Interrogating the Genetic Determinants of Tourette’s Syndrome and Other Tic Disorders Through Genome-Wide Association Studies
Open accessAbstract
OBJECTIVE: Tourette's syndrome is polygenic and highly heritable. Genome-wide association study (GWAS) approaches are useful for interrogating the genetic architecture and determinants of Tourette's syndrome and other tic disorders. The authors conducted a GWAS meta-analysis and probed aggregated Tourette's syndrome polygenic risk to test whether Tourette's and related tic disorders have an underlying shared genetic etiology and whether Tourette's polygenic risk scores correlate with worst-ever tic severity and may represent a potential predictor of disease severity. METHODS: GWAS meta-analysis, gene-based association, and genetic enrichment analyses were conducted in 4,819 Tourette's syndrome case subjects and 9,488 control subjects. Replication of top loci was conducted in an independent population-based sample (706 case subjects, 6,068 control subjects). Relationships between Tourette's polygenic risk scores (PRSs), other tic disorders, ascertainment, and tic severity were examined. RESULTS: GWAS and gene-based analyses identified one genome-wide significant locus within FLT3 on chromosome 13, rs2504235, although this association was not replicated in the population-based sample. Genetic variants spanning evolutionarily conserved regions significantly explained 92.4% of Tourette's syndrome heritability. Tourette's-associated genes were significantly preferentially expressed in dorsolateral prefrontal cortex. Tourette's PRS significantly predicted both Tourette's syndrome and tic spectrum disorders status in the population-based sample. Tourette's PRS also significantly correlated with worst-ever tic severity and was higher in case subjects with a family history of tics than in simplex case subjects. CONCLUSIONS: Modulation of gene expression through noncoding variants, particularly within cortico-striatal circuits, is implicated as a fundamental mechanism in Tourette's syndrome pathogenesis. At a genetic level, tic disorders represent a continuous spectrum of disease, supporting the unification of Tourette's syndrome and other tic disorders in future diagnostic schemata. Tourette's PRSs derived from sufficiently large samples may be useful in the future for predicting conversion of transient tics to chronic tic disorders, as well as tic persistence and lifetime tic severity.
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- Authors
- Yu, D., Sul, J. H., Tsetsos, F., Nawaz, M. S., Huang, A. Y., Zelaya, I., Illmann, C., Osiecki, L., Darrow, S. M., Hirschtritt, M. E., Greenberg, E., Muller-Vahl, K. R., Stuhrmann, M., Dion, Y., Rouleau, G., Aschauer, H., Stamenkovic, M., Schlögelhofer, M., Sandor, P., Barr, C. L., Grados, M., Singer, H. S., Nöthen, M. M., Hebebrand, J., Hinney, A., King, R. A., Fernandez, T. V., Barta, C., Tarnok, Z., Nagy, P., Depienne, C., Worbe, Y., Hartmann, A., Budman, C. L., Rizzo, R., Lyon, G. J., McMahon, W. M., Batterson, J. R., Cath, D. C., Malaty, I. A., Okun, M. S., Berlin, C., Woods, D. W., Lee, P. C., Jankovic, J., Robertson, M. M., Gilbert, D. L., Brown, L. W., Coffey, B. J., Dietrich, A., Hoekstra, P. J., Kuperman, S., Zinner, S. H., Luðvigsson, P., Sæmundsen, E., Thorarensen, Ó., Atzmon, G., Barzilai, N., Wagner, M., Moessner, R., Ophoff, R., Pato, C. N., Pato, M. T., Knowles, J. A., Roffman, J. L., Smoller, J. W., Buckner, R. L., Willsey, A. J., Tischfield, J. A., Heiman, G. A., Stefansson, H., Stefansson, K., Posthuma, D., Cox, N. J., Pauls, D. L., Freimer, N. B., Neale, B. M., Davis, L. K., Paschou, P., Coppola, G., Mathews, C. A., Scharf, J. M., & on behalf of the Tourette Association of America International Consortium for Genetics, T. G. D. L. T. G. R. I.
