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Genome-wide association study of Tourette's syndrome

Abstract

Tourette's syndrome (TS) is a developmental disorder that has one of the highest familial recurrence rates among neuropsychiatric diseases with complex inheritance. However, the identification of definitive TS susceptibility genes remains elusive. Here, we report the first genome-wide association study (GWAS) of TS in 1285 cases and 4964 ancestry-matched controls of European ancestry, including two European-derived population isolates, Ashkenazi Jews from North America and Israel and French Canadians from Quebec, Canada. In a primary meta-analysis of GWAS data from these European ancestry samples, no markers achieved a genome-wide threshold of significance (P<5 × 10−8); the top signal was found in rs7868992 on chromosome 9q32 within COL27A1 (P=1.85 × 10−6). A secondary analysis including an additional 211 cases and 285 controls from two closely related Latin American population isolates from the Central Valley of Costa Rica and Antioquia, Colombia also identified rs7868992 as the top signal (P=3.6 × 10−7 for the combined sample of 1496 cases and 5249 controls following imputation with 1000 Genomes data). This study lays the groundwork for the eventual identification of common TS susceptibility variants in larger cohorts and helps to provide a more complete understanding of the full genetic architecture of this disorder.

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Acknowledgements

We are grateful to all the patients with Tourette's syndrome who generously agreed to participate in this study. Furthermore, the members of the Tourette Syndrome Association International Consortium for Genetics are deeply indebted to the Tourette Syndrome Association for their guidance and support. We also thank Libby Bernier and Janelle Alabiso for their assistance in manuscript preparation and Stephan Ripke for help with meta-analysis figures. This work was supported by a grant from the Judah Foundation, NIH Grants NS40024 to DLP and the Tourette Syndrome Association International Consortium for Genetics, NIH Grant NS16648 and a grant from the Tourette Syndrome Association to DLP, NIH Grant NS037484 to NBF, NIH Grant NS043538 to AR-L, American Recovery and Re-investment Act (ARRA) awards NS40024-07S1 and NS16648-29S1 to DLP, NIH Grant MH079489, and an American Academy of Neurology Foundation Grant and NIH Grant MH085057 to JMS. The Broad Institute Center for Genotyping and Analysis was supported by Grant U54 RR020278 from the National Center for Research Resources. Support was also provided by the New Jersey Center for Tourette Syndrome & Associated Disorders (through New Jersey Department of Health and Senior Services: 08-1827-FS-N-0) to GAH and JAT and P01MH049351, R01MH061940, K05MH076273 and T32MH018268 to JFL. Funding support for generation of the eQTL data was provided by the UK Medical Research Council and the Intramural Research Program of the National Institute on Aging, National Institutes of Health, Department of Health and Human Services project Z01 AG000932-02. Funding support for the Study of Addiction: Genetics and Environment (SAGE) was provided through the NIH Genes, Environment and Health Initiative [GEI] (U01 HG004422). SAGE is one of the genome-wide association studies funded as part of the Gene Environment Association Studies (GENEVA) under GEI. Assistance with phenotype harmonization and genotype cleaning, as well as with general study coordination, was provided by the GENEVA Coordinating Center (U01 HG004446). Assistance with data cleaning was provided by the National Center for Biotechnology Information. Support for collection of data sets and samples was provided by the Collaborative Study on the Genetics of Alcoholism (COGA; U10 AA008401), the Collaborative Genetic Study of Nicotine Dependence (COGEND; P01 CA089392) and the Family Study of Cocaine Dependence (FSCD; R01 DA013423). Funding support for genotyping, which was performed at the Johns Hopkins University Center for Inherited Disease Research, was provided by the NIH GEI (U01HG004438), the National Institute on Alcohol Abuse and Alcoholism, the National Institute on Drug Abuse and the NIH contract ‘High throughput genotyping for studying the genetic contributions to human disease’ (HHSN268200782096C). The data sets used for the analyses described in this manuscript were obtained from dbGaP at http://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/study.cgi?study_id=phs000092.v1.p1 through dbGaP accession number phs000092.v1.p. None of the funding agencies for this project (NINDS, NIMH, the Tourette Syndrome Association and the Judah Foundation) had any influence or played any role in (1) the design or conduct of the study; (2) management, analysis or interpretation of the data; and (3) preparation, review or approval of the manuscript.

Author contributions

Manuscript preparation: JM Scharf, D Yu, CA Mathews, BM Neale, SE Stewart, JA Fagerness, E Gamazon, NB Freimer, NJ Cox and DL Pauls.

Study design: JM Scharf, D Yu, CA Mathews, BM Neale, SE Stewart, JA Fagerness, S Purcell, P Heutink, BA Oostra, WM McMahon, NB Freimer, NJ Cox and DL Pauls.

