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Evidence for Association of DNA Sequence Variants in The Molecular Psychiatry (2006) 11, 837–846 & 2006 Nature Publishing Group All rights reserved 1359-4184/06 $30.00 www.nature.com/mp ORIGINAL ARTICLE Evidence for association of DNA sequence variants in the phosphatidylinositol-4-phosphate 5-kinase IIa gene (PIP5K2A) with schizophrenia SG Schwab1,2,3, M Knapp4, P Sklar5,6, GN Eckstein7, C Sewekow3, M Borrmann-Hassenbach8, M Albus8, T Becker4, JF Hallmayer9, B Lerer10, W Maier3 and DB Wildenauer2,11 1Western Australian Institute of Medical Research and Center for Medical Research, University of Western Australia, Perth, WA, Australia; 2School of Psychiatry and Clinical Neurosciences, University of Western Australia, Perth, WA, Australia; 3Department of Psychiatry, University of Bonn, Bonn, Germany; 4Institute for Medical Biometry, Informatics and Epidemiology, University of Bonn, Bonn, Germany; 5Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Cambridge, MA, USA; 6Department of Psychiatry, Psychiatric and Neurodevelopmental Genetics Unit, Center for Human Genetics Research, Harvard Medical School, Massachusetts General Hospital, Charlestown, MA, USA; 7Institute of Human Genetics, GSF-National Research Center for Environment and Health, Munich, Germany; 8Mental State Hospital, Haar, Germany; 9Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Palo Alto, CA, USA; 10Department of Psychiatry, Hadassah-Hebrew University Medical Center, Jerusalem, Israel and 11Center for Clinical Research in Neuropsychiatry, Graylands Hospital, Mt Claremont, WA, Australia Linkage studies in schizophrenia have identified a candidate region on chromosome 10p14–11 as reported for several independent samples. We investigated association of DNA sequence variants in a plausible candidate gene located in this region, the gene for phosphatidylinositol- 4-phosphate 5-kinase IIa (PIP5K2A), in a sample of 65 sib-pair families for which linkage had been reported. Evidence for association was obtained for 15 polymorphisms spanning 73.6 kb in the genomic region of the gene between intron 4 and the 30 untranslated region, a region with high degree of linkage disequilibrium. Single nucleotide polymorphism (SNP) rs10828317 located in exon 7 and causing a non-synonymous amino-acid exchange (asparagine/serine) produced a P-value of 0.001 (experiment-wide significance level 0.00275) for over-transmission of the major allele coding for serine, analysed by transmission disequilibrium test using FAMHAP. Association of this SNP with schizophrenia has been also described in a sample of 273 Dutch schizophrenic patients and 580 controls (P = 0.0004). PIP5K2A is involved in the biosynthesis of phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2), one of the key metabolic crossroads in phosphoinositide signalling. PI(4,5)P2 plays a role in membrane transduction of neurotransmitter signals as well as in intracellular signalling, pathways that may be impaired in schizophrenia. Molecular Psychiatry (2006) 11, 837–846. doi:10.1038/sj.mp.4001864; published online 27 June 2006 Keywords: linkage disequilibrium; single nucleotide polymorphism; non-synonymous amino-acid exchange; phosphoinositide cell signalling; candidate gene Introduction The lack of a one to one relationship between phenotype and genotype renders application of Schizophrenia is a devastating mental disorder with classical linkage analysis in complex disorders diffi- complex genetic background.1 Susceptibility alleles, cult.2 Despite this constraint, a number of linkage that is, alleles conferring risk for the disorder and studies have been performed in schizophrenia using having only a moderate effect on phenotype expres- parametric and non-parametric methods.3 Statistical sion, are expected to contribute to the development of evidence for linkage has been reported for several the disorder. This is in contrast to most monogenic regions, distributed over the whole genome. However, disorders where causative DNA sequence variants the majority of these linkage studies did not fulfil (mutations) with usually larger effects are involved. stringent criteria such as genome-wide significance, concentration of elevated LOD scores within a narrow defined peak and replication in independent family Correspondence: Dr DB Wildenauer, Center for Clinical Research samples. Consequently, detecting linkage in schizo- in Neuropsychiatry (CCRN), Graylands Hospital, Private Bag #1, phrenia cannot be taken as proof for existence of a Claremont, WA 6910, Australia. susceptibility gene, but may be suggestive for regions E-mail: [email protected] Received 7 March 2006; revised 30 May 2006; accepted 5 June that can be tested for the existence of candidate genes 2006; published online 27 June 2006 associated with