- Affiliations
- Broad Institute (US)
- The Psychiatric and Neurodevelopmental Genetics Unit, Center for Genomic Medicine, Department of Psychiatry, Massachusetts General Hospital, Boston (Yu, Illmann, Osiecki, Smoller, Pauls, Neale, Scharf); the Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, Mass. (Yu, Neale, Scharf); the Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, University of California, Los Angeles (Sul, Huang, Zelaya, Ophoff, Freimer, Coppola); the...
- ORCID
- Yu, Dongmei
- Sul, Jae Hoon
- Tsetsos, Fotis
- Nawaz, Muhammad S.
- Osiecki, Lisa
- Darrow, Sabrina M.
- Hirschtritt, Matthew E.
- Greenberg, Erica
- Dion, Yves
- Rouleau, Guy
- Aschauer, Harald
- Schlögelhofer, Monika
- Sandor, Paul
- Barr, Cathy L.
- Grados, Marco
- Singer, Harvey S.
- Nöthen, Markus M.
- Hebebrand, Johannes
- Hinney, Anke
- King, Robert A.
- Fernandez, Thomas V.
- Barta, Csaba
- Depienne, Christel
- Worbe, Yulia
- Hartmann, Andreas
- Rizzo, Renata
- Lyon, Gholson J.
- Malaty, Irene A.
- Okun, Michael S.
- Woods, Douglas W.
- Lee, Paul C.
- Jankovic, Joseph
- Brown, Lawrence W.
- Dietrich, Andrea
- Hoekstra, Pieter J.
- Zinner, Samuel H.
- Sæmundsen, Evald
- Atzmon, Gil
- Barzilai, Nir
- Wagner, Michael
- Moessner, Rainald
- Ophoff, Roel
- Pato, Carlos N.
- Pato, Michele T.
- Knowles, James A.
- Roffman, Joshua L.
- Smoller, Jordan W.
- Buckner, Randy L.
- Willsey, A. Jeremy
- Tischfield, Jay A.
- Heiman, Gary A.
- Cox, Nancy J.
- Pauls, David L.
- Freimer, Nelson B.
- Neale, Benjamin M.
- Davis, Lea K.
- Paschou, Peristera
- Coppola, Giovanni
- Mathews, Carol A.
- Scharf, Jeremiah M.
- Venue
- American Journal of Psychiatry
- Published
- 2019-03-01
- Volume
- 176
- Issue
- 3
- Pages
- 217-227
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- PMC
- PMC6677250
- OpenAlex
- W2917071648
- Cited by
- 410
- References
- 29
- Citations by year
- 2026: 62 · 2025: 75 · 2024: 79 · 2023: 49 · 2022: 64 · 2021: 49 · 2020: 20 · 2019: 12
- FWCI
- 43.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
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- Funders
- U.S. Department of Defense
- U.S. Department of Health and Human Services (P30AG038072, U01HG004438, P30 NS062691, U01 HG004446)
- Michael J. Fox Foundation for Parkinson's Research
- Simons Foundation
- National Parkinson Foundation
- University of Florida Foundation
- Bachmann-Strauss Dystonia and Parkinson Foundation
- Dystonia Medical Research Foundation
- Amgen
- Eli Lilly and Company
- Pfizer
- McKnight Foundation
- Brigham and Women's Hospital
- Massachusetts General Hospital
- Yale University
- American Academy of Child and Adolescent Psychiatry
- Biogen
- CHDI Foundation
- Teva Pharmaceutical Industries
- Purdue University
- Alnylam Pharmaceuticals
- Children's Hospital of Philadelphia
- Vanderbilt University
- University of Miami
- Child Study Center, Yale School of Medicine
- Cincinnati Children's Hospital Medical Center
- Harvard University
- State University of New York
- University of Washington (CA089392)
- Johns Hopkins University (HHSN268200782096C, U01HG004438, P01 CA089392)
- Boston Scientific Corporation
- Harvard T.H. Chan School of Public Health
- McGill University
- Tourette Association of America
- Children's Mercy Hospital
- Rutgers, The State University of New Jersey
- Marquette University
- Vanderbilt University Medical Center (U01HG004438)
- Broad Institute
- Parkinson Alliance
- Parkinson's Foundation
- McGill University Health Centre