Data analysis: D Yu, BM Neale, JM Scharf, P Evans, E Gamazon, CK Edlund, SK Service, SE Stewart, A Tikhomirov, A Pluzhnikov, A Konkashbaev, LK Davis, B Han, D Posthuma, E Eskin, C Sabatti, DV Conti, JA Knowles, NB Freimer, S Purcell and NJ Cox.

Project management: JM Scharf, JA Fagerness and DL Pauls.

Sample management and processing: JA Fagerness, JM Scharf, J Crane, P Moorjani and DL Pauls.

Genotyping: AT Crenshaw, MA Parkin and DB Mirel.

Phenotype management: CA Mathews, JM Scharf, L Osiecki, C Illmann, SE Stewart, W McMahon and DL Pauls.

Case sample collection:

European Ancestry Samples (ordered by numbers of submitted samples): Yale University: RA King (Site PI), TV Fernandez, KK Kidd, JR Kidd, JF Leckman, AJ Pakstis, MW State; Utrecht University/VU Medical Center: DC Cath (Site PI), JH Smit, P Heutink; University of Toronto: P Sandor (Site PI), CL Barr, N Phan; Massachusetts General Hospital: DL Pauls (Site PI), C Illmann, L Osiecki, JM Scharf; University of Utah: WM McMahon (Site PI), G Lyon, M Leppert, J Morgan, R Weiss; Johns Hopkins School of Medicine: MA Grados (Site PI), K Anderson, S Davarya, H Singer, J Walkup; Baylor College of Medicine: J Jankovic (Site PI); Rutgers University: JA Tischfield (Site PI), GA Heiman, RA King; University of Cincinnati: DL Gilbert (Site PI); University of Groningen: PJ Hoekstra(Site PI); University College London: MM Robertson (Site PI); UCSF: CA Mathews (Site PI), VI Reus, TL Lowe, P Lee, M Rangel-Lugo; University of Rochester School of Medicine: R Kurlan (Site PI).

French Canadian Samples: University of Montreal: GA Rouleau (Site PI), S Chouinard, Y Dion, S Girard.

Ashkenazi Jewish Samples: UCSF: CA Mathews (Site PI), VI Reus, TL Lowe, M Rangel-Lugo. Shaare Zedek Medical Center: V Gross-Tsur (Site PI), Y Pollak; Hadassah Mount Scopus Hospital: F Benarroch; North Shore-Long Island Jewish Medical Center: C Budman (Site PI), R Bruun.

Central Valley Costa Rica (CVCR) Samples: UCSF: CA Mathews (Site PI), VI Reus, TL Lowe, M Rangel-Lugo; N Weiss; Hospital Nacional de Niños: LD Herrera (Site PI), R Romero, E Fournier; UCLA: NB Freimer (Site PI).

Antioquia Colombian Samples: University of College London: A Ruiz-Linares (Site PI), B Kremeyer, DD Campbell, H Muller; Universidad de Antioquia: G Bedoya Berrío, J Cardona Silgado, W Cornejo Ochoa, S Mesa Restrepo, A Valencia Duarte.

Control Sample Collection: University Medical Center, Utrecht: RA Ophoff, E Strengman; University of Bonn: M Wagner, R Moessner.

eQTL and mQTL data: C Liu; JR Gibbs and A Singleton for the North American Brain Expression Consortium ; J Hardy for the UK Human Brain Expression Database.

North American Brain Expression Consortium: S Arepalli1, MR Cookson1, A Dillman1, L Ferrucci2, JR Gibbs1,3, DG Hernandez1,3, R Johnson4, DL Longo5, Michael A Nalls1, Richard O'Brien6, Andrew Singleton1, Bryan Traynor1, Juan Troncoso6, Marcel van der Brug1,7, HR Zielke4, A Zonderman8; UK Human Brain Expression Database: JA Hardy3, M Ryten3, C Smith9, D Trabzuni3, R Walker9 and Mike Weale10

1Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA; 2Clinical Research Branch, National Institute on Aging, Baltimore, MD, USA; 3Department of Molecular Neuroscience, UCL Institute of Neurology, London, UK; 4NICHD Brain and Tissue Bank for Developmental Disorders, University of Maryland Medical School, Baltimore, MD, USA; 5Lymphocyte Cell Biology Unit, Laboratory of Immunology, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA; 6Brain Resource Center, Johns Hopkins University, Baltimore, MD, USA; 7ITGR Biomarker Discovery Group, Genentech, South San Francisco, CA, USA; 8Research Resources Branch, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA; 9Department of Pathology, The University of Edinburgh, Edinburgh, UK and 10King's College London, Department of Medical & Molecular Genetics, UK.

