De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia.
paper
Cited
Public
- Authors
- Kirov, G; Pocklington, A J; Holmans, P; Ivanov, D; Ikeda, M; Ruderfer, D; Moran, J; Chambert, K; Toncheva, D; Georgieva, L; Grozeva, D; Fjodorova, M; Wollerton, R; Rees, E; Nikolov, I; van de Lagemaat, L N; BayΓ©s, A; Fernandez, E; Olason, P I; BΓΆttcher, Y; Komiyama, N H; Collins, M O; Choudhary, J; Stefansson, K; Stefansson, H; Grant, S G N; Purcell, S; Sklar, P; O'Donovan, M C; Owen, M J
- Year
- 2012
- Journal
- Molecular psychiatry
- PMID
- 22083728
- DOI
- 10.1038/mp.2011.154
- PMCID
- PMC3603134
A small number of rare, recurrent genomic copy number variants (CNVs) are known to substantially increase susceptibility to schizophrenia. As a consequence of the low fecundity in people with schizophrenia and other neurodevelopmental phenotypes to which these CNVs contribute, CNVs with large effects on risk are likely to be rapidly removed from the population by natural selection. Accordingly, such CNVs must frequently occur as recurrent de novo mutations. In a sample of 662 schizophrenia proband-parent trios, we found that rare de novo CNV mutations were significantly more frequent in cases (5.1% all cases, 5.5% family history negative) compared with 2.2% among 2623 controls, confirming the involvement of de novo CNVs in the pathogenesis of schizophrenia. Eight de novo CNVs occurred at four known schizophrenia loci (3q29, 15q11.2, 15q13.3 and 16p11.2). De novo CNVs of known pathogenic significance in other genomic disorders were also observed, including deletion at the TAR (thrombocytopenia absent radius) region on 1q21.1 and duplication at the WBS (Williams-Beuren syndrome) region at 7q11.23. Multiple de novos spanned genes encoding members of the DLG (discs large) family of membrane-associated guanylate kinases (MAGUKs) that are components of the postsynaptic density (PSD). Two de novos also affected EHMT1, a histone methyl transferase known to directly regulate DLG family members. Using a systems biology approach and merging novel CNV and proteomics data sets, systematic analysis of synaptic protein complexes showed that, compared with control CNVs, case de novos were significantly enriched for the PSD proteome (P=1.72 Γ 10β»βΆ. This was largely explained by enrichment for members of the N-methyl-D-aspartate receptor (NMDAR) (P=4.24 Γ 10β»βΆ) and neuronal activity-regulated cytoskeleton-associated protein (ARC) (P=3.78 Γ 10β»βΈ) postsynaptic signalling complexes. In an analysis of 18β492 subjects (7907 cases and 10β585 controls), case CNVs were enriched for members of the NMDAR complex (P=0.0015) but not ARC (P=0.14). Our data indicate that defects in NMDAR postsynaptic signalling and, possibly, ARC complexes, which are known to be important in synaptic plasticity and cognition, play a significant role in the pathogenesis of schizophrenia.
Histograms of distributions of z-scores. (a) A suggestive de novo and (b) an ambiguous de novo MeZOD call. Black arrows indicate the position of a parent, and red arrows of a child. The x axis shows the median z-scores for all individuals for a particular copy number variant (CNV) region.
Size of copy number variants (CNVs). KaplanβMeier survival graph for the size of de novo CNVs in cases, Icelandic controls, Bulgarian controls and unaffected siblings of autism probands.25
Disruption of postsynaptic signalling within activity-regulated cytoskeleton-associated protein (ARC) and N-methyl-D-aspartate receptor (NMDAR) complexes by copy number variants (CNVs). ARC and NMDAR bind to diverse structural and signalling molecules forming multiprotein complexes. Functional pathways encoded by these complexes are disrupted by de novo CNVs at multiple levels, as indicated by the purple asterisks (number of asterisks=number of de novos overlapping a gene or gene family). Calcium influx via the NMDAR, modulated by calcium release from internal stores (RYR2), drives downstream pathways whose association with the receptor is mediated by scaffold proteins (DLG1, DLG2, DLGAP1). Multiple pathways converge on ERK kinases (extracellular signal-regulated kinases), a focal point in the regulation of ARC transcription, dendritic localisation and local translation.47 ARC mRNA is transported to sites of synaptic activity in complexes containing CYFIP1, dissociation of which is required for ARC translation.49 CYFIP1 also regulates translation of CAMKII,49 a key component of NMDAR complexes. Although not identified in this study, deletions of synaptic adhesion protein NRXN1 (blue asterisk) have previously been found in schizophrenia.29 CNVs disrupting genes within these same functional pathways have also been identified in autism30(black asterisks).
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