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November 2019; 6 (6) ArticleOpen Access

IL6 receptor358Ala variant and trans-signaling are disease modifiers in amyotrophic lateral sclerosis

Marlena Wosiski-Kuhn, Mac Robinson, Jane Strupe, Phonepasong Arounleut, Matthew Martin, James Caress, Michael Cartwright, Robert Bowser, Merit Cudkowicz, Carl Langefeld, Gregory A. Hawkins, Carol Milligan
First published October 14, 2019, DOI: https://doi.org/10.1212/NXI.0000000000000631
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Article Information

vol. 6 no. 6 e631
DOI: 
https://doi.org/10.1212/NXI.0000000000000631
PubMed: 
31611269
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received April 26, 2019
  • Accepted in final form August 28, 2019
  • First Published October 14, 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. Marlena Wosiski-Kuhn, BA,
    2. Mac Robinson, PhD,
    3. Jane Strupe, BS,
    4. Phonepasong Arounleut, BS,
    5. Matthew Martin, MD,
    6. James Caress, MD,
    7. Michael Cartwright, MD,
    8. Robert Bowser, PhD,
    9. Merit Cudkowicz, MD,
    10. Carl Langefeld, PhD,
    11. Gregory A. Hawkins, PhD and
    12. Carol Milligan, PhD
  1. Marlena Wosiski-Kuhn, BA,
    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. Mac Robinson, 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. Jane Strupe, BS,
    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. Phonepasong Arounleut, BS,
    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. Matthew Martin, MD,
    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. James Caress, MD,
    7. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Muscle & Nerve, Associate Editor, 2016-present

    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. Orion Pharmaceuticals Cytokinetics Incorporated

    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. Michael Cartwright, MD,
    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. Elsevier, Inc, 2012-present – royalties from sale of textbook

    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. Robert Bowser, PhD,
    9. Scientific Advisory Boards:

    1. 1)MT Pharma; 2) Above & Beyond, LLC.

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. 1)Scientific Reports, Editor, 2017 - present; 2) International Journal of Proteomics, Editor, 2010 - present; 3)American Journal of Neurodegenerative Disease, Senior Editorial Board, 2012-present

    Patents:

    1. 1)Biomarkers for the diagnosis and prognosis of ALS; 2) Biomarkers to monitor drug treatment of ALS and other neuromuscular disease patients; 3)Biomarkers for detecting and treating joint related pain.

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. 1)Iron Horse Diagnostics, Inc., President, 2012 - present.

    Consultancies:

    1. 1)Above & Beyond, LLC

    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. 1)NIH NS091299

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. 1)ALS Association; 2)Target ALS; 3) Muscular Dystrophy Association

    Stock/Stock Options/Board of Directors Compensation:

    1. 1)Iron Horse Diagnostics, Inc.

    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. Merit Cudkowicz, MD,
    10. Scientific Advisory Boards:

    1. Lilly DSMB

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Neurotherapeutics editorial board JAMA Neurology editorial board

    Patents:

    1. Metabolomics in ALS - patent MIR 155 inhibitor - patent

    Publishing Royalties:

    1. UptoDate MND chapter

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Cytokinetics, Biogen, Orion, ImmunityPharm, Biohaven, Avexis, Revalesio, MT Pharma

    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. NINDS - U01 NeuroNEXT

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. Muscular dystrophy association, als association, als finding a cure foundation, ALS One

    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. Carl Langefeld, PhD,
    11. Scientific Advisory Boards:

    1. (1) Oklahoma Medical Research Foundation, Wake Forest Nonhuman Primate Center (2) National Jewish Health

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (2) NIH; (2) National Jewish Health

    Editorial Boards:

    1. Rheumatic Disease Clinics

    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. U01 NS069763-01 08/01/2010 - 07/31/2016 NINDS Minorities with Ischemic Stroke Study (ERICH) PI of Biostatistics and Bioinformatics Center P01 AR048929 09/01/2011 – 08/30/2016 NIH Gene Expression in Pediatric Arthritis PI of Analysis Center Subcontract P30 CA12197 02/01/2012 – 01/31/2017 NCI Comprehensive Cancer Center of Wake Forest University- Cancer Center Support Grant Co-Investigator HG007112 -01 05/01/2012 – 03/31/2017 NIH Exome Sequencing to Identify CVD Risk Variants in Hispanic and African Americans Co-PI R01 DK090111-01 04/01/2011 - 03/31/2017 NIDDK Mapping Diabetes Susceptibility by expression traits in African Americans Co-Investigator R01 DK071891 07/01/2005 – 06/30/2017 NIDDK Subclinical DVD in African American Type 2 Diabetes Co-Investigator R21 DK106554 08/01/2015 – 07/31/2017 NIH Biomarkers for Molecular-Based-Decision-Making in Diagnosis and Treatment of Interstitial Cystitis Co-Investigator R01 HL 114587 06/01/2013 – 05/31/2018 NIH Genetic Risk for Granulomatous Interstitial Lung Disease PI of Subcontract R01 HL119962 07/01/2013 – 06/30/2018 NHLBI The Role of Hepatocyte ABCA1 in Lipid Metabolism and Transport Co-Investigator UG1 VA189824 08/01/2014 – 07/31/2019 NCI Wake Forest NCORP Research Base Co-Investigator R01 NS093870 02/01/2016 – 01/31/2021 NIH Recurrence of Stroke in Minority Populations Co-Investigator

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. RILITE Foundation 12/01/2015 – 11/30/2017 Informing Drug Repositioning and Development Through Genomics PI

    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. Gregory A. Hawkins, PhD 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. Current Support NOT related to current publication: 1 R03 AI137866-01 (PI: Hawkins) 04-1-2018 to 03-31-20 National Institute of Health TDC: $100,000 Development of IL6 Trans-signaling Mouse Model as a Shared Resource This project is to develop a mouse model that lacks incorporates a single nucleotide coding change that is predicted to make the IL6 receptor more susceptible to shedding. The mouse should model human subjects who inherit the IL6R Ala allele. If successful the model will be used in research related to neurodegenerative diseases, asthma, cancer and cardiovascular diseases. AL170130 (Hawkins, PI) 07/15/18-06/30/20 Department of the Army DC: $250,000 Generation of a Mouse Model to Investigate IL-6 Trans-signaling in ALS In this study, we are proposing that IL6 transsignaling plays a role in making ALS progression and severity worse. Based on our early study, we also propose that ALS patients that inherit the mutation in the IL6 receptor gene may develop ALS that progresses faster and is more severe. This study will investigate specific mechanisms in mouse models.

    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. Carol Milligan, PhD
    13. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Academic Editor- Neuroscience Journal, Hindawi (present)

    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. Support NOT related to study: 1 R03 AI137866-01 (PI: Hawkins; Milligan, co-PI) 04-1-2018 to 03-31-20 National Institute of Health TDC: $100,000 Development of IL6 Trans-signaling Mouse Model as a Shared Resource This project is to develop a mouse model that lacks incorporates a single nucleotide change to promote increased shedding in the mouse IL6 receptor to create a model of human subjects who inherit the Il6R Ala allele. If successful the model will be used in research related to neurodegenerative diseases, asthma, cancer and cardiovascular diseases. Role: co-PI Overlap: None AL170130 (Hawkins, PI) 07/15/18-06/30/20 Department of the Army DC: $250,000 Generation of a Mouse Model to Investigate IL-6 Trans-signaling in ALS In this study, we are proposing that IL6 transsignaling plays a role in making ALS progression and severity worse. Based on our early study, we also propose that ALS patients that inherit the mutation in the IL6 receptor gene may develop ALS that progresses faster and is more severe. This studies utilizes mouse models to investigate specific mechanisms. Role: co-I Overlap: None NIH 5R25NS089458 08/01/2015- 07/31/2020 (NCE) National Institute of Health TDC – 1,165,910 Training in Health Disparity Research for a Diverse Neuroscience Workforce This is a new Master’s Program specifically developed to broaden educational opportunities for individuals interested in pursuing a career in Health Disparities in Neuroscience-related Disorders (HDND). The overall goal is to train individuals who will contribute to expanding diversity in the Neuroscience work-force. Role: co-PI Overlap: None

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. Blazeman Foundation for ALS (Milligan)

    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 Neurobiology and Anatomy (M.W.-K., M.R., J.S., P.A., M.M., C.M.); Department of Neurology (J.C., M. Cartwright); and Department of Biochemistry (G.A.H.), Wake Forest School of Medicine; Division of Public Health (C.L.), Department of Biostatistical Sciences, Wake Forest School of Medicine; Departments of Neurology and Neurobiology (R.B.), Barrow Neurological Institute & St. Joseph's Hospital and Medical Center; Department of Neurology (M. Cudkowicz), Neurological Clinical Research Institute, Massachusetts General Hospital, Harvard Medical School; and Current Address Department of Pediatrics (M.M.), Nationwide Children's Hospital, Columbus OH.
  1. Correspondence
    Dr. Milligan milligan{at}wakehealth.edu
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