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Competing interests

Drs Pauls, Scharf, Mathews, Cox, Freimer, McMahon, Heutink, Oostra, Grados, King, Rouleau, Sandor and Budman have all received research support from the NIH and the Tourette Syndrome Association (TSA) on behalf of the TSA International Consortium for Genetics (TSAICG). Drs Scharf, Mathews and Grados have received honoraria and travel support from the TSA. Dr Mathews is a member of the TSA Medical Advisory Board. Dr Sandor has received support and consulting fees from Psyadon, Shire, Solway, UCB Pharma, Janssen, Eli Lilly, Pfizer and Prestwick. Dr Budman has been funded by Psyadon Pharmaceuticals, Otsuka Pharmaceuticals and NINDS and is a member of the National TSA Medical Advisory Board, LI TSA and LI CHADD Medical Advisory Boards. Dr Hoekstra has received honoraria for advice through Desitin, Eli Lilly and Shire. Dr Dion has received honoraria from Biovail Pharma, Pfizer and Eli Lilly. Dr Leckman has been funded by the NIH, the TSA, Talecris Biotherapeutics, Klingenstein Third Generation Foundation, John Wiley and Sons, McGraw Hill and Oxford University Press. Dr Walkup receives research support, travel support for paid and unpaid activities, serves in an unpaid position on the Medical Advisory Board and receives an honorarium for an Educational Meeting from the TSA. He receives royalties from Guilford Press and Oxford Press. He received free medication and placebo from Lilly, Pfizer and Abbott for NIH-funded studies. Dr Jankovic has received research grants from the following: Allergan, Allon Therapeutics, Ceregene, Chelsea Therapeutics, Diana Helis Henry Medical Research Foundation, EMD Serono, Huntington's Disease Society of America, Huntington Study Group, Impax Pharmaceuticals, Ipsen Limited, Lundbeck, Medtronic, Merz Pharmaceuticals, Michael J Fox Foundation for Parkinson Research, National Institutes of Health, National Parkinson Foundation, Neurogen, St Jude Medical, Teva Pharmaceutical Industries, University of Rochester and Parkinson Study Group. He has served as a consultant or advisory committee member for Allergan, Chelsea Therapeutics, EMD Serono, Lundbeck, Merz Pharmaceuticals, Michael J Fox Foundation for Parkinson Research and Teva Pharmaceutical Industries. He also serves on the editorial boards for Elsevier, Medlink: Neurology, Neurology in Clinical Practice, Neurotoxin Institute, Scientiae and UpToDate. Dr Knowles is on the Scientific Advisory Committee for Next-Generation Sequencing of Life Technologies, and is a technical advisor to SoftGenetics. Ms Anderson, Dr Barr, Dr Benarroch, Mr Berrío, Dr Bruun, Mr Campbell, Dr Cath, Dr Chouinard, Dr Conti, Ms Crane, Mr Crenshaw, Ms Davarya, Dr Davis, Ms Duarte, Mr Edlund, Dr Erenberg, Dr Eskin, Dr Evans, Mr Fagerness, Dr Fernandez, Mr Fournier, Mr Gamazon, Mr Gibbs, Dr Gilbert, Dr Girard, Dr Gross-Tsur, Dr Han, Dr Hardy, Dr Heiman, Dr Herrera, Dr Heutink, Dr Illmann, Dr J Kidd, Dr K Kidd, Mr. Konkashbaev, Dr Kremeyer, Dr Kurlan, Dr Lee, Dr Leppert, Dr Liu, Dr Lowe, Dr Lyon, Dr Mirel, Dr Moessner, Ms Moorjani, Mr Morgan, Mr Muller, Dr Naarden, Dr Neale, Dr Ochoa, Dr Ophoff, Ms Osiecki, Dr Pakstis, Ms Parkin, Mr Phan, Dr Pluzhnikov, Dr Pollak, Dr Posthuma, Dr Purcell, Dr Rangel-Lugo, Dr Restrepo, Dr Reus, Ms Rivas, Dr Robertson, Ms Romero, Dr Ruiz-Linares, Dr Sabatti, Ms Service, Mr Silgado, Dr Singer, Dr Singleton, Dr Smit, Dr State, Dr Stewart, Mr. Strengman, Dr Tikhomirov, Dr Tischfield, Dr Wagner, Dr N Weiss, Dr R Weiss and Ms Yu declare no conflict of interest.

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Scharf, J., Yu, D., Mathews, C. et al. Genome-wide association study of Tourette's syndrome. Mol Psychiatry 18, 721–728 (2013). https://doi.org/10.1038/mp.2012.69

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Keywords

  • genetics
  • GWAS
  • neurodevelopmental disorder
  • tics
  • Tourette's syndrome

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