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Expanding the Range of ZNF804A Variants Conferring Risk of Psychosis

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Expanding the Range of ZNF804A Variants Conferring Risk of Psychosis Molecular Psychiatry (2011) 16, 59–66 & 2011 Macmillan Publishers Limited All rights reserved 1359-4184/11 www.nature.com/mp ORIGINAL ARTICLE Expanding the range of ZNF804A variants conferring risk of psychosis S Steinberg1, O Mors2, AD Børglum2,3, O Gustafsson1,4, T Werge5, PB Mortensen6, OA Andreassen4, E Sigurdsson7,8, TE Thorgeirsson1,YBo¨ttcher1, P Olason1, RA Ophoff9,10, S Cichon11, IH Gudjonsdottir1, OPH Pietila¨inen12,13, M Nyegaard3, A Tuulio-Henriksson14, A Ingason1, T Hansen5, L Athanasiu4, J Suvisaari14, J Lonnqvist14, T Paunio15, A Hartmann16,GJu¨rgens17, M Nordentoft18, D Hougaard19, B Norgaard-Pedersen20, R Breuer21, H-J Mo¨ller22, I Giegling16, B Glenthøj23, HB Rasmussen5, M Mattheisen10, I Bitter24,JMRe´thelyi24, T Sigmundsson7,8, R Fossdal1, U Thorsteinsdottir1,8, M Ruggeri25, S Tosato25, E Strengman9, GROUP37, LA Kiemeney26, I Melle4, S Djurovic27, L Abramova28, V Kaleda28, M Walshe29, E Bramon29, E Vassos29,30,TLi29,31, G Fraser32, N Walker33, T Toulopoulou29, J Yoon34, NB Freimer10, RM Cantor10,34, R Murray29, A Kong1, V Golimbet28,EGJo¨nsson35, L Terenius35, I Agartz35, H Petursson7,8,MMNo¨then36, M Rietschel21, L Peltonen12,13, D Rujescu16, DA Collier30,31, H Stefansson1, D St Clair32 and K Stefansson1,8 1deCODE genetics, Reykjavik, Iceland; 2Centre for Psychiatric Research, Aarhus University Hospital, Risskov, Denmark; 3Department of Human Genetics, Aarhus University, Arhus C, Denmark; 4Department of Psychiatry, Ulleva˚l University Hospital and Institute of Psychiatry, University of Oslo, Oslo, Norway; 5Research Institute of Biological Psychiatry, Mental Health Centre Sct. Hans Copenhagen University Hospital, Roskilde, Denmark; 6National Centre for Register-based Research, Aarhus University, Aarhus, Denmark; 7Department of Psychiatry, National University Hospital, Reykjavik, Iceland; 8School of Medicine, University of Iceland, Reykjavik, Iceland; 9Department of Medical Genetics and Rudolf Magnus Institute of Neuroscience, University Medical Center, Utrecht, The Netherlands; 10UCLA Center for Neurobehavioral Genetics, Los Angeles, CA, USA; 11Department of Genomics, Life & Brain Center, University of Bonn, Bonn, Germany; 12Institute for Molecular Medicine Finland FIMM and Department of Medical Genetics, University of Helsinki, Helsinki, Finland; 13Wellcome Trust Sanger Institute, Cambridge, UK; 14Department of Mental Health and Alcohol Research, National Public Health Institute, Helsinki, Finland; 15Public Health Genomics Unit, National Institute for Health and Welfare THL, Helsinki, Finland; 16Division of Molecular and Clinical Neurobiology, Department of Psychiatry, Ludwig-Maximilians University, Munich, Germany; 17Department of Clinical Pharmacology, Bispebjerg University Hospital, Copenhagen NV, Denmark; 18Psychiatric Centre Bisbebjerg, Bispebjerg University Hospital, Copenhagen NV, Denmark; 19Section of Neonatal Screening and Hormones, Department Clinical Chemistry and Immunology, The State Serum Institute, Copenhagen S, Denmark; 20Department of Neurology, Glostrup Hospital, Copenhagen, Denmark; 21Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany; 22Department of Psychiatry, Ludwig- Maximilians-University, Munich, Germany; 23Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research, Copenhagen University Hospital, Psychiatric Center, Glostrup, Denmark; 24Department of Psychiatry and Psychotherapy, Semmelweis University, Budapest, Hungary; 25Section of Psychiatry and Clinical Psychology, University of Verona, Verona, Italy; 26Department of Epidemiology and Biostatistics and Department of Urology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands; 27Department of Medical Genetics, Ulleval University Hospital and Institute of Psychiatry, University of Oslo, Oslo, Norway; 28Mental Health Research Center, Russian Academy of Medical Sciences, Moscow, Russia; 29Division of Psychological Medicine, Institute of Psychiatry, King’s College, London, UK; 30Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, King’s College, London, UK; 31Psychiatric Laboratory, Department of Psychiatry, West China Hospital, Sichuan University, Sichuan, China; 32Department of Mental Health, University of Aberdeen, Royal Cornhill Hospital, Aberdeen, UK; 33Ravenscraig Hospital, Greenock, UK; 34Department of Human Genetics, UCLA, Los Angeles, CA, USA; 35Department of Clinical Neuroscience, HUBIN project, Karolinska Institutet and Hospital, Stockholm, Sweden and 36Institute of Human Genetics, University of Bonn, Bonn, Germany Correspondence: Dr K Stefansson, deCODE genetics, Sturlugata 8, Reykjavik IS-101, Iceland. E-mail: [email protected] 