corresponding author：

Wu Songdi, Email: wusongdi@gmail.com

Keywords：

Neuromyelitis optica spectrum disorder; Monoclonal antibodies; Biological therapy; Review

DOI：

10.3760/cma.j.cn511434-20230822-00351

Video：

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Abstract Full text Figures/Tables Video References Cited by

Neuromyelitis optica spectrum disorder (NMOSD) is a immune-mediated demyelinating disease of the central nervous system, characterized by high recurrence and disability rates. Preventing relapses is crucial in the treatment of this condition. Monoclonal antibodies have emerged as a novel and rapidly evolving clinical therapeutic strategy targeting NMOSD in recent years. An increasing number of studies and clinical trials have also confirmed the effectiveness and safety of monoclonal antibodies. Rituximab, a monoclonal antibody targeting the B-cell surface antigen CD20, has been widely used in the treatment of NMOSD. Currently, in China, the only approved monoclonal antibody for treating NMOSD is Inebilizumab, which targets the B-cell surface antigen CD19. Additionally, various monoclonal antibodies, such as interleukin-6 receptor inhibitors and complement C5 inhibitors, have been used in the treatment of NMOSD. With the deepening of the research on the pathogenesis of NMOSD, the molecular mechanism of disease-related immune network is further clarified, and multi-center clinical trials are widely carried out. More accurate monoclonal antibody treatment strategies for NMOSD will be applied to clinical practice, benefiting more patients.

Citation： Chang Qiaoqiao, Wu Songdi. Pathogenesis and advances in monoclonal antibody treatment of neuromyelitis optica spectrum disorder. Chinese Journal of Ocular Fundus Diseases, 2024, 40(3): 247-251. doi: 10.3760/cma.j.cn511434-20230822-00351 Copy

