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Gene expression imputation across multiple brain regions provides insights into schizophrenia risk

Nature Genetics volume 51, pages 659–674 (2019)Cite this article

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A Publisher Correction to this article was published on 13 May 2019

This article has been updated

Abstract

Transcriptomic imputation approaches combine eQTL reference panels with large-scale genotype data in order to test associations between disease and gene expression. These genic associations could elucidate signals in complex genome-wide association study (GWAS) loci and may disentangle the role of different tissues in disease development. We used the largest eQTL reference panel for the dorso-lateral prefrontal cortex (DLPFC) to create a set of gene expression predictors and demonstrate their utility. We applied DLPFC and 12 GTEx-brain predictors to 40,299 schizophrenia cases and 65,264 matched controls for a large transcriptomic imputation study of schizophrenia. We identified 413 genic associations across 13 brain regions. Stepwise conditioning identified 67 non-MHC genes, of which 14 did not fall within previous GWAS loci. We identified 36 significantly enriched pathways, including hexosaminidase-A deficiency, and multiple porphyric disorder pathways. We investigated developmental expression patterns among the 67 non-MHC genes and identified specific groups of pre- and postnatal expression.

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Fig. 1: Replication of DLPFC prediction models in independent data.
Fig. 2: SCZ association results.
Fig. 3: SCZ-associated genes are coexpressed throughout development and across brain regions.
Fig. 4: Gene expression patterns for SCZ-associated genes cluster into four groups, relating to distinct spatiotemporal expression.

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Data availability

Our CMC-derived DLPFC prediction models are publicly available at https://github.com/laurahuckins/CMC_DLPFC_prediXcan.

Change history

  • 13 May 2019

    In the HTML version of the article originally published, the author group ‘The Schizophrenia Working Group of the Psychiatric Genomics Consortium’ was displayed incorrectly. The error has been corrected in the HTML version of the article.

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Acknowledgements

We dedicate this manuscript to the memory of Pamela Sklar, whose guidance and wisdom we miss daily. We strive to continue her legacy of thoughtful, innovative, and collaborative science. Data were generated as part of the CommonMind Consortium supported by funding from Takeda Pharmaceuticals Company Limited, F. Hoffman-La Roche Ltd and NIH grants R01MH085542, R01MH093725, P50MH066392, P50MH080405, R01MH097276, RO1-MH-075916, P50M096891, P50MH084053S1, R37MH057881 and R37MH057881S1, HHSN271201300031C, AG02219, AG05138 and MH06692.

Brain tissue for the study was obtained from the following brain bank collections: the Mount Sinai NIH Brain and Tissue Repository, the University of Pennsylvania Alzheimer’s Disease Core Center, the University of Pittsburgh NeuroBioBank and Brain and Tissue Repositories and the NIMH Human Brain Collection Core. CMC Leadership: P. Sklar, J. Buxbaum (Icahn School of Medicine at Mount Sinai), B. Devlin, D. Lewis (University of Pittsburgh), R. Gur, C.-G. Hahn (University of Pennsylvania), K. Hirai, H. Toyoshiba (Takeda Pharmaceuticals Company Limited), E. Domenici, L. Essioux (F. Hoffman-La Roche Ltd), L. Mangravite, M. Peters (Sage Bionetworks), T. Lehner, B. Lipska (NIMH).

ROSMAP study data were provided by the Rush Alzheimer’s Disease Center, Rush University Medical Center, Chicago. Data collection was supported through funding by NIA grants P30AG10161, R01AG15819, R01AG17917, R01AG30146, R01AG36836, U01AG32984, U01AG46152, the Illinois Department of Public Health, and the Translational Genomics Research Institute.

The iPSYCH-GEMS team acknowledges funding from the Lundbeck Foundation (grant no. R102-A9118 and R155-2014-1724), the Stanley Medical Research Institute, an Advanced Grant from the European Research Council (project no. 294838), the Danish Strategic Research Council the Novo Nordisk Foundation for supporting the Danish National Biobank resource, and grants from Aarhus and Copenhagen Universities and University Hospitals, including support to the iSEQ Center, the GenomeDK HPC facility, and the CIRRAU Center.

The Genotype-Tissue Expression (GTEx) Project was supported by the Common Fund of the Office of the Director of the National Institutes of Health, and by NCI, NHGRI, NHLBI, NIDA, NIMH, and NINDS. The data used for the analyses described in this manuscript were obtained from the GTEx Portal on September 5, 2016. BrainSpan: Atlas of the Developing Human Brain (Internet). Funded by ARRA Awards 1RC2MH089921-01, 1RC2MH090047-01, and 1RC2MH089929-01.

H.K.I. was supported by R01 MH107666-01.

