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January 2023; 10 (1) Research ArticleOpen Access

More Efficient Complement Activation by Anti–Aquaporin-4 Compared With Anti–Myelin Oligodendrocyte Glycoprotein Antibodies

Magdalena Lerch, Kathrin Schanda, Eliott Lafon, Reinhard Würzner, Sara Mariotto, View ORCID ProfileAlessandro Dinoto, Eva Maria Wendel, Christian Lechner, Harald Hegen, Kevin Rostásy, Thomas Berger, Doris Wilflingseder, Romana Höftberger, View ORCID ProfileMarkus Reindl
First published November 22, 2022, DOI: https://doi.org/10.1212/NXI.0000000000200059
Magdalena Lerch
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Kathrin Schanda
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Eliott Lafon
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Reinhard Würzner
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Sara Mariotto
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Alessandro Dinoto
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Eva Maria Wendel
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Christian Lechner
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Harald Hegen
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Kevin Rostásy
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Thomas Berger
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Doris Wilflingseder
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Romana Höftberger
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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Markus Reindl
From the Clinical Department of Neurology (M.L., K.S., H.H., M.R.), Medical University of Innsbruck, Austria; Institute of Hygiene and Medical Microbiology (E.L., R.W., D.W.), Medical University of Innsbruck, Austria; Neurology Unit (S.M., A.D.), Department of Neuroscience, Biomedicine, and Movement Sciences, University of Verona, Italy; Department of Pediatric Neurology (E.M.W.), Olgahospital/Klinikum Stuttgart, Germany; Department of Pediatrics I (C.L.), Medical University of Innsbruck, Austria; Paediatric Neurology (K.R.), Witten/Herdecke University, Children's Hospital Datteln, Germany; Department of Neurology (T.B.), Medical University of Vienna, Austria; and Division of Neuropathology and Neurochemistry (C.L., R.H.), Department of Neurology, Medical University of Vienna, Austria.
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More Efficient Complement Activation by Anti–Aquaporin-4 Compared With Anti–Myelin Oligodendrocyte Glycoprotein Antibodies
Magdalena Lerch, Kathrin Schanda, Eliott Lafon, Reinhard Würzner, Sara Mariotto, Alessandro Dinoto, Eva Maria Wendel, Christian Lechner, Harald Hegen, Kevin Rostásy, Thomas Berger, Doris Wilflingseder, Romana Höftberger, Markus Reindl
Neurol Neuroimmunol Neuroinflamm Jan 2023, 10 (1) e200059; DOI: 10.1212/NXI.0000000000200059

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    Figure 1 AQP4-IgG–Positive Serum Samples Show Stronger Complement Activation Than MOG-IgG–Positive Serum Samples

    (A) CDC (shown as percentage of lysis buffer determined by the LDH assay) of 68 MOG-IgG–positive human serum samples (blue circles; MOGα1-EGFP–transfected cells) and 39 AQP4-IgG–positive human serum samples (red triangles; AQP4-M23-EmGFP–transfected cells) is plotted against the antibody titers. Semi-log linear regression lines are shown. Spearman correlation: MOG: r = 0.58, p < 0.0001; AQP4: r = 0.71, p < 0.0001. (B) Violin plot (dashed line: median, dotted lines: quartiles) of all MOG-IgG (blue; n = 68) and AQP4-IgG (red; n = 39) positive serum samples tested is shown. Asterisks indicate the statistical difference of a Mann-Whitney test: ****p < 0.0001. The solid lines indicate the cutoff levels (mean + 2SD of cells treated with complement alone). (C) Percentage of MOG-IgG (blue) or AQP4-IgG (red) positive samples above the cutoff level (mean + 2SD of cells treated with complement alone) is demonstrated as bar graph. (D) The predictive role of MOG-IgG and AQP4-IgG antibody titers and status, age, and sex on complement-dependent cell lysis were analyzed by multivariate regression (R = 0.827, R2 = 0.684, F = 53.1, p < 0.001). Standardized regression coefficient beta is shown with 95% CI. ***p < 0.001. AQP4 = aquaporin-4; CDC = complement-dependent cytotoxicity; LB = lysis buffer; MOG = myelin oligodendrocyte glycoprotein.

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    Figure 2 Complement Activation on Different MOG Isoforms

    (A) Comparison of CDC (as percentage of lysis buffer) of MOG-IgG–positive serum samples (n = 68) with 6 different MOG isoforms (MOGα1-3 and MOGβ1-3) is shown as a scatter dot plot. Bars indicate medians with interquartile range (Friedman test with post hoc Dunn: *p < 0.05, ***p < 0.001, and ****p < 0.0001). The solid line indicates the cutoff level (mean + 2SD of cells treated with complement alone). (B) Shows the percentage of MOG-IgG–positive serum samples above the cutoff value (mean + 2SD of cells treated with complement alone) for the 6 MOG isoforms. The percentages are plotted according to their respective binding patterns (α1β1, α1-3β1, and α1-3β1-3; values are given within the bars). AQP4 = aquaporin-4; LB = lysis buffer; MOG = myelin oligodendrocyte glycoprotein.

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    Figure 3 Quantification of TCC Deposition

    TCC deposition after complement activation of either MOGα1-EGFP (blue) or AQP4-EmGFP (red) transfected HEK293A cells by MOG-IgG or AQP4-IgG–positive serum samples together with human complement was quantified using an flow cytometry assay. (A) Mean fluorescence intensity (MFI) values are plotted against the antibody titers. The lines show semi-log linear regression. Spearman correlation: MOG: r = 0.56, p < 0.05, n = 19; AQP4: r = 0.77, p < 0.001, n = 19. (B) Comparison of MFI values between MOG (n = 19) and AQP4 (n = 19) is shown as violin plot (dashed line: median, dotted lines: quartiles). Mann-Whitney test: **p = 0.002. (C) The MFI values of TCC deposition of human sera are plotted against the respective values from the LDH assay (see Figure 1). Spearman correlation: MOG: r = 0.48, p < 0.05, n = 19; AQP4: r = 0.57, p < 0.05, n = 19. AQP4 = aquaporin-4; LDH = lactate dehydrogenase; MFI = mean fluorescence intensity; MOG = myelin oligodendrocyte glycoprotein; TCC = terminal complement complex.

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