the disorder. Association of PIP5K2A with schizophrenia SG Schwab et al 838 DNA sequence variants in potential susceptibility approach and investigated association of DNA se- genes associated with schizophrenia have been quence variants in the region, where PIP5K2A is detected in some regions where evidence for linkage located, using the family sample where we had has been reported previously. On chromosome detected linkage. We detected several variants in 8p22–21,4–6 DNA sequence variants in the gene for linkage disequilibrium (LD) with schizophrenia in the neuregulin 1 have been found to be associated with genomic region of PIP5K2A. One of the variants, M41, schizophrenia as single markers and, in combination, that produced nominally significant P-values in this as multilocus haplotypes.7,8 Association of single study is located in exon 7 of the gene and constitutes nucleotide polymorphisms (SNPs) in the genomic a non-synonymous amino-acid exchange N/S in region of dystrobrevin binding protein 1 (dysbindin) position 251 of the protein. Over-transmission of the located on chromosome 6p24–22, another region with allele with major frequency coding for S was observed evidence for linkage to schizophrenia,4,9–15 has been in our family sample. reported.16–20 Further candidate genes identified in areas with reported linkage to schizophrenia include G72 on chromosome 13q32–q34,21 RGS4,22 Materials and methods Capon23 and DISC124,25 on chromosome 1q21–q22, Families TRAR4 on chromosome 6q13–q2626 and Epsin 4 on The sib-pair sample consisted of 65 families with chromosome 5q.27 141 affected offspring. Fifty-six families were from For most of these genes, a role in brain function has Germany and nine from Israel. The sample was taken been proposed,28 but DNA variants (mutations in from 71 families included in the linkage studies coding or regulatory sequences) with impact on brain previously reported.33,37 For six families, the supply function and eventually leading to the development of DNA was not available in sufficient quantity for of schizophrenia have not been identified yet. Thus, these studies. There were 57 families with affected some of the currently proposed susceptibility genes sib pairs, six families with three affected, one with may turn out to be false positives, whereas others still four and one with five. With the exception of three remain to be discovered. The number of true suscept- sib-pair families and one triplet with one parent, but ibility genes involved in development of schizophre- with additional unaffected family members, DNA nia cannot be estimated at the present stage. was available for both parents. All individuals had Evidence from linkage analysis for a locus, con- been interviewed with the Schedule for Affective ferring susceptibility to schizophrenia on chromo- Disorder Schizophrenia-Lifetime Version (SADS-L) some 10p14–p11, has been reported by a number of or the Structured Clinical Interview for DSM-III-R studies.29–36 In addition, evidence for linkage to bipolar Disorders (SCID-II).42 Case records were evaluated by disorder has been reported in this region for the NIMH operational criteria checklist for psychotic illness consortium bipolar sample.30 The highest LOD scores (OPCRIT).43 The complete interview form, family obtained in these studies were concentrating around history information and the medical record of each the microsatellite marker D10S1423 comprising a individual were reviewed by an independent relatively small area. As parental genotype information psychiatrist without prior knowledge of family is available in our sample with linkage,37 we had relationship to the index patient or of morbidity in been able to apply a transmission disequilibrium test the family. The 141 affected offspring consisted of modified for application to sib-pairs in order to test for 121 individuals with a core diagnosis of schizo- association in the presence of linkage.38 We tested all phrenia (DSM-III-R) and 20 individuals with a diag- microsatellite markers from our genome-wide scan nosis of schizoaffective disorder, schizophrenic sub- using the ASPEX program and obtained a nominally type, according to the Research Diagnostic Criteria.44 significant P-value of 0.038 for marker D10S211,37 Written informed consent was obtained from all which is located in the linkage peak. participants after a detailed description of the study, We searched databases for candidate genes in the which was approved by the internal review boards of vicinity of D10S211 and identified approximately the University of Bonn, Germany; the Hadassah- 900 kb downstream the gene for the enzyme phos- Hebrew University Medical Center, Israel; and the phatidylinositol-4-phosphate 5-kinase, type II, alpha Mental State Hospital,
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