Author information

Authors and Affiliations

  1. Pamela Sklar Division of Psychiatric Genomics, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Laura M. Huckins, Amanda Dobbyn, Gabriel Hoffman, Weiqing Wang, Hoang T. Nguyen, Kiran Girdhar, Panos Roussos, Menachem Fromer, Shaun Purcell, Jessica S. Johnson, Vahram Haroutunian, Menachem Fromer, Shaun M. Purcell, Panos Roussos, Douglas M. Ruderfer, Eli A. Stahl, Pamela Sklar, Pamela Sklar & Eli A. Stahl

  2. Department of Genetics and Genomics, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Laura M. Huckins, Amanda Dobbyn, Weiqing Wang, Hoang T. Nguyen, Kiran Girdhar, Panos Roussos, Menachem Fromer, Shaun Purcell, Hardik R. Shah, Milind C. Mahajan, Eric Schadt, Guiqing Cai, Eli A. Stahl, Joseph D. Buxbaum, Pamela Sklar, Pamela Sklar & Eli A. Stahl

  3. Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Laura M. Huckins, Panos Roussos, Guiqing Cai, Kenneth L. Davis, Elodie Drapeau, Joseph I. Friedman, Vahram Haroutunian, Elena Parkhomenko, Abraham Reichenberg, Jeremy M. Silverman, Eli A. Stahl, Joseph D. Buxbaum, Pamela Sklar, Pamela Sklar & Eli A. Stahl

  4. Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Laura M. Huckins, Gabriel Hoffman, Panos Roussos, Shaun Purcell, Hardik R. Shah, Milind C. Mahajan, Eric Schadt, Panos Roussos, Eli A. Stahl, Pamela Sklar, Pamela Sklar & Eli A. Stahl

  5. Vanderbilt University Medical Center, Nashville, TN, USA

    Douglas M. Ruderfer, Eric R. Gamazon, Douglas M. Ruderfer & Nancy J. Cox

  6. MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University, Cardiff, UK

    Antonio F. Pardiñas, James T. R. Walters, Peter A. Holmans, Noa Carrera, Nick Craddock, Valentina Escott-Price, Lyudmila Georgieva, Marian L. Hamshere, David Kavanagh, Sophie E. Legge, Andrew J. Pocklington, Alexander L. Richards, Douglas M. Ruderfer, Nigel M. Williams, George Kirov, Michael J. Owen, Michael C. O’Donovan, James T. R. Walters, Michael C. O’Donovan & Michael J. Owen

  7. Department of Biomedicine, Aarhus University, Aarhus, Denmark

    Veera M. Rajagopal, Thomas D. Als, Ditte Demontis, Manuel Mattheisen, Anders D. Børglum, Anders D. Børglum, Ditte Demontis, Veera Manikandan Rajagopal, Thomas D. Als, Manuel Mattheisen, Jakob Grove, Preben Bo Mortensen, Ditte Demontis & Anders D. Børglum

  8. The Lundbeck Foundation Initiative for Integrative Psychiatric Research, iPSYCH, Denmark

    Veera M. Rajagopal, Thomas D. Als, Esben Agerbo, Ditte Demontis, Thomas Hansen, Manuel Mattheisen, Ole Mors, Line Olsen, Anders D. Børglum, Preben B. Mortensen, Thomas Werge, Anders D. Børglum, Ditte Demontis, Veera Manikandan Rajagopal, Thomas D. Als, Manuel Mattheisen, Jakob Grove, Thomas Werge, Preben Bo Mortensen, Carsten Bøcker Pedersen, Esben Agerbo, Marianne Giørtz Pedersen, Ole Mors, Merete Nordentoft, David M. Hougaard, Jonas Bybjerg-Grauholm, Marie Bækvad-Hansen, Christine Søholm Hansen, Ditte Demontis & Anders D. Børglum

  9. Center for Integrative Sequencing, Aarhus University, Aarhus, Denmark

    Veera M. Rajagopal, Thomas D. Als, Ditte Demontis, Manuel Mattheisen, Ole Mors, Anders D. Børglum, Anders D. Børglum, Ditte Demontis, Veera Manikandan Rajagopal, Thomas D. Als, Manuel Mattheisen, Jakob Grove, Ditte Demontis & Anders D. Børglum

  10. Department of Human Genetics, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA

    James Boocock, Rita M. Cantor & Roel A. Ophoff

  11. Human Brain Collection Core, National Institute of Mental Health, Bethesda, MD, USA

    Robin Kramer & Barbara K. Lipska

  12. Laboratory of Neurogenomic Biomarkers, Centre for Integrative Biology (CIBIO), University of Trento, Trento, Italy

    Enrico Domenici

  13. Clare Hall, University of Cambridge, Cambridge, UK

    Eric R. Gamazon

  14. University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Wei Cheng & Patrick Sullivan

  15. Karolinska Institutet, Stockholm, Sweden

    Patrick Sullivan

  16. Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA

    Lambertus L. Klein, David A. Lewis & Bernie Devlin

  17. Systems Biology, Sage Bionetworks, Seattle, WA, USA

    Kristen K. Dang, Benjamin A. Logsdon, Lara M. Mangravite, Vahram Haroutunian, Mette A. Peters, Thanneer M. Perumal & Solveig K. Sieberts

  18. Section of Genetic Medicine, Department of Medicine, University of Chicago, Chicago, IL, USA

    Hae Kyung Im

  19. Integrated Technology Research Laboratories, Pharmaceutical Research Division, Takeda Pharmaceutical Company Limited, Fujisawa, Japan

