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March 2021; 8 (2) ArticleOpen Access

Immune Skew of Circulating Follicular Helper T Cells Associates With Myasthenia Gravis Severity

Shinji Ashida, Hirofumi Ochi, Mio Hamatani, Chihiro Fujii, Kimitoshi Kimura, Yoichiro Okada, Yuichiro Hashi, Kazuyuki Kawamura, Hideki Ueno, Ryosuke Takahashi, Toshiki Mizuno, Takayuki Kondo
First published January 12, 2021, DOI: https://doi.org/10.1212/NXI.0000000000000945
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Article Information

vol. 8 no. 2 e945
DOI: 
https://doi.org/10.1212/NXI.0000000000000945
PubMed: 
33436376
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received June 5, 2020
  • Accepted in final form November 4, 2020
  • First Published January 12, 2021.
Copyright & Usage: 
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.

Author Disclosures

    1. Shinji Ashida, MD (shinji-a{at}koto.kpu-m.ac.jp),
    2. Hirofumi Ochi, MD, PhD (hochi{at}m.ehime-u.ac.jp),
    3. Mio Hamatani, MD, PhD (kawa30{at}kuhp.kyoto-u.ac.jp),
    4. Chihiro Fujii, MD, PhD (chihirof{at}koto.kpu-m.ac.jp),
    5. Kimitoshi Kimura, MD, PhD (kimura{at}kuhp.kyoto-u.ac.jp),
    6. Yoichiro Okada, MD, PhD (okady{at}kuhp.kyoto-u.ac.jp),
    7. Yuichiro Hashi, MD (hashiu{at}kuhp.kyoto-u.ac.jp),
    8. Kazuyuki Kawamura, MD, PhD (kawamura.kazuyuki.tg{at}mail.hosp.go.jp),
    9. Hideki Ueno, MD, PhD (ueno.hideki.8e{at}kyoto-u.ac.jp),
    10. Ryosuke Takahashi, MD, PhD (ryosuket{at}kuhp.kyoto-u.ac.jp),
    11. Toshiki Mizuno, MD, PhD (mizuno{at}koto.kpu-m.ac.jp) and
    12. Takayuki Kondo, MD, PhD
  1. Shinji Ashida, MD (shinji-a{at}koto.kpu-m.ac.jp),
    2. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  2. Hirofumi Ochi, MD, PhD (hochi{at}m.ehime-u.ac.jp),
    3. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  3. Mio Hamatani, MD, PhD (kawa30{at}kuhp.kyoto-u.ac.jp),
    4. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  4. Chihiro Fujii, MD, PhD (chihirof{at}koto.kpu-m.ac.jp),
    5. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. Grants from JSPS KAKENHI (Grant No. 19K16923), Lead investigator, 2019-2021

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. The Shimizu Foundation for Immunology and Neuroscience

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  5. Kimitoshi Kimura, MD, PhD (kimura{at}kuhp.kyoto-u.ac.jp),
    6. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1)Mitsubishi Tanabe Pharma Corporation, travel/speaker honoraria (2)Takeda Pharmaceutical Co. Ltd., travel/speaker honoraria (3)Biogen Idec, travel/speaker honoraria (4)Japan Blood Products Organization, travel/speaker honoraria

    Editorial Boards:

    1. NONE

    Patents:

    1. (1) A method of collecting data to predict good response to plasmapheresis in autoimmune diseases (only in Japan)

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1)Novartis Pharmaceuticals (2)Japan Blood Products Organization

    Research Support, Government Entities:

    1. (1)AMED (Japan), JP19ek0109382, principal investigator, 2018- 2019 (2)JSPS KAKENHI (Japan), JP18K15473, principal investigator, 2018-

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. (1)Fujiwara Kinen Zaidan, (2)Konishi Foundation for International Exchange, (3)Takeda Science Foundation, (4)Mochida Memorial Foundation for Medical and Pharmaceutical Research, (5)KANAE Fondation for the Promotion of Medical Science

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  6. Yoichiro Okada, MD, PhD (okady{at}kuhp.kyoto-u.ac.jp),
    7. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  7. Yuichiro Hashi, MD (hashiu{at}kuhp.kyoto-u.ac.jp),
    8. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  8. Kazuyuki Kawamura, MD, PhD (kawamura.kazuyuki.tg{at}mail.hosp.go.jp),
    9. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  9. Hideki Ueno, MD, PhD (ueno.hideki.8e{at}kyoto-u.ac.jp),
    10. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Frontiers in Immunology, Editorial board, since 2016

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. EMD Serono

    Research Support, Government Entities:

    1. NIH U19-AI082715, PI of Project 1, 2019 AMED, PI, 2019, 2020

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  10. Ryosuke Takahashi, MD, PhD (ryosuket{at}kuhp.kyoto-u.ac.jp),
    11. Scientific Advisory Boards:

    1. (1) KAN Research Institute INC., Scientific Advisory Board (2) DAINIPPON SUMITOMO PHARMA., Scientific Advisory Board (3) Japan Agency of Medical Research and Development, Program Supervisor of a Regenerative Medicine Medicine Research Project

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) Novartis Pharma Japan, honoraria for lectures (2) Boehringer Ingelheim Japan, honoraria for lectures (3) GlaxoSmithKline Japan, honoraria for lectures (4) Dainippon Sumitomo Pharma, honoraria for lectures (5) FP pharmaceuticals, honoraria for lectures (6) Mitsubishi Tanabe Pharma, honoraria for lectures (7) Kyowa Hakko Kirin Co., honoraria for lectures (8) Otsuka Pharmaceutical Co., honoraria for lectures

    Editorial Boards:

    1. (1) Journal of Neural Transmission, Editorial Board, 11 years (2) Neurology and Clinical Neuroscience, Editorial Board, 6 years (3) Experimental Neurobiology, Editorial Board, 7 years (4) Movement Disorders, Editorial Board, 6 years (5) Molecular Brain, Editorial Board, 3 year

    Patents:

    1. (1) The use of Mutant mouse of Chimaerin for drug screening (2) Drug Screening using iPS cells

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) Novartis Pharma Japan (2) Boehringer Ingelheim Japan (3) Dainippon Sumitomo Pharma (4)Eisai Pahrma

    Research Support, Government Entities:

    1. (1) Ministry of Education, Culture, Sports, Science and Technology, Japan (2) Ministry of health labor and welfare, Japan (3) Japan Agency for Medical Research and Development

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  11. Toshiki Mizuno, MD, PhD (mizuno{at}koto.kpu-m.ac.jp) and
    12. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  12. Takayuki Kondo, MD, PhD
    13. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  1. From the Department of Neurology (S.A., C.F., T.M.), Graduate School of Medical Science, Kyoto Prefectural University of Medicine; Department of Geriatric Medicine and Neurology (H.O.), Ehime University Graduate School of Medicine, Toon; Department of Neurology (M.H., R.T.), Kyoto University Graduate School of Medicine; Department of Neurology (M.H., Y.O., Y.H., T.K.), Kansai Medical University Medical Center, Osaka, Japan; Brigham and Women's Hospital (K. Kimura), Harvard Medical School, Boston, MA; Department of Neurology (K. Kawamura), National Hospital Organization Minami Kyoto Hospital; and Department of Immunology (H.U.), Kyoto University Graduate School of Medicine, Japan.
  1. Correspondence
    Dr. Kondo takakon78{at}hotmail.com
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