Neuromyelitis optica spectrum disorders and complement system: issues of pathogenesis and therapeutic options
https://doi.org/10.14412/2074-2711-2023-6-135-141
Abstract
An important component of the pathogenesis of neuromyelitis optica spectrum diseases (NMOSD) with antibodies to aquaporin-4 (AQP4-IgG) is a classical pathway of complement system (CS) activation with the implementation of mechanisms of complement-mediated cytotoxicity. Eculizumab is a humanized monoclonal antibody that suppresses the final stage of CS activation and has a high affinity for its C5 component. The most important components in the pathogenesis of NMOSD with AQP4-IgG, the role of CS, the results of clinical trials with the drug eculizumab and its place in the treatment of NMOSD are discussed.
Supporting agencies: This article has been supported by Generium
About the Author
V. S. Krasnov
Acad. I.P. Pavlov First Saint Petersburg State Medical University of Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
Vladimir Sergeevich Krasnov
6-8, L’va Tolstogo St., St. Petersburg 197022
Competing Interests:
The conflict of interest has not affected the results of the investigation
References
1. Bruscolini A, Sacchetti M, La Cava M, et al. Diagnosis and management of neuromyelitis optica spectrum disorders – An update. Autoimmun Rev. 2018 Mar;17(3):195-200. doi: 10.1016/j.autrev.2018.01.001. Epub 2018 Jan 13.
2. Krasnov VS, Bakhtiyarova KZ, Evdoshenko EP, et al. Consensus opinion on the management of patients with neuromyelitis optica spectrum diseases: issues of terminology and therapy. Nevrologiya, neiropsikhiatriya, psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2022;14(6):139-48. doi: 10.14412/2074-2711-2022-6-139-148 (In Russ.)].
3. Weinshenker BG, Wingerchuk DM. Neuromyelitis Spectrum Disorders. Mayo Clin Proc. 2017 Apr;92(4):663-79. doi: 10.1016/j.mayocp.2016.12.014
4. Whittam D, Wilson M, Hamid S, et al. What’s new in neuromyelitis optica? A short review for clinical neurologist. J Neurol. 2017 Nov;264(11):2330-4. doi: 10.1007/s00415-0178445-8
5. Wingerchuk DM, Banwell B, Bennett JL, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015 Jul 14;85(2):177-89. doi: 10.1212/WNL.0000000000001729
6. Lucchinetti СF, Guo Y, Popescu BFG, et al. The Pathology of an autoimmune astrocytopathy: lessons learned from neuromyelitis optica Brain Pathol. 2014 Jan;24(1):83-97. doi: 10.1111/bpa.12099
7. Levin MH, Bennett JL, Verkman AS. Optic neuritis in neuromyelitis optica. Prog Retin Eye Res. 2013 Sep;36:159-71. doi: 10.1016/j.preteyeres.2013.03.001
8. Wu Y, Zhong L, Geng J. Neuromyelitis optica spectrum disorder: Pathogenesis, treatment, and experimental models. Mult Scler Relat Disord. 2019 Jan;27:412-8. doi: 10.1016/j.msard.2018.12.002
9. Asavapanumas N, Tradtrantip L, Verkman AS. Targeting the complement system in neuromyelitis optica spectrum disorder. Expert Opin Biol Ther. 2021 Aug;21(8):1073-86. doi: 10.1080/14712598.2021.1884223
10. Höftberger R, Guo Y, Flanagan EP, et al. The pathology of central nervous system inflammatory demyelinating disease accompanying myelin oligodendrocyte glycoprotein autoantibody. Acta Neuropathol. 2020;139:87592. doi: 10.1007/s00401-020-02132-y
11. Takai Y, Misu T, Kaneko K, et al. Myelin oligodendrocyte glycoprotein antibody-associated disease: an immunopathological study. Brain. 2020;143:1431-46. doi: 10.1093/brain/awaa102