    Hiroyoshi Toyoshiba

  20. Neuropsychiatry Section, Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Raquel E. Gur

  21. Neuropsychiatric Signaling Program, Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Chang-Gyu Hahn

  22. Psychiatry, JJ Peters Virginia Medical Center, Bronx, NY, USA

    Vahram Haroutunian & Vahram Haroutunian

  23. Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, New York, NY, USA

    Vahram Haroutunian & Joseph D. Buxbaum

  24. Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Joseph D. Buxbaum, Vahram Haroutunian, Joseph D. Buxbaum & Pamela Sklar

  25. Seaver Autism Center for Research and Treatment, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Joseph D. Buxbaum

  26. CNS Drug Discovery Unit, Pharmaceutical Research Division, Takeda Pharmaceutical Company Limited, Fujisawa, Japan

    Keisuke Hirai

  27. F. Hoffman-La Roche Ltd, Basel, Switzerland

    Laurent Essioux

  28. Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark

    Jakob Grove

  29. Institute of Biological Psychiatry, MHC Sct. Hans, Mental Health Services Copenhagen, Roskilde, Denmark

    Thomas Hansen, Henrik B. Rasmussen, Thomas Werge & Thomas Werge

  30. Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

    Thomas Werge

  31. National Centre for Register-Based Research, Aarhus University, Aarhus, Denmark

    Esben Agerbo, Preben B. Mortensen, Preben Bo Mortensen, Carsten Bøcker Pedersen, Esben Agerbo & Marianne Giørtz Pedersen

  32. Centre for Integrated Register-based Research, Aarhus University, Aarhus, Denmark

    Esben Agerbo, Preben B. Mortensen, Preben Bo Mortensen, Carsten Bøcker Pedersen, Esben Agerbo & Marianne Giørtz Pedersen

  33. Psychosis Research Unit, Aarhus University Hospital, Risskov, Denmark

    Ole Mors

  34. Mental Health Services in the Capital Region of Denmark, Mental Health Center Copenhagen, University of Copenhagen, Copenhagen, Denmark

    Merete Nordentoft

  35. Center for Neonatal Screening, Department for Congenital Disorders, Statens Serum Institut, Copenhagen, Denmark

    Mads V. Hollegaard, David M. Hougaard, David M. Hougaard, Jonas Bybjerg-Grauholm, Marie Bækvad-Hansen & Christine Søholm Hansen

  36. Analytic and Translational Genetics Unit, Massachusetts General Hospital, Boston, MA, USA

    Stephan Ripke, Benjamin M. Neale, Kai-How Farh, Phil Lee, Brendan Bulik-Sullivan, Hailiang Huang, Menachem Fromer, Jacqueline I. Goldstein & Mark J. Daly

  37. Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA

    Stephan Ripke, Benjamin M. Neale, Phil Lee, Brendan Bulik-Sullivan, Richard A. Belliveau Jr, Sarah E. Bergen, Elizabeth Bevilacqua, Kimberly D. Chambert, Menachem Fromer, Giulio Genovese, Colm O’Dushlaine, Edward M. Scolnick, Jordan W. Smoller, Steven A. McCarroll, Jennifer L. Moran, Aarno Palotie, Tracey L. Petryshen & Mark J. Daly

  38. Medical and Population Genetics Program, Broad Institute of MIT and Harvard, Cambridge, MA, USA

    Benjamin M. Neale, Hailiang Huang, Tune H. Pers, Jacqueline I. Goldstein, Joel N. Hirschhorn, Alkes Price, Tonu Esko & Mark J. Daly

  39. Psychiatric and Neurodevelopmental Genetics Unit, Massachusetts General Hospital, Boston, MA, USA

    Benjamin M. Neale, Phil Lee, Menachem Fromer, Jordan W. Smoller & Aarno Palotie

  40. Neuropsychiatric Genetics Research Group, Department of Psychiatry, Trinity College Dublin, Dublin, Ireland

    Aiden Corvin, Paul Cormican, Gary Donohoe, Derek W. Morris & Michael Gill

  41. NationalCentre for Mental Health, Cardiff University, Cardiff, UK

    Peter A. Holmans, Nick Craddock, Michael J. Owen & Michael C. O’Donovan

  42. Eli Lilly and Company Limited, Erl Wood Manor, Sunninghill Road, Windlesham, Surrey, UK

    David A. Collier, Younes Mokrab & Henrik B. Rasmussen

  43. Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, King’s College London, London, UK

    David A. Collier

  44. Center for BiologicalSequence Analysis, Department of Systems Biology, Technical University of Denmark, Kongens Lyngby, Denmark

    Tune H. Pers

  45. Division of Endocrinology and Center for Basic and Translational Obesity Research, Boston Children’s Hospital, Boston, MA, USA

    Tune H. Pers, Joel N. Hirschhorn & Tonu Esko

  46. Department of Clinical Neuroscience, Psychiatry Section, Karolinska Institutet, Stockholm, Sweden

    Ingrid Agartz, Erik Soderman & Erik G. Jonsson

  47. Department of Psychiatry, Diakonhjemmet Hospital, Oslo, Norway

    Ingrid Agartz

  48. NORMENT, KG Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway

    Ingrid Agartz, Srdjan Djurovic, Morten Mattingsdal, Ingrid Melle, Ole A. Andreassen & Erik G. Jonsson

