Cited by 356Parkinson's Disease Mechanisms and TreatmentsGenetic Associations and EpidemiologyMultiple Sclerosis Research Studies

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Genome-wide Pleiotropy Between Parkinson Disease and Autoimmune Diseases

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Witoelar, Aree, Jansen, Iris E., Wang, Yunpeng, Desikan, Rahul S., Gibbs, J. Raphael, Blauwendraat, Cornelis, Thompson, Wesley K., Hernandez, Dena G., Djurovic, Srdjan, Schork, Andrew J., Bettella, Francesco, Ellinghaus, David, Franke, Andre, Lie, Benedicte A., McEvoy, Linda K., Karlsen, Tom H., Lesage, Suzanne, Morris, Huw R., Brice, Alexis, Wood, Nicholas W., Heutink, Peter, Hardy, John, Singleton, Andrew B., Dale, Anders M., Gasser, Thomas, Andreassen, Ole A., Sharma, Manu, for the International Parkinson’s Disease Genomics Consortium (IPDGC), North American Brain Expression Consortium (NABEC), and United Kingdom Brain Expression Consortium (UKBEC) Investigators·2017·JAMA Neurology

DOI 10.1001/jamaneurol.2017.0469PMC PMC5710535

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Abstract

Importance: Recent genome-wide association studies (GWAS) and pathway analyses supported long-standing observations of an association between immune-mediated diseases and Parkinson disease (PD). The post-GWAS era provides an opportunity for cross-phenotype analyses between different complex phenotypes. Objectives: To test the hypothesis that there are common genetic risk variants conveying risk of both PD and autoimmune diseases (ie, pleiotropy) and to identify new shared genetic variants and their pathways by applying a novel statistical framework in a genome-wide approach. Design, Setting, and Participants: Using the conjunction false discovery rate method, this study analyzed GWAS data from a selection of archetypal autoimmune diseases among 138 511 individuals of European ancestry and systemically investigated pleiotropy between PD and type 1 diabetes, Crohn disease, ulcerative colitis, rheumatoid arthritis, celiac disease, psoriasis, and multiple sclerosis. NeuroX data (6927 PD cases and 6108 controls) were used for replication. The study investigated the biological correlation between the top loci through protein-protein interaction and changes in the gene expression and methylation levels. The dates of the analysis were June 10, 2015, to March 4, 2017. Main Outcomes and Measures: The primary outcome was a list of novel loci and their pathways involved in PD and autoimmune diseases. Results: Genome-wide conjunctional analysis identified 17 novel loci at false discovery rate less than 0.05 with overlap between PD and autoimmune diseases, including known PD loci adjacent to GAK, HLA-DRB5, LRRK2, and MAPT for rheumatoid arthritis, ulcerative colitis and Crohn disease. Replication confirmed the involvement of HLA, LRRK2, MAPT, TRIM10, and SETD1A in PD. Among the novel genes discovered, WNT3, KANSL1, CRHR1, BOLA2, and GUCY1A3 are within a protein-protein interaction network with known PD genes. A subset of novel loci was significantly associated with changes in methylation or expression levels of adjacent genes. Conclusions and Relevance: The study findings provide novel mechanistic insights into PD and autoimmune diseases and identify a common genetic pathway between these phenotypes. The results may have implications for future therapeutic trials involving anti-inflammatory agents.

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Additional file 13 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567907
Additional file 15 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567949
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Additional file 10 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567871
Additional file 6 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15568021
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Additional file 7 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15568048
Additional file 5 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15568006
Additional file 2 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567961
Additional file 12 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567889
Additional file 2 of Epidemiologic association and shared genetic architecture between cataract and hearing difficulties among middle-aged and older adults
Zhang, X., Wang, S., Liu, S., Du, Z., Wu, G., Liang, Y., Huang, Y., Shang, X., Hu, Y., Zhu, Z., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25633042
Additional file 1 of Biomarker discovery in attention deficit hyperactivity disorder: RNA sequencing of whole blood in discordant twin and case-controlled cohorts
McCaffrey, T. A., St. Laurent, G., Shtokalo, D., Антонец, Д., Vyatkin, Y., Jones, D., Battison, E., & Nigg, J. T. (2020) · Figshare · doi:10.6084/m9.figshare.13160997
Additional file 3 of Biomarker discovery in attention deficit hyperactivity disorder: RNA sequencing of whole blood in discordant twin and case-controlled cohorts
McCaffrey, T. A., St. Laurent, G., Shtokalo, D., Антонец, Д., Vyatkin, Y., Jones, D., Battison, E., & Nigg, J. T. (2020) · Figshare · doi:10.6084/m9.figshare.13161003
Additional file 9 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15568078
Additional file 11 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567880
Additional file 2 of The landscape of rare genetic variation associated with inflammatory bowel disease and Parkinson’s disease comorbidity
Kars, M. E., Wu, Y., Stenson, P. D., Cooper, D. N., Burisch, J., Peter, I., & Itan, Y. (2024) · Figshare · doi:10.6084/m9.figshare.25815588
Additional file 8 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15568066
Additional file 1 of Epidemiologic association and shared genetic architecture between cataract and hearing difficulties among middle-aged and older adults
Zhang, X., Wang, S., Liu, S., Du, Z., Wu, G., Liang, Y., Huang, Y., Shang, X., Hu, Y., Zhu, Z., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25632901
Additional file 3 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567985
Additional file 14 of Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology
Houser, M. C., Caudle, W. M., Chang, J., Kannarkat, G. T., Yang, Y., Kelly, S. D., Oliver, D. L., Joers, V. L., Shannon, K. M., Keshavarzian, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.15567928
Additional file 2 of Genome-wide genetic links between amyotrophic lateral sclerosis and autoimmune diseases
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PD-1/PD-L1 signaling in neurological and psychiatric disorders: neuroimmune mechanisms and therapeutic potential
Chen, X., Wang, X., Li, C., Shan, K., Wang, L., Hashimoto, K., Shao, K., Wei, P., & Yang, J.-J. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106965 · Cited by 1

