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May 2019; 6 (3) ArticleOpen Access

PD1 pathway in immune-mediated myopathies

Pathogenesis of dysfunctional T cells revisited

Samuel Knauss, Corinna Preusse, Yves Allenbach, Sarah Leonard-Louis, Mehdi Touat, Norina Fischer, Helena Radbruch, Ronja Mothes, Vitali Matyash, Wolfgang Böhmerle, Matthias Endres, Hans-Hilmar Goebel, Olivier Benveniste, Werner Stenzel
First published April 10, 2019, DOI: https://doi.org/10.1212/NXI.0000000000000558
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Article Information

vol. 6 no. 3 e558
DOI: 
https://doi.org/10.1212/NXI.0000000000000558
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received September 7, 2018
  • Accepted in final form January 23, 2019
  • First Published April 10, 2019.
Copyright & Usage: 
Copyright © 2019 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. Samuel Knauss, MD,
    2. Corinna Preusse, PhD,
    3. Yves Allenbach, MD, PhD,
    4. Sarah Leonard-Louis, MD,
    5. Mehdi Touat, MD,
    6. Norina Fischer,
    7. Helena Radbruch, MD,
    8. Ronja Mothes,
    9. Vitali Matyash, PhD,
    10. Wolfgang Böhmerle, MD,
    11. Matthias Endres, MD,
    12. Hans-Hilmar Goebel, MD,
    13. Olivier Benveniste, MD, PhD and
    14. Werner Stenzel, MD
  1. Samuel Knauss, MD,
    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. Corinna Preusse, PhD,
    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. Yves Allenbach, MD, PhD,
    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. Sarah Leonard-Louis, MD,
    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. 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

  5. Mehdi Touat, MD,
    6. Scientific Advisory Boards:

    1. Agios Pharmaceuticals, Taiho Oncology, outside the submitted work.

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. Funding for travel from Agios Pharmaceuticals and Merck Sharp and Dohme, outside the submitted work.

    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. Research grants from Fondation pour la Recherche Medicale (FDM 41635).

    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. Norina Fischer,
    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. Helena Radbruch, MD,
    8. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) Novartis, (2) Sanofi

    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. (1)Novartis, (2) Sanofi

    Research Support, Government Entities:

    1. (1)Deutsche Forschungsgemeinschaft CRC 130 TP17

    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. Ronja Mothes,
    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. Vitali Matyash, PhD,
    10. 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

  10. Wolfgang Böhmerle, MD,
    11. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NOGGO e.V. speaker honoraria, BMS speaker honoraria

    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. NeuroCure Innovation and Flex-Fund, DZNE I2A project, BIH QUEST Replication challenge, BIH QUEST Validation fund

    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. Matthias Endres, MD,
    12. Scientific Advisory Boards:

    1. (1) non profit entity: safety monitoring board of STEMO study at the Center of Stroke research Berlin, no compensation (2) commercial entity: scientific advisory board Boehringer Ingelheim, honoraria paid to institution (3) commercial entity: scientific advisory board Bayer, honoraria paid to institution; (4) commercial entity: scientific advisory board Amgen, honoraria paid to institution; (5) commercial entity: scientific advisory board Covidien; honoraria paid to institution

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) Boehringer Ingelheim, speaker honoraria paid to institution (2) Pfizer, speaker honoraria paid to institution(3) Sanofi, speaker honoraria paid to institution (4) Bayer, speaker honoraria paid to institution,(5) BMS, speaker honoraria paid to institution (6) Ever, speaker honoraria paid to institution (7) GSK, speaker honoraria paid to institution (8) Amgen, speaker honoraria paid to institution; (9) Novartis, speaker honoraria paid to institution

    Editorial Boards:

    1. (1) Stroke, Editorial Board , no compensation, (2) Journal of Molecular Medicine, Editorial Board, no compensation (3) Neuropsychopharmacology, Editorial Board, compensation; (4) Aktuelle Neurologie, Editorial Board, compensation (modest); (5) Journal of the European Stroke Organization, Editorial board, no compenstaion

