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Genomewide association study for susceptibility genes contributing to familial Parkinson disease

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Abstract

Five genes have been identified that contribute to Mendelian forms of Parkinson disease (PD); however, mutations have been found in fewer than 5% of patients, suggesting that additional genes contribute to disease risk. Unlike previous studies that focused primarily on sporadic PD, we have performed the first genomewide association study (GWAS) in familial PD. Genotyping was performed with the Illumina HumanCNV370Duo array in 857 familial PD cases and 867 controls. A logistic model was employed to test for association under additive and recessive modes of inheritance after adjusting for gender and age. No result met genomewide significance based on a conservative Bonferroni correction. The strongest association result was with SNPs in the GAK/DGKQ region on chromosome 4 (additive model: p = 3.4 × 10−6; OR = 1.69). Consistent evidence of association was also observed to the chromosomal regions containing SNCA (additive model: p = 5.5 × 10−5; OR = 1.35) and MAPT (recessive model: p = 2.0 × 10−5; OR = 0.56). Both of these genes have been implicated previously in PD susceptibility; however, neither was identified in previous GWAS studies of PD. Meta-analysis was performed using data from a previous case–control GWAS, and yielded improved p values for several regions, including GAK/DGKQ (additive model: p = 2.5 × 10−7) and the MAPT region (recessive model: p = 9.8 × 10−6; additive model: p = 4.8 × 10−5). These data suggest the identification of new susceptibility alleles for PD in the GAK/DGKQ region, and also provide further support for the role of SNCA and MAPT in PD susceptibility.

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Acknowledgments

This project was supported by R01 NS37167, R01 NS036711, the Robert P. & Judith N. Goldberg Foundation, the Bumpus Foundation and the Harvard NeuroDiscovery Center. This study used samples from the NINDS Human Genetics Resource Center DNA and Cell Line Repository (http://ccr.coriell.org/ninds), as well as clinical data. DNA samples contributed by the Parkinson Institute—Istituti Clinici di Perfezionamento, Milan, Italy were from the “Human genetic bank of patients affected by PD and parkinsonisms”, supported by Italian Telethon grant n. GTB07001 and by the “Fondazione Grigioni per il Morbo di Parkinson”. Genotyping services were provided by the Center for Inherited Disease Research (CIDR). CIDR is fully funded through a federal contract from the National Institutes of Health to The Johns Hopkins University, contract number HHSN268200782096C. We particularly thank Justin Paschall from the NCBI dbGaP staff for his assistance in developing the dataset available at dbGaP. The data generated from this case–control study are available at http://www.ncbi.nlm.nih.gov/sites/entrez?db=gap through dbGaP accession number: phs000126.v1.p1. Data from the Fung et al. study were obtained from dbGaP. Funding support for “NINDS-Genome-Wide Genotyping in Parkinson’s Disease: First Stage Analysis and Public Release of Data” was provided by intramural programs of the National Institute on Aging and the National Institute on Neurological Disorders and Stroke (NINDS) and the genotyping of samples was provided by NINDS. The dataset used for the meta-analyses described in this manuscript were obtained from the NINDS Database found at http://www.ncbi.nlm.nih.gov/sites/entrez?db=gap through dbGaP accession number phs000089.v1.p1. The following are members of the PROGENI Steering Committee. University of Tennessee Health Science Center: R. F. Pfeiffer; University of Rochester: F. Marshall, D. Oakes, A. Rudolph, A. Shinaman; Columbia University Medical Center: K. Marder; Indiana University School of Medicine: P. M. Conneally, T. Foroud, C. Halter; University of Kansas Medical Center: K. Lyons; Eli Lilly & Company: E. Siemers; Medical College of Ohio: L. Elmers; University of California, Irvine: N. Hermanowicz. The following are members of the GenePD Steering Committee. University of Virginia Health System: G. F. Wooten; UMDNJ-Robert Wood Johnson Medical School: L. Golbe; Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School: J. F. Gusella; Boston University School of Medicine: R. H. Myers. We thank the subjects for their participation in this research study.