  49. State Mental Hospital, Haar, Germany

    Margot Albus

  50. Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA

    Madeline Alexander, Claudine Laurent & Douglas F. Levinson

  51. Department of Psychiatry and Behavioral Sciences, Atlanta Veterans Affairs Medical Center, Atlanta, GA, USA

    Farooq Amin

  52. Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA, USA

    Farooq Amin

  53. Virginia Institute for Psychiatric and Behavioral Genetics, Department of Psychiatry, Virginia Commonwealth University, Richmond, VA, USA

    Silviu A. Bacanu, Tim B. Bigdeli, Bradley T. Webb & Brandon K. Wormley

  54. Clinical Neuroscience, Max Planck Institute of Experimental Medicine, Gottingen, Germany

    Martin Begemann, Christian Hammer, Sergi Papiol & Hannelore Ehrenreich

  55. Department of Medical Genetics, University of Pécs, Pécs, Hungary

    Judit Bene & Bela Melegh

  56. Szentagothai Research Center, University of Pécs, Pécs, Hungary

    Judit Bene & Bela Melegh

  57. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    Sarah E. Bergen, Anna K. Kahler, Patrik K. E. Magnusson, Christina M. Hultman & Patrick F. Sullivan

  58. Department of Psychiatry, University of Iowa Carver College of Medicine, Iowa City, IA, USA

    Donald W. Black

  59. University Medical Center Groningen, Department of Psychiatry, University of Groningen, Groningen, the Netherlands

    Richard Bruggeman

  60. School of Nursing, Louisiana State University Health Sciences Center, New Orleans, LA, USA

    Nancy G. Buccola

  61. Athinoula A. Martinos Center, Massachusetts General Hospital, Boston, MA, USA

    Randy L. Buckner & Joshua L. Roffman

  62. Center for Brain Science, Harvard University, Cambridge, MA, USA

    Randy L. Buckner

  63. Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA

    Randy L. Buckner, Line Olsen & Joshua L. Roffman

  64. Department of Psychiatry, University of California at San Francisco, San Francisco, CA, USA

    William Byerley

  65. University Medical Center Utrecht, Department of Psychiatry, Rudolf Magnus Institute of Neuroscience, Utrecht, the Netherlands

    Wiepke Cahn, Rene S. Kahn, Eric Strengman & Roel A. Ophoff

  66. Centre Hospitalier du Rouvray and INSERM U1079 Faculty of Medicine, Rouen, France

    Dominique Campion

  67. Schizophrenia Research Institute, Sydney, New South Wales, Australia

    Vaughan J. Carr, Stanley V. Catts, Frans A. Henskens, Carmel M. Loughland, Patricia T. Michie, Christos Pantelis, Ulrich Schall, Rodney J. Scott & Assen V. Jablensky

  68. School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia

    Vaughan J. Carr

  69. Royal Brisbane and Women’s Hospital, University of Queensland, Brisbane, Queensland, Australia

    Stanley V. Catts

  70. Institute of Psychology, Chinese Academy of Science, Beijing, China

    Raymond C. K. Chan

  71. Department of Psychiatry, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, China

    Ronald Y. L. Chen, Eric Y. H. Chen, Miaoxin Li, Hon-Cheong So, Emily H. M. Wong & Pak C. Sham

  72. State Key Laboratory for Brain and Cognitive Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, China

    Eric Y. H. Chen, Miaoxin Li & Pak C. Sham

  73. Castle Peak Hospital, Hong Kong, China

    Eric F. C. Cheung

  74. Institute of Mental Health, Singapore, Singapore

    Siow Ann Chong, Jimmy Lee Chee Keong, Kang Sim & Mythily Subramaniam

  75. Department of Psychiatry, Washington University, St. Louis, MO, USA

    C. Robert Cloninger & Dragan M. Svrakic

  76. Department of Child and Adolescent Psychiatry, Assistance Publique Hopitaux de Paris, Pierre and Marie Curie Faculty of Medicine and Institute for Intelligent Systems and Robotics, Paris, France

    David Cohen

  77. Blue Note Biosciences, Princeton, NJ, USA

    Nadine Cohen

  78. Department of Genetics, University of North Carolina, Chapel Hill, NC, USA

    James J. Crowley, Martilias S. Farrell, Paola Giusti-Rodríguez, Yunjung Kim, Jin P. Szatkiewicz, Stephanie Williams & Patrick F. Sullivan

  79. Department of Psychological Medicine, Queen Mary University of London, London, UK

    David Curtis

  80. Molecular Psychiatry Laboratory, Division of Psychiatry, University College London, London, UK

    David Curtis, Jonathan Pimm, Hugh Gurling & Andrew McQuillin

  81. Sheba Medical Center, Tel Hashomer, Israel

    Michael Davidson & Mark Weiser

  82. Department of Genomics, Life and Brain Center, Bonn, Germany

    Franziska Degenhardt, Stefan Herms, Per Hoffmann, Andrea Hofman, Sven Cichon & Markus M. Nothen

