De novo mutations in schizophrenia implicate synaptic networks
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 m...
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| Published in | Nature (London) Vol. 506; no. 7487; pp. 179 - 184 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
13.02.2014
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | 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.
The authors report the largest family-trio exome sequencing study of schizophrenia to date; mutations are overrepresented in genes for glutamatergic synaptic proteins and also genes mutated in autism and intellectual disability, providing insights into aetiological mechanisms and pathopshyisology shared with other neurodevelopmental disorders.
Pathogenic mechanisms in schizophrenia
Two major sequencing studies of the exome — the protein-coding portion of the genome — in schizophrenia sufferers and their relatives are published in this issue of
Nature
. Together they provide strong pointers to specific pathogenic mechanisms that disrupt the glutamatergic synapses in schizophrenia. In particular, mutations that influence the action of the scaffold protein ARC (activity-regulated cytoskeleton-associated protein) are prominently involved, as are mutations in targets of the fragile X mental retardation protein (FMRP). Defects in FMRP have previously been shown to be associated with autism spectrum disorders. |
|---|---|
| AbstractList | 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. 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. The authors report the largest family-trio exome sequencing study of schizophrenia to date; mutations are overrepresented in genes for glutamatergic synaptic proteins and also genes mutated in autism and intellectual disability, providing insights into aetiological mechanisms and pathopshyisology shared with other neurodevelopmental disorders. Pathogenic mechanisms in schizophrenia Two major sequencing studies of the exome — the protein-coding portion of the genome — in schizophrenia sufferers and their relatives are published in this issue of Nature . Together they provide strong pointers to specific pathogenic mechanisms that disrupt the glutamatergic synapses in schizophrenia. In particular, mutations that influence the action of the scaffold protein ARC (activity-regulated cytoskeleton-associated protein) are prominently involved, as are mutations in targets of the fragile X mental retardation protein (FMRP). Defects in FMRP have previously been shown to be associated with autism spectrum disorders. 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. The authors report the largest family-trio exome sequencing study of schizophrenia to date; mutations are overrepresented in genes for glutamatergic synaptic proteins and also genes mutated in autism and intellectual disability, providing insights into aetiological mechanisms and pathopshyisology shared with other neurodevelopmental disorders. Pathogenic mechanisms in schizophrenia Two major sequencing studies of the exome -- the protein-coding portion of the genome -- in schizophrenia sufferers and their relatives are published in this issue of Nature. Together they provide strong pointers to specific pathogenic mechanisms that disrupt the glutamatergic synapses in schizophrenia. In particular, mutations that influence the action of the scaffold protein ARC (activity-regulated cytoskeleton-associated protein) are prominently involved, as are mutations in targets of the fragile X mental retardation protein (FMRP). Defects in FMRP have previously been shown to be associated with autism spectrum disorders. 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. [PUBLICATION ABSTRACT] 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 mRNAs 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. |
| Audience | Academic |
| Author | Kavanagh, David H. Gormley, Padhraig Williams, Hywel J. Banks, Eric Scolnick, Edward M. Barker, Douglas D. Fromer, Menachem Milanova, Vihra Palta, Priit Holmans, Peter Johnson, Jessica S. Ruderfer, Douglas M. Humphreys, Isla Rose, Samuel A. Grant, Seth G. Dwyer, Sarah Carrera, Noa Purcell, Shaun M. Chambert, Kimberly Moran, Jennifer L. Roussos, Panos Palotie, Aarno Kirov, George McCarroll, Steven A. Hannon, Eilis Georgieva, Lyudmila O’Donovan, Michael C. Mahajan, Milind Rees, Elliott Pocklington, Andrew J. Sklar, Pamela Owen, Michael J. |
| AuthorAffiliation | 7 Department of Psychiatry, Medical University, Sofia 1431, Bulgaria 1 Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA 4 Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA 6 Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA 10 Department of Genetics, Harvard Medical School, Boston, MA, 02115, USA 12 Analytic and Translational Genetics Unit, Psychiatric and Neurodevelopmental Genetics Unit, Massachusetts General Hospital, Boston, MA, 02114, USA 2 Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University 5 Department of Bioinformatics, Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia 9 Institute for Molecular Medicine Finland (FIM |