Authors: Witoelar, A., Jansen, I. E., Wang, Y., Desikan, R. S., Gibbs, J. R., Blauwendraat, C., Thompson, W. K., Hernandez, D. G., Djurovic, S., Schork, A. J., Bettella, F., Ellinghaus, D., Franke, A., Lie, B. A., McEvoy, L. K., Karlsen, T. H., Lesage, S., Morris, H. R., Brice, A., Wood, N. W., Heutink, P., Hardy, J., Singleton, A. B., Dale, A. M., Gasser, T., Andreassen, O. A., Sharma, M., & for the International Parkinson’s Disease Genomics Consortium (IPDGC), N. A. B. E. C. (.
Affiliations: Oslo University Hospital (NO)
German Center for Neurodegenerative Diseases (DE)
University of Oslo (NO)
University of California, San Francisco (US)
National Institutes of Health (US)
University of Copenhagen (DK)
University of California San Diego (US)
Christian-Albrechts-Universität zu Kiel (DE)
Institute of Clinical Molecular Biology, Christian Albrechts University of Kiel, Kiel, Germany
Centre National de la Recherche Scientifique (FR)
National Hospital for Neurology and Neurosurgery (GB)
UCL Queen Square Institute of Neurology (GB)
University College London (GB)
Hertie Institute for Clinical Brain Research (DE)
Corresponding author: Sharma, Manu
ORCID: Witoelar, Aree
Jansen, Iris E.
Wang, Yunpeng
Desikan, Rahul S.
Gibbs, J. Raphael
Blauwendraat, Cornelis
Thompson, Wesley K.
Hernandez, Dena G.
Djurovic, Srdjan
Schork, Andrew J.
Bettella, Francesco
Ellinghaus, David
Lie, Benedicte A.
McEvoy, Linda K.
Karlsen, Tom H.
Lesage, Suzanne
Morris, Huw R.
Brice, Alexis
Wood, Nicholas W.
Heutink, Peter
Hardy, John
Singleton, Andrew B.
Dale, Anders M.
Gasser, Thomas
Andreassen, Ole A.
Sharma, Manu
Venue: JAMA Neurology
Publisher: American Medical Association (AMA)
Published: 2017-07-01
Volume: 74
Issue: 7
Pages: 780
ISSN: 2168-6149 (ISSN-L)
DOI: 10.1001/jamaneurol.2017.0469
PMC: PMC5710535
OpenAlex: W2622719965
Semantic Scholar: 77f8aa61d1d32875fc37fcce3fe356cd20cd596e
Cited by: 352
References: 84
Citations by year: 2026: 14 · 2025: 39 · 2024: 60 · 2023: 41 · 2022: 39 · 2021: 62 · 2020: 34 · 2019: 30 · 2018: 24 · 2017: 7
FWCI: 18.08
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: JAMA Neurology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion, cc-by)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
HAL (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Site cant be reached (submittedVersion)
DZNE Pub (submittedVersion)
PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
Explore Bristol Research (submittedVersion)
Bristol Research (University of Bristol) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Newcastle University ePrints (Newcastle Univesity)
Funders: Biogen
Washington University in St. Louis
Johns Hopkins University
University of Rochester
Wellcome Trust
Sandwell and West Birmingham Hospitals NHS Trust
University Hospitals Birmingham NHS Foundation Trust
Université de Lille
Parkinson's UK (G-0907, J-0901, J-1402, K-1501)
Imperial College London
University College London
University of Oxford
Newcastle University
Cardiff University
University of Aberdeen
Institut National de la Santé et de la Recherche Médicale
Universiteit Leiden
Universiteit van Amsterdam
Radboud Universiteit
Vrije Universiteit Amsterdam
Eberhard Karls Universität Tübingen
Centre National de la Recherche Scientifique
Leids Universitair Medisch Centrum
Deutsches Zentrum für Neurodegenerative Erkrankungen
Université Pierre et Marie Curie
National Institutes of Health
Genentech
Medical Research Council
Erasmus Universitair Medisch Centrum Rotterdam
Helmholtz Zentrum München
National Human Genome Research Institute
National Institute of General Medical Sciences (R01GM104400)
National Institute of Neurological Disorders and Stroke
NIH Clinical Center
Topics: Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Keywords: Parkinson's disease, autoimmune disease, pleiotropy, type 1 diabetes, Crohn's disease, ulcerative colitis, rheumatoid arthritis, celiac disease, psoriasis, multiple sclerosis, LRRK2, HLA, MAPT, SETD1A, protein-protein interaction network, DNA methylation, gene expression, anti-inflammatory therapy
MeSH terms: Arthritis, Rheumatoid, Autoimmune Diseases, Celiac Disease, Colitis, Ulcerative, Crohn Disease, Diabetes Mellitus, Type 1, Humans, Multiple Sclerosis, Parkinson Disease, Psoriasis, Risk Factors, Genetic Predisposition to Disease, Genome-Wide Association Study, Genetic Loci, Genetic Pleiotropy

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