  83. Institute of Human Genetics, University of Bonn, Bonn, Germany

    Franziska Degenhardt, Stefan Herms, Per Hoffmann, Andrea Hofman, Sven Cichon & Markus M. Nothen

  84. AppliedMolecular Genomics Unit, VIB Department of Molecular Genetics, University of Antwerp, Antwerp, Belgium

    Jurgen Del Favero

  85. First Department of Psychiatry, University of Athens Medical School, Athens, Greece

    Dimitris Dikeos & George N. Papadimitriou

  86. Department of Psychiatry, University College Cork, Co, Cork, Ireland

    Timothy Dinan

  87. Department of Medical Genetics, Oslo University Hospital, Oslo, Norway

    Srdjan Djurovic

  88. Cognitive Genetics and Therapy Group, School of Psychology and Discipline of Biochemistry, National University of Ireland Galway, Co, Galway, Ireland

    Gary Donohoe & Derek W. Morris

  89. Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA

    Jubao Duan, Alan R. Sanders & Pablo V. Gejman

  90. Department of Psychiatry and Behavioral Sciences, North Shore University Health System, Evanston, IL, USA

    Jubao Duan, Alan R. Sanders & Pablo V. Gejman

  91. Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK

    Frank Dudbridge

  92. Department of Child and Adolescent Psychiatry, University Clinic of Psychiatry, Skopje, Republic of Macedonia

    Naser Durmishi

  93. Department of Psychiatry, University of Regensburg, Regensburg, Germany

    Peter Eichhammer

  94. Department of General Practice, Helsinki University Central Hospital, University of Helsinki, Helsinki, Finland

    Johan Eriksson

  95. Folkhälsan Research Center, Helsinki, Finland, Biomedicum Helsinki, Helsinki, Finland

    Johan Eriksson

  96. National Institute for Health and Welfare, Helsinki, Finland

    Johan Eriksson & Veikko Salomaa

  97. Translational Technologies and Bioinformatics, Pharma Research and Early Development, F. Hoffman-La Roche, Basel, Switzerland

    Laurent Essioux

  98. Department of Psychiatry, Georgetown University School of Medicine, Washington, DC, USA

    Ayman H. Fanous

  99. Department of Psychiatry, Keck School of Medicine of the University of Southern California, Los Angeles, CA, USA

    Ayman H. Fanous

  100. Department of Psychiatry, Virginia Commonwealth University School of Medicine, Richmond, VA, USA

    Ayman H. Fanous

  101. Mental Health Service Line, Washington VA Medical Center, Washington, DC, USA

    Ayman H. Fanous

  102. Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Heidelberg, Mannheim, Germany

    Josef Frank, Sandra Meier, Thomas G. Schulze, Jana Strohmaier, Stephanie H. Witt & Marcella Rietschel

  103. Department of Genetics, University of Groningen, University Medical Centre Groningen, Groningen, the Netherlands

    Lude Franke & Juha Karjalainen

  104. Department of Psychiatry, University of Colorado Denver, Aurora, CO, USA

    Robert Freedman & Roel A. Ophoff

  105. Center for Neurobehavioral Genetics, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA

    Nelson B. Freimer

  106. Department of Psychiatry, University of Halle, Halle, Germany

    Marion Friedl, Ina Giegling, Annette M. Hartmann, Bettina Konte & Dan Rujescu

  107. Department of Psychiatry, University of Munich, Munich, Germany

    Ina Giegling & Dan Rujescu

  108. Departments of Psychiatry and Human and Molecular Genetics, INSERM, Institut de Myologie, Hôpital de la Pitiè-Salpêtrière, Paris, France

    Stephanie Godard

  109. Mental Health Research Centre, Russian Academy of Medical Sciences, Moscow, Russia

    Vera Golimbet

  110. Neuroscience Therapeutic Area, Janssen Research and Development, Raritan, NJ, USA

    Srihari Gopal, Dai Wang & Qingqin S. Li

  111. Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia

    Jacob Gratten, S. Hong Lee, Naomi R. Wray, Peter M. Visscher & Bryan J. Mowry

  112. Academic Medical Centre University of Amsterdam, Department of Psychiatry, Amsterdam, the Netherlands

    Lieuwe de Haan & Carin J. Meijer

  113. Illumina, La Jolla, CA, USA

    Mark Hansen

  114. Priority Research Centre for Health Behaviour, University of Newcastle, Newcastle, New South Wales, Australia

    Frans A. Henskens

  115. School of Electrical Engineering and Computer Science, University of Newcastle, Newcastle, New South Wales, Australia

    Frans A. Henskens

  116. Division of Medical Genetics, Department of Biomedicine, University of Basel, Basel, Switzerland

    Stefan Herms, Per Hoffmann & Sven Cichon

  117. Department of Genetics, Harvard Medical School, Boston, MA, USA

    Joel N. Hirschhorn, Tonu Esko & Steven A. McCarroll

  118. Department of Psychiatry, Fujita Health University School of Medicine, Toyoake, Japan

    Masashi Ikeda & Nakao Iwata

  119. Regional Centre for Clinical Researchin Psychosis, Department of Psychiatry, Stavanger University Hospital, Stavanger, Norway