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1. 黄德晖, 吴卫平, 胡学强. 中国视神经脊髓炎谱系疾病诊断与治疗指南(2021版)[J]. 中国神经免疫学和神经病学杂志, 2021, 28(6): 423-436. DOI: 10.3969/j.issn.1006-2963.2021.06.002.Huang DH, Wu WP, Hu XQ. Chinese guidelines for diagnosis and treatment of optic neuromyelitis spectrum diseases (2021 edition)[J]. Chin J Neuroimmunol & Neurol, 2021, 28(6): 423-436. DOI: 10.3969/j.issn.1006-2963.2021.06.002.
2. Pittock SJ, Zekeridou A, Weinshenker BG. Hope for patients with neuromyelitis optica spectrum disorders-from mechanisms to trials[J]. Nat Rev Neurol, 2021, 17(12): 759-773. DOI: 10.1038/s41582-021-00568-8.
3. Sinmaz N, Nguyen T, Tea F, et al. Mapping autoantigen epitopes: molecular insights into autoantibody-associated disorders of the nervous system[J]. J Neuroinflammation, 2016, 13(1): 219. DOI: 10.1186/s12974-016-0678-4.
4. Vaishnav RA, Liu R, Chapman J, et al. Aquaporin 4 molecular mimicry and implications for neuromyelitis optica[J]. J Neuroimmunol, 2013, 260(1-2): 92-98. DOI: 10.1016/j.jneuroim.2013.04.015.
5. Chan KH, Lee CY. Treatment of neuromyelitis optica spectrum disorders[J/OL]. Int J Mol Sci, 2021, 22(16): 8638[2021-08-11]. https://pubmed.ncbi.nlm.nih.gov/34445343/. DOI: 10.3390/ijms22168638.
6. Takeshita Y, Fujikawa S, Serizawa K, et al. New BBB model reveals that IL-6 blockade suppressed the BBB disorder, preventing onset of NMOSD[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2021, 8(6): e1076[2021-10-19]. https://pubmed.ncbi.nlm.nih.gov/34667128/. DOI: 10.1212/nxi.0000000000001076.
7. Zipfel PF, Skerka C. Complement regulators and inhibitory proteins[J]. Nat Rev Immunol, 2009, 9(10): 729-740. DOI: 10.1038/nri2620.
8. Carnero Contentti E, Correale J. Neuromyelitis optica spectrum disorders: from pathophysiology to therapeutic strategies[J]. J Neuroinflammation, 2021, 18(1): 208. DOI: 10.1186/s12974-021-02249-1.
9. Yin Z, Qiu Y, Duan A, et al. Different monoclonal antibodies and immunosuppressants administration in patients with neuromyelitis optica spectrum disorder: a bayesian network meta-analysis[J]. J Neurol, 2023, 270(6): 2950-2963. DOI: 10.1007/s00415-023-11641-1.
10. Mader S, Gredler V, Schanda K, et al. Complement activating antibodies to myelin oligodendrocyte glycoprotein in neuromyelitis optica and related disorders[J]. J Neuroinflammation, 2011, 8: 184. DOI: 10.1186/1742-2094-8-184.
11. Pechlivanidou M, Xenou K, Tzanetakos D. Potential role of antibodies against aquaporin-1 in patients with central nervous system demyelination[J/OL]. Int J Mol Sci, 2023, 24(16): 12982[2023-08-19]. https://pubmed.ncbi.nlm.nih.gov/37629163/. DOI: 10.3390/ijms241612982.
12. Türkoğlu R, Lassmann H, Aker FV, et al. Recurrent tumefactive demyelinating lesions: a pathological study[J]. Clin Neuropathol, 2017, 36(4): 195-198. DOI: 10.5414/np301005.
13. Hou MM, Li YF, He LL, et al. Proportions of Th17 cells and Th17-related cytokines in neuromyelitis optica spectrum disorders patients: a meta-analysis[J/OL]. Int Immunopharmacol, 2019, 75: 105793[2019-08-08]. https://pubmed.ncbi.nlm.nih.gov/31401379/. DOI: 10.1016/j.intimp.2019.105793.
14. Agasing AM, Wu Q, Khatri B, et al. Transcriptomics and proteomics reveal a cooperation between interferon and T-helper 17 cells in neuromyelitis optica[J/OL]. 2020, 11 (1): 2856[2020-06-05]. https://pubmed.ncbi.nlm.nih.gov/32503977/. DOI: 10.1038/s41467-020-16625-7.
15. Lin J, Li X, Xia J. Th17 cells in neuromyelitis optica spectrum disorder: a review[J]. Int J Neurosci, 2016, 126(12): 1051-1060. DOI: 10.3109/00207454.2016.1163550.
16. Maciak K, Pietrasik S, Dziedzic A, et al. Th17-related cytokines as potential discriminatory markers between neuromyelitis optica (devic's disease) and multiple sclerosis-a review[J/OL]. Int J Mol Sci, 2021, 22(16): 8946[2021-08-20]. https://pubmed.ncbi.nlm.nih.gov/34445668/. DOI: 10.3390/ijms22168946.
17. Collongues N, Ayme-Dietrich E, Monassier L, et al. Pharmacotherapy for neuromyelitis optica spectrum disorders: current management and future options[J]. Drugs, 2019, 79(2): 125-142. DOI: 10.1007/s40265-018-1039-7.
18. Graves J, Vinayagasundaram U, Mowry EM, et al. Effects of Rituximab on lymphocytes in multiple sclerosis and neuromyelitis optica[J]. Mult Scler Relat Disord, 2014, 3(2): 244-252. DOI: 10.1016/j.msard.2013.10.003.
19. Cree BA, Lamb S, Morgan K, et al. An open label study of the effects of Rituximab in neuromyelitis optica[J]. Neurology, 2005, 64(7): 1270-1272. DOI: 10.1212/01.wnl.0000159399.81861.d5.
20. Tahara M, Oeda T, Okada K, et al. Safety and efficacy of rituximab in neuromyelitis optica spectrum disorders (RIN-1 study): a multicentre, randomised, double-blind, placebo-controlled trial[J]. Lancet Neurol, 2020, 19(4): 298-306. DOI: 10.1016/s1474-4422(20)30066-1.