37See Appendix. Received 29 July 2009; revised 1 October 2009; accepted 21 October 2009; published online 5 January 2010 ZNF804A variants associated with psychosis S Steinberg et al 60 A trio of genome-wide association studies recently reported sequence variants at three loci to be significantly associated with schizophrenia. No sequence polymorphism had been unequivocally (P <5Â 10À8) associated with schizophrenia earlier. However, one variant, rs1344706[T], had come very close. This polymorphism, located in an intron of ZNF804A, was reported to associate with schizophrenia with a P-value of 1.6 Â 10À7, and with psychosis (schizophrenia plus bipolar disorder) with a P-value of 1.0 Â 10À8. In this study, using 5164 schizophrenia cases and 20 709 controls, we replicated the association with schizophrenia (odds ratio OR = 1.08, P = 0.0029) and, by adding bipolar disorder patients, we also confirmed the association with psychosis (added N = 609, OR = 1.09, P = 0.00065). Furthermore, as it has been proposed that variants such as rs1344706[T]—common and with low relative risk—may also serve to identify regions harboring less common, higher-risk susceptibility alleles, we searched ZNF804A for large copy number variants (CNVs) in 4235 psychosis patients, 1173 patients with other psychiatric disorders and 39 481 controls. We identified two CNVs including at least part of ZNF804A in psychosis patients and no ZNF804A CNVs in controls (P = 0.013 for association with psychosis). In addition, we found a ZNF804A CNV in an anxiety patient (P = 0.0016 for association with the larger set of psychiatric disorders). Molecular Psychiatry (2011) 16, 59–66; doi:10.1038/mp.2009.149; published online 5 January 2010 Keywords: schizophrenia; bipolar disorder; ZNF804A; CNV; association Introduction phenotype was expanded to psychosis. In addition, we examined ZNF804A for large structural variants, Before the publication of recent genome-wide asso- and found CNVs in three patients with psychiatric 1–3 ciation (GWA) studies, the sequence variant having disorders, but not in controls. the strongest evidence for unconditional association with schizophrenia was rs1344706[T]. This variant Materials and methods was reported to be associated with schizophrenia with an odds ratio (OR) of 1.12 and a P-value of Samples 1.6 Â 10À7. Evidence for association was strengthened Full information about each study group is presented (OR = 1.12, P = 1.0 Â 10À8) when a psychosis pheno- in the Supplementary Methods. Individuals were type (schizophrenia plus bipolar disorder) was diagnosed according to International Statistical Clas- assessed.4 More recently, rs1344706 was shown to sification of Diseases and Related Health Problems be associated with alterations in the functional 10th Revision (ICD-10) or Diagnostic and Statistical connectivity of various regions of the brain.5 The Manual of Mental Disorders, Fourth Edition (DSM-IV) single-nucleotide polymorphism (SNP) is located in criteria. Because of variation in diagnostic criteria and an intron of ZNF804A, a gene encoding a protein protocols between the various centers, some pheno- predicted to be a transcription factor. typic heterogeneity is expected. All individuals Current discussions of GWA studies have suggested provided written, informed consent for participation that findings of common SNP association may be and approval was obtained from the ethics commit- exploited by examining the region surrounding the tees at each location. initial variant for additional polymorphisms not In the initial analysis of rs1344706 association with tagged by the original variant.6–8 Of particular interest schizophrenia, genome-wide typed samples from are low frequency (between 5 and 1%) and rare seven European locations were included. After ( < 1%) susceptibility polymorphisms that may confer quality control, case/control samples from England a higher risk than the originally described variant but (93/88), Finland/excluding Kuusamo (59/147), Fin- are unlikely, because of their frequency, to be land/Kuusamo (123/50), Iceland (589/11 492), Italy discovered by standard GWA study. An example of (84/89), the Netherlands (693/3689) and Scotland the successful use of this strategy is in nonalcoholic (658/661) were included. With the exception of the fatty liver disease where the finding of a common samples from the Netherlands, these samples derived PNPLA3 susceptibility allele was followed by the from the genome-wide data described in our primary discovery, using re-sequencing, of an excess of null GWA report.3 Additional samples from Bonn and sequence mutations in individuals with the highest Munich that were part of the earlier data set were not hepatic fat levels as well as a protective allele that was used here as they had been included in the initial
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