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November 2021; 8 (6) ArticleOpen Access

Intrathymic Plasmablasts Are Affected in Patients With Myasthenia Gravis With Active Disease

Yohei Yamamoto, Naoko Matsui, Akiyuki Uzawa, View ORCID ProfileYukiko Ozawa, Tetsuya Kanai, Fumiko Oda, Hiroyuki Kondo, View ORCID ProfileIzumi Ohigashi, Hiromitsu Takizawa, Kazuya Kondo, Mikio Sugano, Takashi Kitaichi, Hiroki Hata, Ryuji Kaji, Satoshi Kuwabara, Takashi Yamamura, Yuishin Izumi
First published September 24, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001087
Yohei Yamamoto
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Naoko Matsui
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Akiyuki Uzawa
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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  • For correspondence: auzawa@chiba-u.jp
Yukiko Ozawa
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Tetsuya Kanai
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Fumiko Oda
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Hiroyuki Kondo
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Izumi Ohigashi
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Hiromitsu Takizawa
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Kazuya Kondo
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Mikio Sugano
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Takashi Kitaichi
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Hiroki Hata
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Ryuji Kaji
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Satoshi Kuwabara
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Takashi Yamamura
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Yuishin Izumi
From the Department of Neurology (Y.Y., N.M., Y.I.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (A.U., Y.O., T. Kanai, F.O., S.K.), Graduate School of Medicine, Chiba University; Division of Experimental Immunology (H.K., I.O.), Institute of Advanced Medical Sciences, Tokushima University; Department of Thoracic, Endocrine Surgery and Oncology (H.T.), Tokushima University Graduate School of Biomedical Sciences; Department of Oncological Medical Services (K.K.), Tokushima University Graduate School of Biomedical Sciences; Department of Cardiovascular Surgery (M.S., T. Kitaichi, H.H.), Tokushima University Graduate School of Biomedical Sciences; Department of Neurology (R.K.), National Hospital Organization Utano Hospital, Kyoto; and Department of Immunology (T.Y.), National Institute of Neuroscience, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan.
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Citation
Intrathymic Plasmablasts Are Affected in Patients With Myasthenia Gravis With Active Disease
Yohei Yamamoto, Naoko Matsui, Akiyuki Uzawa, Yukiko Ozawa, Tetsuya Kanai, Fumiko Oda, Hiroyuki Kondo, Izumi Ohigashi, Hiromitsu Takizawa, Kazuya Kondo, Mikio Sugano, Takashi Kitaichi, Hiroki Hata, Ryuji Kaji, Satoshi Kuwabara, Takashi Yamamura, Yuishin Izumi
Neurol Neuroimmunol Neuroinflamm Nov 2021, 8 (6) e1087; DOI: 10.1212/NXI.0000000000001087

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Abstract

Background and Objectives To investigate intrathymic B lymphopoiesis in patients with myasthenia gravis (MG) and explore thymus pathology associated with clinical impact.

Methods Thymic lymphocytes from 15 young patients without MG, 22 adult patients without MG, 14 patients with MG without thymoma, and 11 patients with MG with thymoma were subjected to flow cytometry analysis of T follicular helper (Tfh), naive B, memory B, plasmablasts, CD19+B220high thymic B cells, B-cell activating factor receptor, and C-X-C chemokine receptor 5 (CXCR5). Peripheral blood mononuclear cells of 16 healthy subjects and 21 untreated patients with MG were also analyzed. Immunologic values were compared, and correlations between relevant values and clinical parameters were evaluated.

Results The frequencies of circulating and intrathymic plasmablasts were significantly higher in patients with MG than controls. On the other hand, the frequency of CD19+B220high thymic B cells was not increased in MG thymus. We observed a significant increase in CXCR5 expression on plasmablasts in MG thymus and an increased frequency of intrathymic plasmablasts that was correlated with preoperative disease activity. The frequency of intrathymic Tfh cells was significantly lower in patients who received immunosuppressive (IS) therapy than those without IS therapy. However, there was no significant difference in the frequency of intrathymic plasmablasts irrespective of IS therapy.

Discussion Our findings confirmed a correlation between increased frequency of intrathymic plasmablasts and disease activity before thymectomy. We postulate that activated intrathymic plasmablasts endow pathogenic capacity in MG.

Glossary

AChR=
acetylcholine receptor;
ADL=
activities of daily living;
BAFF-R=
B-cell activating factor receptor;
CXCR5=
C-X-C chemokine receptor 5;
GC=
germinal center;
HS=
healthy subjects;
IS=
immunosuppressive;
MFI=
mean fluorescence intensity;
MG=
myasthenia gravis;
PMBC=
peripheral blood mononuclear cell;
Tfh=
T follicular helper;
TFH=
thymic follicular hyperplasia;
TNF=
tumor necrosis factor

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • The Article Processing Charge was funded by the authors.

  • Received September 23, 2020.
  • Accepted in final form August 4, 2021.
  • Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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