    Inge Joa

  120. Rheumatology Research Group, Vall d’Hebron Research Institute, Barcelona, Spain

    Antonio Julia & Sara Marsal

  121. Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia

    Luba Kalaydjieva

  122. The Perkins Institute for Medical Research, The University of Western Australia, Perth, Western Australia, Australia

    Luba Kalaydjieva & Assen V. Jablensky

  123. Department of Medical Genetics, Medical University, Sofia, Bulgaria

    Sena Karachanak-Yankova & Draga Toncheva

  124. Department of Psychology, University of Colorado Boulder, Boulder, CO, USA

    Matthew C. Keller & Jo Knight

  125. Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Ontario, Canada

    James L. Kennedy, Ann Olincy & Clement C. Zai

  126. Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada

    James L. Kennedy, Clement C. Zai & Jo Knight

  127. Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada

    James L. Kennedy & Jo Knight

  128. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, Russia

    Andrey Khrunin, Svetlana Limborska & Petr Slominsky

  129. Latvian Biomedical Research and Study Centre, Riga, Latvia

    Janis Klovins & Liene Nikitina-Zake

  130. Department of Psychiatry and Zilkha Neurogenetics Institute, Keck School of Medicine at University of Southern California, Los Angeles, CA, USA

    James A. Knowles, Michele T. Pato & Carlos N. Pato

  131. Faculty of Medicine, Vilnius University, Vilnius, Lithuania

    Vaidutis Kucinskas & Zita Ausrele Kucinskiene

  132. Department of Biology and Medical Genetics, 2nd Faculty of Medicine and University Hospital Motol, Prague, Czech Republic

    Hana Kuzelova-Ptackova & Milan Macek Jr

  133. Department of Child and Adolescent Psychiatry, Pierre and Marie Curie Faculty of Medicine, Paris, France

    Claudine Laurent

  134. Duke-NUS Graduate Medical School, Singapore, Singapore

    Jimmy Lee Chee Keong

  135. Department of Psychiatry, Hadassah-Hebrew University Medical Center, Jerusalem, Israel

    Bernard Lerer

  136. Centre for Genomic Sciences, The University of Hong Kong, Hong Kong, China

    Miaoxin Li & Pak C. Sham

  137. Mental Health Centre and Psychiatric Laboratory, West China Hospital, Sichuan University, Chengdu, Sichuan, China

    Tao Li & Qiang Wang

  138. Department of Biostatistics, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA

    Kung-Yee Liang

  139. Department of Psychiatry, Columbia University, New York, New York, NY, USA

    Jeffrey Lieberman & T. Scott Stroup

  140. Priority Centre for Translational Neuroscience and Mental Health, University of Newcastle, Newcastle, New South Wales, Australia

    Carmel M. Loughland & Ulrich Schall

  141. Department of Genetics and Pathology, International Hereditary Cancer Center, Pomeranian Medical University in Szczecin, Szczecin, Poland

    Jan Lubinski

  142. Department of Mental Health and Substance Abuse Services, National Institute for Health and Welfare, Helsinki, Finland

    Jouko Lonnqvist & Jaana Suvisaari

  143. Department of Mental Health, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA

    Brion S. Maher & Larry J. Seidman

  144. Department of Psychiatry, University of Bonn, Bonn, Germany

    Wolfgang Maier

  145. Centre National de la Recherche Scientifique, Laboratoire de Génétique Moléculaire de la Neurotransmission et des Processus Neurodénégératifs, Hôpital de la Pitiè-Salpêtrière, Paris, France

    Jacques Mallet

  146. Department of Genomics Mathematics, University of Bonn, Bonn, Germany

    Manuel Mattheisen

  147. Research Unit, Sørlandet Hospital, Kristiansand, Norway

    Morten Mattingsdal

  148. Department of Psychiatry, Harvard Medical School, Boston, MA, USA

    Robert W. McCarley, Raquelle I. Mesholam-Gately & Tracey L. Petryshen

  149. VA Boston Health Care System, Brockton, MA, USA

    Robert W. McCarley

  150. Department of Psychiatry, National University of Ireland Galway, Co, Galway, Ireland

    Colm McDonald

  151. Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK

    Andrew M. McIntosh

  152. Division of Psychiatry, University of Edinburgh, Edinburgh, UK

    Andrew M. McIntosh & Douglas H. R. Blackwood

  153. Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway

    Ingrid Melle & Ole A. Andreassen

  154. Massachusetts Mental Health Center Public Psychiatry Division of the Beth Israel Deaconess Medical Center, Boston, MA, USA

    Raquelle I. Mesholam-Gately & Larry J. Seidman

  155. Estonian Genome Center, University of Tartu, Tartu, Estonia

    Andres Metspalu, Lili Milani, Mari Nelis & Tonu Esko

  156. School of Psychology, University of Newcastle, Newcastle, New South Wales, Australia

    Patricia T. Michie

  157. First Psychiatric Clinic, Medical University, Sofia, Bulgaria

    Vihra Milanova

  158. Department P, Aarhus University Hospital, Risskov, Denmark

    Ole Mors & Anders D. Børglum

  159. Department of Psychiatry, Royal College of Surgeons in Ireland, Dublin, Ireland

    Kieran C. Murphy

  160. King’s College London, London, UK

    Robin M. Murray & John Powell

  161. Maastricht University Medical Centre, South Limburg Mental Health Research and TeachingNetwork, EURON, Maastricht, the Netherlands