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Authors and Affiliations

  1. Indiana University School of Medicine, Health Information and Translational Sciences Building—HS 4000, 410 West 10th Street, Indianapolis, IN, 46202-3002, USA

    Nathan Pankratz, Cheryl Halter & Tatiana Foroud

  2. Department of Neurology, Boston University School of Medicine, 715 Albany Street, E-304, Boston, MA, 02118-2526, USA

    Jemma B. Wilk, Jeanne C. Latourelle, Anita L. DeStefano & Richard H. Myers

  3. Boston University School of Public Health, Boston, MA, 02118, USA

    Anita L. DeStefano

  4. Johns Hopkins University School of Medicine, Baltimore, MD, 21224, USA

    Elizabeth W. Pugh & Kimberly F. Doheny

  5. Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114, USA

    James F. Gusella

  6. Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, 45229, USA

    William C. Nichols

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  1. Nathan Pankratz
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  2. Jemma B. Wilk
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  3. Jeanne C. Latourelle
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  4. Anita L. DeStefano
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  5. Cheryl Halter
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  6. Elizabeth W. Pugh
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  7. Kimberly F. Doheny
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  8. James F. Gusella
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  9. William C. Nichols
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  10. Tatiana Foroud
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  11. Richard H. Myers
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Consortia

The PSG—PROGENI and GenePD Investigators, Coordinators and Molecular Genetic Laboratories

Corresponding authors

Correspondence to Tatiana Foroud or Richard H. Myers.

Additional information

N. Pankratz and J. B. Wilk are joint first authors.

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Appendices

PSG-PROGENI Investigators and Coordinators

Albany Medical College: S. Factor, D. Higgins, S. Evans; Barrow Neurological Institute: H. Shill, M. Stacy, J. Danielson, L. Marlor, K. Williamson; Baylor College of Medicine: J. Jankovic, C. Hunter; Beth Israel Deaconess Medical Center: D. Simon, P. Ryan, L. Scollins; Beth Israel Medical Center: R. Saunders-Pullman, K. Boyar, C. Costan-Toth, E. Ohmann; Brigham & Women’s Hospital: L. Sudarsky, C. Joubert; Brown University (Memorial Hospital of RI): J. Friedman, K. Chou, H. Fernandez, M. Lannon; Cleveland Clinic Florida-Weston: N. Galvez-Jimenez, A. Podichetty, K. Thompson; Clinical Neuroscience Center: P. Lewitt, M. DeAngelis; Colorado Neurological Institute: C. O’Brien, L. Seeberger, C. Dingmann, D. Judd; Columbia University Medical Center: K. Marder, J. Fraser, J. Harris; Creighton University: J. Bertoni, C. Peterson; Evanston Northwestern Healthcare: M. Rezak, G. Medalle; Hotel-Dieu Hospital-Chum: S. Chouinard, M. Panisset, J. Hall, H. Poiffaut; Hunter Homes McGuire Veterans Medical Center: V. Calabrese, P. Roberge; Indiana University School of Medicine: J. Wojcieszek, J. Belden; Institute For Neurodegenerative Disorders: D. Jennings, K. Marek, S. Mendick; Johns Hopkins University: S. Reich, B. Dunlop; London Health Sciences Centre: M. Jog, C. Horn; Mayo Clinic Jacksonville: R. Uitti, M. Turk; McFarland Neurosciences: T. Ajax, J. Mannetter; Medical College of Georgia: K. Sethi, J. Carpenter, B. Dill, L. Hatch, K. Ligon, S. Narayan; Medical College of Wisconsin: K. Blindauer, K. Abou-Samra, J. Petit; Medical University of Ohio: L. Elmer, E. Aiken, K. Davis, C. Schell, S. Wilson; Mount Sinai School of Medicine: M. Velickovic, W. Koller (deceased), S. Phipps; North Shore-LIJ Health System: A. Feigin, M. Gordon, J. Hamann, E. Licari, M. Marotta-Kollarus, B. Shannon, R. Winnick; Northwestern University: T. Simuni, A. Videnovic, A. Kaczmarek, K. Williams, M. Wolff; Ochsner Clinic Foundation: J. Rao, M. Cook; Ohio State University: M. Fernandez, S. Kostyk, J. Hubble, A. Campbell, C. Reider, A. Seward; Oregon Health & Science University: R. Camicioli, J. Carter, J. Nutt, P. Andrews, S. Morehouse, C. Stone; Ottawa Hospital Civic Site: T. Mendis, D. Grimes, C. Alcorn-Costa, P. Gray, K. Haas, J. Vendette; Pacific Neuroscience Medical Group: J. Sutton, B. Hutchinson, J. Young; Saskatoon Dist Health Board Royal Univ Hosp: A. Rajput, A. Rajput, L. Klassen, T. Shirley; Scott & White Hospital/Texas A&M University: B. Manyam, P. Simpson, J. Whetteckey, B. Wulbrecht; The Parkinson’s & Movement Disorder Institute: D. Truong, M. Pathak, K. Frei, N. Luong, T. Tra, A. Tran, J. Vo; Toronto Western Hospital, University Health: A. Lang, G. Kleiner-Fisman, A. Nieves, L. Johnston, J. So; UMDNJ-School of Osteopathic Medicine: G. Podskalny, L. Giffin; University of Alabama at Birmingham: P. Atchison, C. Allen; University of Alberta: W. Martin, M. Wieler; University of Calgary: O. Suchowersky, M. Klimek; University of California Irvine: N. Hermanowicz, S. Niswonger; University of California San Diego: C. Shults (deceased), D. Fontaine; University of California San Francisco: M. Aminoff, C. Christine, M. Diminno, J. Hevezi; University of Chicago: A. Dalvi, U. Kang, J. Richman, S. Uy, J. Young; University of Cincinnati: A. Dalvi, A. Sahay, M. Gartner, D. Schwieterman; University of Colorado Health Sciences Center: D. Hall, M. Leehey, S. Culver, T. Derian; University of Connecticut: T. Demarcaida, S. Thurlow; University of Iowa: R. Rodnitzky, J. Dobson; University of Kansas Medical Center: K. Lyons, R. Pahwa, T. Gales, S. Thomas; University of Maryland School of Medicine: L. Shulman, S. Reich, W. Weiner, K. Dustin; University of Miami: K. Lyons, C. Singer, W. Koller (deceased), W. Weiner, L. Zelaya; University of Minnesota: P. Tuite, V. Hagen, S. Rolandelli, R. Schacherer, J. Kosowicz; University of New Mexico: P. Gordon, J. Werner; University of Puerto Rico School of Medicine: C. Serrano, S. Roque; University of Rochester: R. Kurlan, D. Berry, I. Gardiner; University of South Florida: R. Hauser, J. Sanchez-Ramos, T. Zesiewicz, H. Delgado, K. Price, P. Rodriguez, S. Wolfrath; University of Tennessee Health Science Center: R. Pfeiffer, L. Davis, B. Pfeiffer; University of Texas Southwestern Medical Center: R. Dewey, B. Hayward, A. Johnson, M. Meacham, B. Estes; Wake Forest University School of Medicine: F. Walker, V. Hunt, C. O’Neill; Washington University: B. Racette, L. Good, M. Rundle.