- Parkinson Study Group
- Acorda Therapeutics
- Psyadon Pharmaceuticals
- Neurocrine Biosciences
- Zynerba Pharmaceuticals
- Prothena
- Adamas Pharmaceuticals
- Revance
- Northwell Health
- University College London
- University of Oxford
- Deutsche Forschungsgemeinschaft (GZ MU 1527/3-1)
- Rijksuniversiteit Groningen
- Vrije Universiteit Amsterdam
- Semmelweis Egyetem
- Eberhard Karls Universität Tübingen
- Bundesministerium für Bildung und Forschung
- Lundbeckfonden
- University of Toronto
- Università di Catania
- Centre National de la Recherche Scientifique
- Universitair Medisch Centrum Groningen
- Háskóli Íslands
- Medizinischen Hochschule Hannover
- Hospital for Sick Children
- Trakya Üniversitesi
- Rheinische Friedrich-Wilhelms-Universität Bonn
- Universität Duisburg-Essen
- Assistance publique-Hôpitaux de Paris
- H. Lundbeck A/S
- National Institutes of Health (HHSN268200782096C, AA008401, CA089392, NS016648)
- Centers for Disease Control and Prevention (HHSN268200782096C)
- Directorate for Biological Sciences
- University of California, Los Angeles (P30 NS062691)
- Allergan
- University of California, San Francisco
- Parkinsonfonden
- Leonard M. Miller School of Medicine
- SUNY Downstate Medical Center
- Penn State College of Medicine
- Department of Biological Sciences, Purdue University
- Stanley Center for Psychiatric Research, Broad Institute
- Department of Psychology, Harvard University
- Roy J. and Lucille A. Carver College of Medicine, University of Iowa
- Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital
- National Institute on Alcohol Abuse and Alcoholism (HHSN268200782096C, AA008401, U10AA008401)
- National Institute on Aging (R01AG042188, P01AG021654, P30AG038072)
- National Institute of Mental Health (K23MH085057, MH085057, R01MH092293, R01MH115993, R01MH115963, R01MH115961, R01MH092290, R01MH092289, R01MH092291, R01MH092520, U01MH109536, R01MH092513, U24MH068457, R01MH096767, R01MH092516, R01MH085548, R01MH104964, R01MH092292, R01MH115958, R25MH077823, R01MH123451)
- National Institute on Drug Abuse (R01DA013423, HHSN268200782096C, DA013423)
- National Human Genome Research Institute (U01HG004422, U01HG004446, U01HG004438, HHSN268200782096C)
- National Cancer Institute (P01CA089392)
- National Institute of Nursing Research (R01NR014852)
- National Institute of Neurological Disorders and Stroke (R01NS102371, NS040024, K02NS085048, R01NS096008, R01NS016648, U01NS040024, R01NS040024, NS085048, R01NS105746, P30NS062691, NS016648, NS062691, NS040024-07S1)
- David Geffen School of Medicine, University of California, Los Angeles
- Jane and Terry Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles
- Weill Institute for Neurosciences, University of California, San Francisco
- Daiichi Sankyo Europe
- Dystonia Coalition
- Topics
- Social Sciences › Psychology › Clinical Psychology › Obsessive-Compulsive Spectrum Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- Tourette syndrome, tic disorders, polygenic risk score, genetic architecture, tic severity, FLT3, dorsolateral prefrontal cortex, corticostriatal circuits, non-coding variants, heritability, disease severity prediction
- MeSH terms
- Tourette Syndrome, Humans, Risk Factors, Severity of Illness Index, Tic Disorders, Case-Control Studies, Genetic Predisposition to Disease, Multifactorial Inheritance, Polymorphism, Single Nucleotide, fms-Like Tyrosine Kinase 3, Genome-Wide Association Study
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