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September 2021; 8 (5) ArticleOpen Access

The Aryl Hydrocarbon Receptor–Dependent TGF-α/VEGF-B Ratio Correlates With Disease Subtype and Prognosis in Multiple Sclerosis

Ana Cirac, Thanos Tsaktanis, Tobias Beyer, Mathias Linnerbauer, Till Andlauer, Verena Grummel, Lucy Nirschl, Lena Loesslein, Francisco J. Quintana, Bernhard Hemmer, Veit Rothhammer
First published July 23, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001043
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Article Information

vol. 8 no. 5 e1043
DOI: 
https://doi.org/10.1212/NXI.0000000000001043
PubMed: 
34301821
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received January 17, 2021
  • Accepted in final form May 28, 2021
  • First Published July 23, 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. Ana Cirac, MD (a.cirac{at}tum.de),
    2. Thanos Tsaktanis, MD (thanos.tsaktanis{at}uk-erlangen.de),
    3. Tobias Beyer, MSc (t.beyer{at}tum.de),
    4. Mathias Linnerbauer, MSc (mathias.linnerbauer{at}fau.de),
    5. Till Andlauer, PhD (till.andlauer{at}tum.de),
    6. Verena Grummel, BSc (v.grummel{at}tum.de),
    7. Lucy Nirschl, BSc (lucy.nirschl{at}tum.de),
    8. Lena Loesslein, MSc (lena.loesslein{at}uk-erlangen.de),
    9. Francisco J. Quintana, PhD (fquintana{at}rics.bwh.harvard.edu),
    10. Bernhard Hemmer, MD (hemmer{at}tum.de) and
    11. Veit Rothhammer, MD
  1. Ana Cirac, MD (a.cirac{at}tum.de),
    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. Thanos Tsaktanis, MD (thanos.tsaktanis{at}uk-erlangen.de),
    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. Tobias Beyer, MSc (t.beyer{at}tum.de),
    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. German Research Foundation (DFG, RO4866/2-1)

    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. Mathias Linnerbauer, MSc (mathias.linnerbauer{at}fau.de),
    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. Till Andlauer, PhD (till.andlauer{at}tum.de),
    6. 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. Boehringer Ingelheim Pharma GmbH & Co. KG, Principal Scientist Human Genetics, 03/2021-present

    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. My salary was paid by the Max Planck Institute of Psychiatry and, subsequently, the Klinikum rechts der Isar, using third party funding by the German Federal Ministry of Education and Research (BMBF) through the Integrated Network IntegraMent, under the auspices of the e:Med Programme (grant 01ZX1614J) and through the DIFUTURE consortium of the Medical Informatics Initiative Germany (grant 01ZZ1804A), and by the European Union’s Horizon 2020 Research and Innovation Programme (grant MultipleMS, EU RIA 733161). None of these grants were awarded directly to me.

    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

  6. Verena Grummel, BSc (v.grummel{at}tum.de),
    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. Lucy Nirschl, BSc (lucy.nirschl{at}tum.de),
    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. Lena Loesslein, MSc (lena.loesslein{at}uk-erlangen.de),
    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. Francisco J. Quintana, PhD (fquintana{at}rics.bwh.harvard.edu),
    10. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. 2012 Editorial Board Member Systems Biomedicine 2012 Editorial Board Member Inmunologia (Spain) 2013- Associate Editor Immunology (UK) 2013- Senior Editorial Board Member American Journal of Clinical and Experimental Immunology 2014- Advisory Board MemberSeminars in Immunopathology

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Teva, Blueprint Medicines, AnTolRx

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. 1. EMD-Serono 2. Sanofi 3. Novartis 4. Teva 5. ONO

    Research Support, Government Entities:

    1. (1) NIH, R00 AI075285-01A2, Role PI, 2010-2012, (2) NIH, R01 AI093903-01, Role PI, 2011–2016, (3) NIH, K99AI075285-01A2, Role PI, 2009-2010, (4) NIH, 1R01NS102807-01A1, role PI, 09/01/18 – 08/31/23, (5) NIH, R01 ES025530-02, role PI, 06/01/16 – 05/31/21, (6) NMSS, JF 2161-A-5, role PI, 07/01/14 – 06/30/19, (7) American Cancer Soc., 126566-RSG-14-198-01-LIB, role PI, 01/01/15 – 12/31/18, (8) NMSS, RR-1601-07385, role PI, 10/01/16 – 09/30/19, (9) Israel Cancer Research Fund, 15-975-ICG, role PI, 09/01/16 – 08/30/19, (10) NIH-NIAID, 1R01AI126880-01A1, role PI, 02/01/17 – 01/31/22, (11) NIH-NIAID, 2R01HL095722-06A1, role PI, 09/01/15 – 08/31/20, (12) NMSS, PA-1604-08459, role PI, 06/01/17 – 05/31/21, (13) NMSS, PA-1604-08459, role PI, 06/01/17 – 05/31/21, (14) King Abdulaziz City for Science & Technology, 117427, role PI, 06/01/17 – 05/31/18, (15) NIH, 5R01DK108894-01, role Co-I, 02/01/17 – 01/31/22,

    Research Support, Academic Entities:

    1. (1) Harvard Medical School, Diversity and Community Partnership Faculty Fellowship, Role PI, 2010-2012, (2) BADERC, Pilot and Feasibility Award (Quintana), Role PI, 2010-2012

    Research Support, Foundations and Societies:

    1. (1) NMSS, RG4111A1/1, Role PI, 2009-2012, (2) NMSS, RG4048A11, Role Research Associate, 2008-2011

    Stock/Stock Options/Board of Directors Compensation:

    1. AnTolRx

    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. Bernhard Hemmer, MD (hemmer{at}tum.de) and
    11. Scientific Advisory Boards:

    1. Advisory Boards for Novartis, he has served as DMSC member for AllergyCare, TG Therapeutics and Polpharma Biologics

    Gifts:

    1. Me or my institution have received speaker honoraria from Desitin

    Funding for travel or speaker honoraria:

    1. Excemed

    Editorial Boards:

    1. Editorial board member of Jama Neurology, Experimental Neurology and Multiple sclerosis Journal

    Patents:

    1. I hold part of two patents; one for the detection of antibodies and T cells against KIR4.1 in a subpopulati on of MS patients and one for genetic determinants of neutralizing antibodies to interferon β

    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. Regeneron - not related

    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

  11. Veit Rothhammer, MD
    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. Novartis Pharmaceuticals, Research Support

    Research Support, Government Entities:

    1. German Research Foundation, RO4866, PI, 2018 - 2023 European Research Council, HICI, 2020 - 2024

    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 (A.C., T.T., T.B., M.L., T.A., V.G., L.N., B.H., V.R.), Klinikum Rechts der Isar, Technical University of Munich Department of Neurology (T.T., M.L., L.L., V.R.), University Hospital Erlangen, Friedrich Alexander University Erlangen-Nuernberg, Germany; Ann Romney Center for Neurologic Diseases (F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston; Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA; and Munich Cluster for Systems Neurology (SyNergy) (B.H.), Germany.
  1. Correspondence
    Prof. Dr. Rothhammer veit.rothhammer{at}uk-erlangen.de
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