PROGENI Molecular Genetic Laboratory

Division of Human Genetics, Cincinnati Children’s Hospital Medical Center: William C. Nichols, Michael W. Pauciulo, Diane K. Marek, Veronika E. Elsaesser.

GenePD Investigators and Coordinators

University Southern California School of Medicine: M. Lew; University of Calgary: O. Suchowersky; University of Lübeck, Germany: C. Klein; UMDNJ-Robert Wood Johnson Medical School: L. Golbe, M. H. Mark; Massachusetts General Hospital, Harvard Medical School: J. Growdon, N. Huggins; University of Virginia Health System: G. F. Wooten; University of Alabama at Birmingham : R. Watts; University of Toronto: M. Guttman; Washington University School of Medicine: B. Racette, J. Perlmutter; Barrow Neurological Institute: L. Marlor, Sun Health Research Institute: H. Shill; University of Miami: C. Singer; Parkinson Institute, Istituti Clinici di Perfezionamento, Milano, Italy: S. Goldwurm, G. Pezzoli; Boston University School of Medicine: M. H. Saint-Hilaire, T. Massood; Cleveland Clinic Foundation: K. Baker, I. Itin; University of Louisville School of Medicine: I. Litvan; University of Sydney ANZAC Research Institute, Concord Hospital, Sydney, Australia: G. Nicholson, A. Corbett; Struthers Parkinson’s Center, Minneapolis: M. Nance; Port City Neurology, Scarborough, ME: E. Drasby; Parkinson’s Disease and Movement Disorder Center of Boca Raton: S. Isaacson; Newcastle University, Newcastle upon Tyne, UK: D. Burn, P. Chinnery; General Regional Hospital Bolzano, Bolzano, Italy: P. Pramstaller; University of Arkansas for Medical Sciences: J. Al-hinti; Aarhus University Hospital, Aarhus, Denmark: A. Moller, K. Ostergaard; University of Arizona: S. Sherman; Auckland City Hospital, Auckland, New Zealand: R. Roxburgh, B. Snow; University of Kentucky College of Medicine: J. Slevin, F. Cambi.

GenePD Molecular Genetics Laboratories

Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School: J. F. Gusella, M. E. McDonald, M. Sun, L. Mysore, M. A. Anderson, D. Lucente; Neurogenetics Laboratory, Boston University School of Medicine: S. Williamson, M. W. Nagle, R. H. Myers.

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Pankratz, N., Wilk, J.B., Latourelle, J.C. et al. Genomewide association study for susceptibility genes contributing to familial Parkinson disease. Hum Genet 124, 593–605 (2009). https://doi.org/10.1007/s00439-008-0582-9

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  • DOI: https://doi.org/10.1007/s00439-008-0582-9

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