12. Nakashima I. Is MOG-IgG another biomarker for neuromyelitis optica? J Neurol Neurosurg Psychiatry. 2017 Oct;88(10):807. doi: 10.1136/jnnp-2017-316247
13. Hamid SHM, Whittam D, Mutch K, et al. What proportion of AQP4-IgG-negative NMO spectrum disorder patients are MOG-IgG positive? A cross sectional study of 132 patients. J Neurol. 2017 Oct;264(10):2088-94. doi: 10.1007/s00415-017-8596-7
14. Contentti EC, Rojas JI, Cristiano E, et al. Latin American consensus recommendations for management and treatment of neuromyelitis optica spectrum disorders in clinical practice. Mult Scler Relat Disord. 2020 Oct;45:102428. doi: 10.1016/j.msard.2020.102428
15. Kümpfel T, Giglhuber K, Aktas O, et al. Update on the diagnosis and treatment of neuromyelitis optica spectrum disorders (NMOSD) – revised recommendations of the Neuromyelitis Optica Study Group (NEMOS). Part II: Attack therapy and longterm management. J Neurol. 2023 Jul;270(7):3341-68. doi: 10.1007/s00415-02311634-0
16. Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci. 2013 Apr;14(4):265-77. doi: 10.1038/nrn3468
17. Simaniv TO, Krasnov VS, Kasatkin DS. Optikonevromielit v fokuse. Prakticheskoe rukovodstvo v skhemakh i tablitsakh [Opticoneuromyelitis in focus. Practical guidance in diagrams and tables]. Moscow: Prakticheskaya meditsina; 2023. 176 p. (In Russ.)].
18. Nagelhus EA, Ottersen OP. Physiological roles of aquaporin-4 in brain. Physiol Rev. 2013 Oct;93(4):1543-62. doi: 10.1152/physrev.00011.2013
19. Hinson SR, Romero MF, Popescu BFG, et al. Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci. 2011;109(4):1245-50. doi: 10.1073/pnas.1109980108. Epub 2011 Nov 29.
20. Day RE, Kitchen P, Owen DS, et al. Human aquaporins: regulators of transcellular water flow. Biochim Biophys Acta. 2014 May;1840(5):1492-506. doi: 10.1016/j.bbagen.2013.09.033
21. Saadoun S, Papadopoulos M. Role of membrane complement regulators in neuromyelitis optica. Mult Scler J. 2015;21(13):1644-54. doi: 10.1177/1352458515571446
22. Wingerchuk DM, Weinshenker BG. The emerging relationship between neuromyelitis optica and systemic rheumatologic autoimmune disease. Mult Scler J. 2012;18(1):510. doi: 10.1177/1352458511431077
23. Wang Y, Zhu M, Liu C. Blood Brain Barrier Permeability Could Be a Biomarker to Predict Severity of Neuromyelitis Optica Spectrum Disorders: A Retrospective Analysis. Front Neurol. 2018 Aug 7;9:648. doi: 10.3389/fneur.2018.00648
24. Krasnov VS, Makshakov GS, Kalinin IV, et al. Comorbidity of neuromyelitis optica spectrum disorder and systemic lupus erythematosus. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry. 2020;120(7):102-8. doi: 10.17116/jnevro2020120071102 (In Russ.).
25. Shahmohammadi S, Doosti R, Shahmohammadi A, et al. Neuromyelitis optica spectrum disorder (NMOSD) associated with cancer: A systematic review. Mult Scler Relat Disord. 2021 Nov;56:103227. doi: 10.1016/j.msard.2021.103227
26. Holers VM. Complement and its receptors: new insights into human disease. Annu Rev Immunol. 2014;32:433-59. doi: 10.1146/annurev-immunol-032713-120154
27. Pettigrew HD, Teuber SS, Gershwin ME. Clinical Significance of Complement Deficiencies. Ann N Y Acad Sci. 2009;1173(1):108-23. doi: 10.1111/j.17496632.2009.04633.x
28. Shakhidzhanov SS, Filippova AE, Butilin AA, Ataullakhanov FI. Pathologies of the complement system. Voprosy gematologii/onkologii i immunopatologii v pediatrii = Pediatric Hematology/Oncology and Immunopathology. 2019;18(3):130-44. doi: 10.24287/1726-1708-2019-18-3-130-144 (In Russ.).