    Inez Myin-Germeys & Jim Van Os

  162. Institute of Translational Medicine, University of Liverpool, Liverpool, UK

    Bertram Muller-Myhsok

  163. Max Planck Institute of Psychiatry, Munich, Germany

    Bertram Muller-Myhsok

  164. Munich Cluster for Systems Neurology (SyNergy), Munich, Germany

    Bertram Muller-Myhsok

  165. Department of Psychiatry and Psychotherapy, Jena University Hospital, Jena, Germany

    Igor Nenadic

  166. Department of Psychiatry, Queensland Brain Institute and Queensland Centre for Mental Health Research, University of Queensland, Brisbane, Queensland, Australia

    Deborah A. Nertney

  167. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Gerald Nestadt & Ann E. Pulver

  168. Department of Psychiatry, Trinity College Dublin, Dublin, Ireland

    Kristin K. Nicodemus

  169. Eli Lilly and Company, Lilly Corporate Center, Indianapolis, IN, USA

    Laura Nisenbaum

  170. Department of Clinical Sciences, Psychiatry, Umeå University, Umeå, Sweden

    Annelie Nordin & Rolf Adolfsson

  171. DETECT Early Intervention Service for Psychosis, Blackrock, Co, Dublin, Ireland

    Eadbhard O’Callaghan

  172. Centre for Public Health, Institute of Clinical Sciences, Queen’s University Belfast, Belfast, UK

    F. Anthony O’Neill

  173. Lawrence Berkeley National Laboratory, University of California at Berkeley, Berkeley, CA, USA

    Sang-Yun Oh

  174. Institute of Psychiatry, King’s College London, London, UK

    Jim Van Os

  175. Melbourne Neuropsychiatry Centre, University of Melbourne & Melbourne Health, Melbourne, Victoria, Australia

    Christos Pantelis

  176. Department of Psychiatry, University of Helsinki, Helsinki, Finland

    Tiina Paunio

  177. Public Health Genomics Unit, National Institute for Health and Welfare, Helsinki, Finland

    Tiina Paunio & Olli Pietiläinen

  178. Medical Faculty, University of Belgrade, Belgrade, Serbia

    Milica Pejovic-Milovancevic

  179. Department of Psychiatry, University of North Carolina, Chapel Hill, NC, USA

    Diana O. Perkins & Patrick F. Sullivan

  180. Institute for Molecular Medicine Finland, FIMM, University of Helsinki, Helsinki, Finland

    Olli Pietiläinen & Aarno Palotie

  181. Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA

    Alkes Price

  182. Department of Psychiatry, University of Oxford, Oxford, UK

    Digby Quested

  183. Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond, VA, USA

    Mark A. Reimers & Aaron R. Wolen

  184. Pharma Therapeutics Clinical Research, Pfizer Worldwide Research and Development, Cambridge, MA, USA

    Christian R. Schubert & Jens R. Wendland

  185. Department of Psychiatry and Psychotherapy, University of Gottingen, Göttingen, Germany

    Thomas G. Schulze

  186. Psychiatry and Psychotherapy Clinic, University of Erlangen, Erlangen, Germany

    Sibylle G. Schwab

  187. Hunter New England Health Service, Newcastle, New South Wales, Australia

    Rodney J. Scott

  188. School of Biomedical Sciences, University of Newcastle, Newcastle, New South Wales, Australia

    Rodney J. Scott

  189. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA

    Jianxin Shi

  190. University of Iceland, Landspitali, National University Hospital, Reykjavik, Iceland

    Engilbert Sigurdsson

  191. Department of Psychiatry and Drug Addiction, Tbilisi State Medical University (TSMU), Tbilisi, Georgia

    Teimuraz Silagadze

  192. Research and Development, Bronx Veterans Affairs Medical Center, New York, NY, USA

    Jeremy M. Silverman

  193. WellcomeTrust Centre for Human Genetics, Oxford, UK

    Chris C. A. Spencer

  194. deCODE Genetics, Reykjavik, Iceland

    Hreinn Stefansson, Stacy Steinberg & Kari Stefansson

  195. Department of Clinical Neurology, Medical University of Vienna, Wien, Austria

    Elisabeth Stogmann & Fritz Zimprich

  196. Lieber Institute for Brain Development, Baltimore, MD, USA

    Richard E. Straub & Daniel R. Weinberger

  197. Department of Medical Genetics, University Medical Centre Utrecht, Utrecht, the Netherlands

    Eric Strengman

  198. Berkshire Healthcare NHS Foundation Trust, Bracknell, UK

    Srinivas Thirumalai

  199. Section of Psychiatry, University of Verona, Verona, Italy

    Sarah Tosato

  200. Department of Psychiatry, University of Oulu, Oulu, Finland

    Juha Veijola

  201. University Hospital of Oulu, Oulu, Finland

    Juha Veijola

  202. Molecular and Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin, Ireland

    John Waddington

  203. Health Research Board, Dublin, Ireland

    Dermot Walsh

  204. School of Psychiatry and Clinical Neurosciences, The University of Western Australia, Perth, Western Australia, Australia