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. non profit entity: German Center for Neurodegenerative Diseases (DZNE), employment, compensation (modest)

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) Commercial entity Roche, unrestricted grant support to Dept Neurolgy Charite (2) Commercial entity Bayer, unrestricted grant support to the Dept Neurology and Center for Stroke Research Charite for Mondafis Trial (investigator initiated trial) and Berlin AF Registry (investigator initiated trial)

    Research Support, Government Entities:

    1. (1) German Ministry of Education and Science (BMBF) grant support (Center for Stroke Research Berlin, (2) Deutsche Forschungsgemeinschaft, grant support (ExcellenceCluster NeuroCure. SFB TR-43; KFO 247,KFO 213) (3) European Union (EUstroke, ARISE, Wake-Up) (4) German Center for Cardiovascular Research (DZHK) (5) Berlin site, German Center for Neurodegenerative Diseases (DZNE), Berlin site (6) Berlin Institute of Health (BiH)

    Research Support, Academic Entities:

    1. German Center for Cardiovascular Research (DZHK), Berlin site, German Center for Neurodegenerative Diseases (DZNE), Berlin site,(6) Berlin Institute of Health (BiH)

    Research Support, Foundations and Societies:

    1. (1) VolkswagenFoundation (Lichtenberg Professorship), (2) CoronaFoundation, (3) Fondation Leducq Transatlantic Network

    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. Hans-Hilmar Goebel, MD,
    13. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. editorial advisory board : Neuromuscular Disorders; Neuropathology and Applied Neurobiology, Brain Pathology, Clinical Neuropathology no compensation received from any journal

    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

  13. Olivier Benveniste, MD, PhD and
    14. Scientific Advisory Boards:

    1. Csl Behring Novartis LFB

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) CSL Behring: funding for travel at the ACR 2014 conference (2) LFB: funding for travel at the ICNMD 2014 conference, ACR 2017

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. (1) Novartis (2) CSL Behring (3) Neovacs

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) LFB,(2) Novartis, (3) Shire, (4) CSL Behring, (5) Neovacs

    Research Support, Government Entities:

    1. (1) DGOS/INSERM, (2) PHRC

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. (1) AFM, (2) The Myositis Association

    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

  14. Werner Stenzel, MD
    15. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. 1 Neuromuscular Disorders editorial board, 5 years 2 Neuropathology and Applied Neurobiology, editorial board, 4 years

    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.K., W.B., M.E.) and Department of Neuropathology (C.P., N.F., H.R., R.M., V.M., H.-H.G., W.S.), Charité—Universitätsmedizin, Berlin, Germany; Department of Internal Medicine and Clinical Immunology (Y.A., O.B.), Assistance Public-Hôpitaux de Paris, Sorbonne-Université, INSERM, UMR974, Pitié-Salpêtrière University Hospital; Unité de Pathologie Neuromusculaire (S.L.-L.), Centre de Référence Paris-Est, Groupe Hospitalier Pitié-Salpêtrière; Service de Neurologie 2-Mazarin (M.T.), Hôpitaux Universitaires La Pitié Salpêtrière—Charles Foix, APHP; OncoNeuroTox Group (M.T.), Center for Patients with Neurological Complications of Oncologic Treatments, Hôpitaux Universitaires Pitié-Salpetrière-Charles Foix et Hôpital Percy; Inserm U 1127 (M.T.), CNRS UMR 7225, Institut du Cerveau et de la Moelle épinière, ICM, Université Pierre-et-Marie-Curie, Sorbonne Université, Paris, France; Leibniz ScienceCampus Chronic Inflammation (H.R., R.M., W.S.); Center for Stroke Research Berlin (M.E.), Charité—Universitätsmedizin, Berlin; German Centre for Cardiovascular Research (DZHK) (M.E.); and German Center for Neurodegenerative Diseases (DZNE) (M.E.).
  1. Correspondence
    Dr. Stenzel werner.stenzel{at}charite.de
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