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De novo mutations in schizophrenia implicate synaptic networks
Open accessAbstract
Inherited alleles account for most of the genetic risk for schizophrenia. However, new (de novo) mutations, in the form of large chromosomal copy number changes, occur in a small fraction of cases and disproportionally disrupt genes encoding postsynaptic proteins. Here we show that small de novo mutations, affecting one or a few nucleotides, are overrepresented among glutamatergic postsynaptic proteins comprising activity-regulated cytoskeleton-associated protein (ARC) and N-methyl-d-aspartate receptor (NMDAR) complexes. Mutations are additionally enriched in proteins that interact with these complexes to modulate synaptic strength, namely proteins regulating actin filament dynamics and those whose messenger RNAs are targets of fragile X mental retardation protein (FMRP). Genes affected by mutations in schizophrenia overlap those mutated in autism and intellectual disability, as do mutation-enriched synaptic pathways. Aligning our findings with a parallel case-control study, we demonstrate reproducible insights into aetiological mechanisms for schizophrenia and reveal pathophysiology shared with other neurodevelopmental disorders.
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“While most children with SCN2A variants fit into one of these three categories, there are some exceptions, including epileptic encephalopathy with choreoathetoid movements [26,27], benign infantile seizures with late-onset episodic ataxia [28–31], childhood-onset epileptic encephalopathy [32], and schizophrenia [33,34].”
From Progress in Understanding and Treating SCN2A-Mediated Disorders (2018) · cites this paper as [33]
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In the citing paper
“We tested for and found that genes in which rare variants increase risk of ASD and DD32,33 are also enriched for schizophrenia common variant associations.”
From Mapping genomic loci implicates genes and synaptic biology in schizophrenia (2022) · cites this paper as [32]
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In the citing paper
“The human NDR2 gene (STK38l) has been identified as a susceptibility gene for neurodevelopmental disorders, intellectual disability (Madencioglu et al. 2021; Firth et al. 2009), and autism spectrum disorder (Fromer et al. 2014).”
From The Serine/Threonine Kinase NDR2 Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Fromer et al. 2014
Experimental — accuracy not yet measuredIn the citing paper
“We controlled for a set of 10,360 genes with detectable expression in brain tissue measured as Fragments Per Kilobase of transcript per Million mapped reads (FPKM)32 to detect synaptic signals above signals simply reflecting the property of brain expression.”
From Mapping genomic loci implicates genes and synaptic biology in schizophrenia (2022) · cites this paper as [32]
In the citing paper
“Thus, many severe mutations do not converge on one specific phenotype but instead seem to cause a range of clinical disorders74,76,80,81,84,87,91.”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [80]
In the citing paper
“Protein-truncating variants (PTVs) are among the most interpretable associations as they suggest that the effect on disease most commonly tracks with decreasing expression of the gene18.”
From Rare coding variants in ten genes confer substantial risk for schizophrenia (2022) · cites this paper as [18]
In the citing paper
“This elevation of protein-compromising URVs was several times larger than an analogously elevated rate for de novo mutations”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [12]
In the citing paper
“A strong and consistent finding in exome-sequencing studies of schizophrenia involves an excess of variants in genes whose mRNAs are bound by the fragile X mental retardation protein (FMRP)9,12,27.”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [12]
In the citing paper
“we identified an ultra-rare splice donor variant in TAF1312, an ultra-rare nonsense variant in SETD1A16,17, and a single ultra-rare nonsense variant in NRXN1, a gene in which exonic deletions associate with schizophrenia18.”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [12]
In the citing paper
“These data yielded an elevation of about 0.03 such DNMs per exome, based on the difference between rates of 0.185 (95% CI 0.151-0.219) for individuals with schizophrenia12 and 0.156 (95% CI 0.139-0.174) for unaffected individuals13.”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [12]
In the citing paper
“Estimated 3rd and 5th principal components corresponded to previously observed Finnish and Northern-Southern Sweden clines12 (Supplementary Fig. 12d)”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [12]
In the citing paper
“The available data are incomplete but implicate synaptic components, including calcium channel subunits and post-synaptic elements5–7.”
From Gene expression elucidates functional impact of polygenic risk for schizophrenia (2016) · cites this paper as [7]
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Metadata
- Authors
- Fromer, M., Pocklington, A. J., Kavanagh, D. H., Williams, H. J., Dwyer, S., Gormley, P., Georgieva, L., Rees, E., Palta, P., Ruderfer, D. M., Carrera, N., Humphreys, I., Johnson, J. S., Roussos, P., Barker, D. D., Banks, E., Milanova, V., Grant, S. G., Hannon, E., Rose, S. A., Chambert, K., Mahajan, M., Scolnick, E. M., Moran, J. L., Kirov, G., Palotie, A., McCarroll, S. A., Holmans, P., Sklar, P., Owen, M. J., Purcell, S. M., & O’Donovan, M. C.
- Affiliations
- Broad Institute (US)
- Cardiff University (GB)
- University of Helsinki (FI)
- Icahn School of Medicine at Mount Sinai (US)
- Medical University of Sofia (BG)
- University of Edinburgh (GB)
- Corresponding author
- Owen, Michael J.
- ORCID
- Fromer, Menachem
- Pocklington, Andrew J.
- Williams, Hywel J.
- Dwyer, Sarah
- Gormley, Padhraig
- Rees, Elliott
- Palta, Priit
- Ruderfer, Douglas M.
- Carrera, Noa
- Johnson, Jessica S.
- Roussos, Panos
- Banks, Eric
- Milanova, Vihra
- Grant, Seth G.
- Hannon, Eilis
- Rose, Samuel A.
- Scolnick, Edward M.
- Moran, Jennifer L.
- Kirov, George
- Palotie, Aarno
- McCarroll, Steven A.
- Holmans, Peter
- Sklar, Pamela
- Owen, Michael J.
- Purcell, Shaun M.
- O’Donovan, Michael C.
- Venue
- Nature
- Published
- 2014-01-22
- Volume
- 506
- Issue
- 7487
- Pages
- 179-184
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4237002
- OpenAlex
- W2023962370
- Cited by
- 1,617
- References
- 43
- Citations by year
- 2026: 39 · 2025: 68 · 2024: 64 · 2023: 91 · 2022: 114 · 2021: 134 · 2020: 127 · 2019: 168 · 2018: 149 · 2017: 193 · 2016: 186 · 2015: 164 · 2014: 120
- FWCI
- 168.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01BX002395)
- Wellcome Trust (089062, WT 098051, WT089062, 098051)
- Medical Research Council (MR/L010305/1)
- National Institute of Mental Health (P50MH066392, R01MH071681, R01MH099126)
- National Human Genome Research Institute (R01HG005827)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Keywords
- schizophrenia, de novo mutations, synaptic proteins, glutamatergic synapses, activity-regulated cytoskeleton-associated protein, NMDA receptor, FMRP, actin filament dynamics, autism spectrum disorder, intellectual disability, neurodevelopmental disorders, synaptic efficacy
- MeSH terms
- Child Development Disorders, Pervasive, Cytoskeletal Proteins, Humans, Intellectual Disability, Models, Neurological, Mutation, Nerve Net, Nerve Tissue Proteins, Neural Pathways, Phenotype, RNA, Messenger, Schizophrenia, Substrate Specificity, Synapses, Receptors, N-Methyl-D-Aspartate, Fragile X Messenger Ribonucleoprotein 1, Exome, Mutation Rate
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