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March 2021; 8 (2) ArticleOpen Access

Aryl Hydrocarbon Receptor Activation in Astrocytes by Laquinimod Ameliorates Autoimmune Inflammation in the CNS

Veit Rothhammer, Jessica E. Kenison, Zahorong Li, Emily Tjon, Maisa C. Takenaka, Chun-Cheih Chao, Kalil Alves de Lima, Davis M. Borucki, Joel Kaye, Francisco J. Quintana
First published January 6, 2021, DOI: https://doi.org/10.1212/NXI.0000000000000946
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Article Information

vol. 8 no. 2 e946
DOI: 
https://doi.org/10.1212/NXI.0000000000000946
PubMed: 
33408169
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received June 12, 2020
  • Accepted in final form November 4, 2020
  • First Published January 6, 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. Veit Rothhammer, MD (veit.rothhammer{at}tum.de),
    2. Jessica E. Kenison, MSc (jessica.kenison{at}antolrx.com),
    3. Zahorong Li, MSc (zli37{at}bwh.harvard.edu),
    4. Emily Tjon, MSc (emilyctjon{at}gmail.com),
    5. Maisa C. Takenaka, PhD (mcstakenaka{at}gmail.com),
    6. Chun-Cheih Chao, PhD (u911636{at}gmail.com),
    7. Kalil Alves de Lima, PhD (kalil.delima{at}gmail.com),
    8. Davis M. Borucki, MSc (boruckid{at}musc.edu),
    9. Joel Kaye, PhD (joel.k{at}ayalapharma.com) and
    10. Francisco J. Quintana, PhD
  1. Veit Rothhammer, MD (veit.rothhammer{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. 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

  2. Jessica E. Kenison, MSc (jessica.kenison{at}antolrx.com),
    3. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) AnTolRx, Inc. Funding for travel to conferences

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. (1) AnTolRx, Inc.

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) AnTolRx, Inc.

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. (1) Boston University

    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. (1) AnTolRx, Inc. (2016-present)

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  3. Zahorong Li, MSc (zli37{at}bwh.harvard.edu),
    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. Emily Tjon, MSc (emilyctjon{at}gmail.com),
    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. Maisa C. Takenaka, PhD (mcstakenaka{at}gmail.com),
    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. 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

  6. Chun-Cheih Chao, PhD (u911636{at}gmail.com),
    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. Kalil Alves de Lima, PhD (kalil.delima{at}gmail.com),
    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. Davis M. Borucki, MSc (boruckid{at}musc.edu),
    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. Joel Kaye, PhD (joel.k{at}ayalapharma.com) and
    10. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. Patents regarding Laquinimod: Patent US 8,598,203: Treatment of Crohn’s Disease with Laquinimod. Patent US 8,501,766: Treatment of Rheumatoid Arthritis with a Combination of Laquinimod and Methotrexate. Patent US 9,161,935: Use of Laquinimod for treating Crohn’s Disease patients who failed first-line anti-TNF therapy. Patent US 9,359,606: Anti-Clusterin Monotherapy for Cancer Treatment. 20130203807: Treatment of Ocular Inflammatory Diseases with Laquinimod. 20130259856: Treatment of Multiple Sclerosis with Combination of Laquinimod and Dimethyl Fumarate. 20130096158: Treatment of Multiple Sclerosis with Combination of Laquinimod and Fingolimid. 20140017226: Treatment of Multiple Sclerosis with Combination of Laquinimod and Fampridine. 20150094332: Laquinimod Combination Therapy For Treatment Of Multiple Sclerosis.

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. Currently employed by Ayala Pharmaceuticals (From December 2018) Previously employed by Teva Pharmaceutical Industries directly related to this manuscript

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. 1) Salary from Teva Pharmaceuticals

    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. I held stock options from Teva Pharmaceuticals, but once I left they were no longer available to me

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  10. Francisco J. Quintana, PhD
    11. 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

  1. From the Ann Romney Center for Neurologic Diseases (V.R., J.E.K., Z.L., E.T., M.C.T., C.-C.C., K.A.d.L., D.M.B., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Klinikum rechts der Isar (V.R.), Department of Neurology, Technical University of Munich, Germany; Department of Neurology (V.R.), University Hospital Erlangen, Friedrich–Alexander University Erlangen–Nürnberg, Germany; Ayala Pharmaceuticals (J.K.), Rehovot, Israel; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
  1. Correspondence
    Dr. Quintana fquintana{at}rics.bwh.harvard.edu
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