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givenname: Elliott surname: Rees fullname: Rees, Elliott organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 9 givenname: Priit surname: Palta fullname: Palta, Priit organization: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, UK , Department of Bioinformatics, Institute of Molecular and Cell Biology, University of Tartu, 51010 Tartu, Estonia, Institute for Molecular Medicine Finland (FIMM), University of Helsinki, 00290 Helsinki, Finland – sequence: 10 givenname: Douglas M. surname: Ruderfer fullname: Ruderfer, Douglas M. organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 11 givenname: Noa surname: Carrera fullname: Carrera, Noa organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 12 givenname: Isla surname: Humphreys fullname: Humphreys, Isla organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 13 givenname: Jessica S. surname: Johnson fullname: Johnson, Jessica S. organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai – sequence: 14 givenname: Panos surname: Roussos fullname: Roussos, Panos organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai – sequence: 15 givenname: Douglas D. surname: Barker fullname: Barker, Douglas D. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard – sequence: 16 givenname: Eric surname: Banks fullname: Banks, Eric organization: Program in Medical and Population Genetics, Broad Institute of MIT and Harvard – sequence: 17 givenname: Vihra surname: Milanova fullname: Milanova, Vihra organization: Department of Psychiatry, Medical University, Sofia 1431, Bulgaria – sequence: 18 givenname: Seth G. surname: Grant fullname: Grant, Seth G. organization: Centre for Neuroregeneration, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 19 givenname: Eilis surname: Hannon fullname: Hannon, Eilis organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 20 givenname: Samuel A. surname: Rose fullname: Rose, Samuel A. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard – sequence: 21 givenname: Kimberly surname: Chambert fullname: Chambert, Kimberly organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard – sequence: 22 givenname: Milind surname: Mahajan fullname: Mahajan, Milind organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai – sequence: 23 givenname: Edward M. surname: Scolnick fullname: Scolnick, Edward M. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard – sequence: 24 givenname: Jennifer L. surname: Moran fullname: Moran, Jennifer L. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard – sequence: 25 givenname: 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Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 29 givenname: Pamela surname: Sklar fullname: Sklar, Pamela organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 30 givenname: Michael J. surname: Owen fullname: Owen, Michael J. email: owenmj@cardiff.ac.uk organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK – sequence: 31 givenname: Shaun M. surname: Purcell fullname: Purcell, Shaun M. organization: Division of Psychiatric Genomics in the Department of Psychiatry, and Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Analytic and Translational Genetics Unit, Psychiatric and Neurodevelopmental Genetics Unit, Massachusetts General Hospital – sequence: 32 givenname: Michael C. surname: O’Donovan fullname: O’Donovan, Michael C. organization: Medical Research Council Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff CF24 4HQ, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24463507$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author Contributions The project was led in Cardiff by MCOD & MJO, in Mount Sinai by SMP & PS, at the Broad by SAMC & JLM, and at the Sanger by AP. HJW, JLM, KC, JSJ, DDB, MM & SAR were responsible for sample processing and data management. MF, HJW, PG, DMR, DHK, GK, ER & SD processed NGS data, annotated and validated mutations. LG, NC, IH, SD, HJW & SAR undertook validation of mutations and additional lab work. AJP, MF, DHK, SMP & PH co-ordinated/undertook the main bioinformatics/statistical analyses. ER, DMR, EB, PP, EH & PR performed additional analyses. SGG contributed additional insights into synaptic biology. Sample recruitment was led by GK and VM. The main findings were interpreted by MOD, MF, MJO, PH, GK, EMS, SAMC, DHK, AJP, AP, SMP, & PS who drafted the manuscript. |
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| Snippet | Inherited alleles account for most of the genetic risk for schizophrenia. However, new (
de novo
) mutations, in the form of large chromosomal copy number... Inherited alleles account for most of the genetic risk for schizophrenia. However, new (de novo) mutations, in the form of large chromosomal copy number... |
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| SubjectTerms | 631/208/514/2254 631/378/2583 692/499 692/699/476/1799 Allelomorphism Autism Child Development Disorders, Pervasive - genetics Cytoskeletal Proteins - metabolism DNA sequencing Exome - genetics Fragile X Mental Retardation Protein - metabolism Gene mutations Genes Genetic aspects Health aspects Humanities and Social Sciences Humans Intellectual Disability - genetics Mental disorders Models, Neurological multidisciplinary Mutation Mutation - genetics Mutation Rate Nerve Net - metabolism Nerve Net - physiopathology Nerve Tissue Proteins - metabolism Neural circuitry Neural Pathways - metabolism Neural Pathways - physiopathology Nucleotide sequencing Phenotype Proteins Psychological aspects Receptors, N-Methyl-D-Aspartate - metabolism Risk factors RNA, Messenger - genetics RNA, Messenger - metabolism Schizophrenia Schizophrenia - genetics Schizophrenia - metabolism Schizophrenia - physiopathology Science Studies Substrate Specificity Synapses Synapses - metabolism |
| Title | De novo mutations in schizophrenia implicate synaptic networks |
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