21. Yang CS, Yang L, Li T, et al. Responsiveness to reduced dosage of rituximab in Chinese patients with neuromyelitis optica[J]. Neurology, 2013, 81(8): 710-713. DOI: 10.1212/WNL.0b013e3182a1aac7.
22. Zhao S, Zhou H, Xu Q, et al. Efficacy of low-dose rituximab on neuromyelitis optica-associated optic neuritis[J/OL]. Front Neurol, 2021, 12: 637932[2021-05-04]. https://pubmed.ncbi.nlm.nih.gov/34017301/. DOI: 10.3389/fneur.2021.637932.
23. Redenbaugh V, Flanagan EP. Monoclonal antibody therapies beyond complement for NMOSD and MOGAD[J]. Neurotherapeutics, 2022, 19(3): 808-822. DOI: 10.1007/s13311-022-01206-x.
24. Mealy MA, Levy M. A pilot safety study of ublituximab, a monoclonal antibody against CD20, in acute relapses of neuromyelitis optica spectrum disorder[J/OL]. Medicine (Baltimore), 2019, 98 (25): e15944[2019-06-21]. https://pubmed.ncbi.nlm.nih.gov/31232925/. DOI: 10.1097/md.0000000000015944.
25. Kang C, Blair HA. Ofatumumab: a review in relapsing forms of multiple sclerosis[J]. Drugs, 2022, 82(1): 55-62. DOI: 10.1007/s40265-021-01650-7.
26. Taylor RP, Lindorfer MA. Immunotherapeutic mechanisms of anti-CD20 monoclonal antibodies[J]. Curr Opin Immunol, 2008, 20(4): 444-449. DOI: 10.1016/j.coi.2008.05.011.
27. Cree BAC, Bennett JL, Kim HJ, et al. Inebilizumab for the treatment of neuromyelitis optica spectrum disorder (N-MOmentum): a double-blind, randomised placebo-controlled phase 2/3 trial[J]. Lancet, 2019, 394(10206): 1352-1363. DOI: 10.1016/s0140-6736(19)31817-3.
28. Fujihara K, Bennett JL, de Seze J, et al. Interleukin-6 in neuromyelitis optica spectrum disorder pathophysiology[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2020, 7(5): e841[2020-08-20]. https://pubmed.ncbi.nlm.nih.gov/32820020/. DOI: 10.1212/nxi.0000000000000841.
29. Ringelstein M, Ayzenberg I, Harmel J, et al. Long-term therapy with interleukin 6 receptor blockade in highly active neuromyelitis optica spectrum disorder[J]. JAMA Neurol, 2015, 72(7): 756-763. DOI: 10.1001/jamaneurol.2015.0533.
30. Zhang C, Zhang M, Qiu W, et al. Safety and efficacy of tocilizumab versus azathioprine in highly relapsing neuromyelitis optica spectrum disorder (TANGO): an open-label, multicentre, randomised, phase 2 trial[J]. Lancet Neurol, 2020, 19(5): 391-401. DOI: 10.1016/s1474-4422(20)30070-3.
31. NPS MedicineWise. Satralizumab for neuromyelitis optica spectrum disorder[J]. Aust Prescr, 2022, 45(1): 32. DOI: 10.18773/austprescr.2021.065.
32. Yamamura T, Kleiter I, Fujihara K, et al. Trial of Satralizumab in neuromyelitis optica spectrum disorder[J]. N Engl J Med, 2019, 381(22): 2114-2124. DOI: 10.1056/NEJMoa1901747.
33. Traboulsee A, Greenberg BM, Bennett JL, et al. Safety and efficacy of satralizumab monotherapy in neuromyelitis optica spectrum disorder: a randomised, double-blind, multicentre, placebo-controlled phase 3 trial[J]. Lancet Neurol, 2020, 19(5): 402-412. DOI: 10.1016/s1474-4422(20)30078-8.
34. Stathopoulos P, Dalakas MC. The role of complement and complement therapeutics in neuromyelitis optica spectrum disorders[J]. Expert Rev Clin Immunol, 2022, 18(9): 933-945. DOI: 10.1080/1744666x.2022.2105205.
35. Pittock SJ, Berthele A, Fujihara K, et al. Eculizumab in aquaporin-4-positive neuromyelitis optica spectrum disorder[J]. N Engl J Med, 2019, 381(7): 614-625. DOI: 10.1056/NEJMoa1900866.
36. Kulasekararaj AG, Hill A, Rottinghaus ST, et al. Ravulizumab (ALXN1210) vs eculizumab in C5-inhibitor-experienced adult patients with PNH: the 302 study[J]. Blood, 2019, 133(6): 540-549. DOI: 10.1182/blood-2018-09-876805.
37. Shimizu F, Sano Y, Takahashi T, et al. Sera from neuromyelitis optica patients disrupt the blood-brain barrier[J]. J Neurol Neurosurg Psychiatry, 2012, 83(3): 288-297. DOI: 10.1136/jnnp-2011-300434.
38. Argaw AT, Asp L, Zhang J, et al. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease[J]. J Clin Invest, 2012, 122(7): 2454-2468. DOI: 10.1172/jci60842.
39. Lotan I, Levy M. New treatment perspectives for acute relapses in neuromyelitis optica spectrum disorder[J]. Transfus Med Rev, 2022, 36(4): 230-232. DOI: 10.1016/j.tmrv.2022.06.008.
40. Mealy MA, Shin K, John G, et al. Bevacizumab is safe in acute relapses of neuromyelitis optica[J]. Clin Exp Neuroimmunol, 2015, 6(4): 413-418. DOI: 10.1111/cen3.12239.
41. Dillon SR, Gross JA, Ansell SM, et al. An APRIL to remember: novel TNF ligands as therapeutic targets[J]. Nat Rev Drug Discov, 2006, 5(3): 235-246. DOI: 10.1038/nrd1982.
42. Wang H, Wang K, Zhong X, et al. Cerebrospinal fluid BAFF and APRIL levels in neuromyelitis optica and multiple sclerosis patients during relapse[J]. J Clin Immunol, 2012, 32(5): 1007-1011. DOI: 10.1007/s10875-012-9709-9.
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Pathogenesis and advances in monoclonal antibody treatment of neuromyelitis optica spectrum disorder

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