29. Nytrova P, Potlukova E, Kemlink D, et al. Complement activation in patients with neuromyelitis optica. J Neuroimmunol. 2014 Sep 15;274(1-2):185-91. doi: 10.1016/j.jneuroim.2014.07.001
30. Kinoshita M, Nakatsuji Y, Moriya M, et al. Astrocytic necrosis is induced by anti-aquaporin-4 antibody-positive serum. Neuroreport. 2009 Mar 25;20(5):508-12. doi: 10.1097/wnr.0b013e32832776f4
31. Hinson SR, Pittock SJ, Lucchinetti CF, et al. Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology. 2007 Dec 11;69(24):2221-31. doi: 10.1212/01.WNL.0000289761.64862.ce
32. Zhang H, Bennett JL, Verkman AS. Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann Neurol. 2011 12;70(6):943-54. doi: 10.1002/ana.22551
33. Chen T, Lennon VA, Liu YU, et al. Astrocyte-microglia interaction drives evolving neuromyelitis optica lesion. J Clin Invest. 2020;130(8):4025-38. doi: 10.1172/JCI134816
34. 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. doi: 10.1007/s00401-017-1734-6
35. 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. doi: 10.1186/s12974-018-1333-z
36. 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. doi: 10.1186/s40478-019-0766-7
37. Levy M, Fujihara K, Palace J. New therapies for neuromyelitis optica spectrum disorder. Lancet Neurol. 2021 Jan;20(1):60-7. doi: 10.1016/S1474-4422(20)30392-6
38. 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):614-25. doi: 10.1056/NEJMoa1900866
39. Wingerchuk DM, Fujihara K, Palace J, et al. Long-Term Safety and Efficacy of Eculizumab in Aquaporin-4 IgG-Positive NMOSD. Ann Neurol. 2021 Jun;89(6):1088-98. doi: 10.1002/ana.26049
40. Palace J, Wingerchuk DM, Fujihara K, et al. Benefits of eculizumab in AQP4+ neuromyelitis optica spectrum disorder: Subgroup analyses of the randomized controlled phase 3 PREVENT trial. Mult Scler Relat Disord. 2021 Jan;47:102641. doi: 10.1016/j.msard.2020.102641
41. Pittock SJ, Fujihara K, Palace J, et al. Eculizumab monotherapy for NMOSD: Data from PREVENT and its open-label extension. Mult Scler J. 2022;28(3):480-6. doi: 10.1177/13524585211038291
42. Hemmer B. Diagnose und Therapie der Multiplen Sklerose, Neuromyelitis-opticaSpektrum-Erkrankungen und MOG-IgGassoziierten Erkrankungen, S2k-Leitlinie, 2021, in: Deutsche Gesellschaft für Neurologie (Hrsg.), Leitlinien für Diagnostik und Therapie in der Neurologie. Available from: www.dgn.org/leitlinien
43. Shosha E, Aljarallah SA, Fugham NA, et al. Saudi consensus recommendations on the management of neuromyelitis optica spectrum disorders (NMOSD). Mult Scler Relat Disord. 2022 Oct;66:104062. doi: 10.1016/j.msard.2022.104062
44. Chatterton S, Parratt JDE, Ng K. Eculizumab for acute relapse of neuromyelitis optica spectrum disorder: Case report. Front Neurol. 2022 Aug 8;13:951423. doi: 10.3389/fneur.2022.951423
45. Mao-Draayer Y, Thiel S, Mills EA, et al. Neuromyelitis optica spectrum disorders and pregnancy: therapeutic considerations. Nat Rev Neurol. 2020 Mar;16(3):154-70. doi: 10.1038/s41582-020-0313-y. Epub 2020 Feb 20.
Review
For citations:
Krasnov VS. Neuromyelitis optica spectrum disorders and complement system: issues of pathogenesis and therapeutic options. Nevrologiya, neiropsikhiatriya, psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2023;15(6):135-141. (In Russ.) https://doi.org/10.14412/2074-2711-2023-6-135-141
Views:
370
Email this article 