    Dieter B. Wildenauer & Assen V. Jablensky

  205. Computational Sciences CoE, Pfizer Worldwide Research and Development, Cambridge, MA, USA

    Hualin Simon Xi

  206. Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

    Xuebin Zheng & Jianjun Liu

  207. University College London, London, UK

    Elvira Bramon

  208. Institute of Neuroscience and Medicine (INM-1), Research Center Juelich, Juelich, Germany

    Sven Cichon

  209. Department of Genetics, The Hebrew University of Jerusalem, Jerusalem, Israel

    Ariel Darvasi

  210. NeuroscienceDiscovery and Translational Area, Pharma Research and Early Development, F. Hoffman-La Roche, Basel, Switzerland

    Enrico Domenici

  211. Centre for Clinical Research in Neuropsychiatry, School of Psychiatry and Clinical Neurosciences, The University of Western Australia, Medical Research Foundation Building, Perth, Western Australia, Australia

    Assen V. Jablensky

  212. Virginia Institute for Psychiatric and Behavioral Genetics, Departments of Psychiatry and Human and Molecular Genetics, Virginia Commonwealth University, Richmond, VA, USA

    Kenneth S. Kendler & Brien P. Riley

  213. The Feinstein Institute for Medical Research, Manhasset, NY, USA

    Todd Lencz & Anil K. Malhotra

  214. The Hofstra NS-LIJ School of Medicine, Hempstead, NY, USA

    Todd Lencz & Anil K. Malhotra

  215. The Zucker Hillside Hospital, Glen Oaks, NY, USA

    Todd Lencz & Anil K. Malhotra

  216. Saw Swee Hock School of Public Health, National University of Singapore, Singapore, Singapore

    Jianjun Liu

  217. Queensland Centre for Mental Health Research, University of Queensland, Brisbane, Queensland, Australia

    Bryan J. Mowry

  218. Center for HumanGenetic Research and Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA

    Tracey L. Petryshen

  219. Department of Child and Adolescent Psychiatry, Erasmus University Medical Centre, Rotterdam, the Netherlands

    Danielle Posthuma

  220. Department of Complex Trait Genetics, Neuroscience Campus Amsterdam, VU University Medical Center Amsterdam, Amsterdam, the Netherlands

    Danielle Posthuma

  221. Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, VU University, Amsterdam, the Netherlands

    Danielle Posthuma

  222. University of Aberdeen, Institute of Medical Sciences, Aberdeen, UK

    David St Clair

  223. Departments of Psychiatry, Neurology, Neuroscience and Institute of Genetic Medicine, Johns Hopkins School of Medicine, Baltimore, MD, USA

    Daniel R. Weinberger

  224. Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

    Thomas Werge

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  1. Laura M. Huckins
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Contributions

L.M.H. designed the study and specific subanalyses, ran analyses, and wrote the manuscript. A.D. designed and ran analyses and contributed to the writing group. D.M.R. contributed to study and analytical design, and writing. G.H. contributed to analytical design and writing. W.W., H.T.N., and J.B. designed and ran specific analyses. A.F.P., V.M.R., T.D.A., K.G., M.F. all ran specific analyses. S.K.S. designed the study and analyses and contributed to the writing group. P.R. and R.K. designed the study and contributed data. E.D. designed the study, contributed data, and contributed to the writing group. E.R.G. designed specific analyses, and contributed to the writing group. S.P. designed the study. All three consortia (CMC, PGC-SCZ, iPSYCH-GEMS) contributed data. D.D., A.D.B., J.T.R.W., M.C.O’D., M.J.O. contributed data, advised on analyses, and contributed to the writing group. P. Sullivan advised on analyses and contributed to the writing group. B.D. designed the study, contributed data, advised on analyses, and contributed to the writing group. N.J.C. and H.K.I. designed the study, advised on analyses, and contributed to the writing group. P. Sklar and E.A.S. designed the study and specific analyses, ran analyses, and contributed to the writing group.

Corresponding author

Correspondence to Laura M. Huckins.

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Competing interests

E.D. has received research support from Roche during 2016–2018. T.W. has acted as advisor and lecturer to H. Lundbeck A/S. All other authors declare no conflicts of interest.

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Supplementary information

Supplementary Information

Supplementary Note and Supplementary Figures 1–12

Reporting Summary

Supplementary Table 1

Forward stepwise conditional analysis results.

Supplementary Table 2

MAGMA based pathway association results.

Supplementary Table 3

Mutant mouse lines lacking expression of SCZ-associated genes

Supplementary Table 4

Gene set membership of SCZ-associated genes, according to BRAINSPAN clusters

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Huckins, L.M., Dobbyn, A., Ruderfer, D.M. et al. Gene expression imputation across multiple brain regions provides insights into schizophrenia risk. Nat Genet 51, 659–674 (2019). https://doi.org/10.1038/s41588-019-0364-4

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