Enrichment of the local synaptic translatome for genetic risk associated with schizophrenia and autism spectrum disorder.

Local translation autism spectrum disorder genome-wide association study schizophrenia synapse transcriptome

Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
14 Dec 2023
Historique:
received: 30 05 2023
revised: 15 11 2023
accepted: 11 12 2023
medline: 17 12 2023
pubmed: 17 12 2023
entrez: 16 12 2023
Statut: aheadofprint

Résumé

Genes encoding synaptic proteins or mRNA targets of the RNA binding protein, Fragile X mental retardation protein (FMRP), have been linked to schizophrenia and autism spectrum disorder (ASD) through the enrichment of genetic variants conferring risk to these disorders. FMRP binds many transcripts with synaptic functions and is thought to regulate their local translation, a process which enables rapid and compartmentalized protein synthesis required for development and plasticity. We used summary statistics from large-scale genome-wide association studies of schizophrenia (74,776 cases, 101,023 controls) and ASD (18,381 cases, 27,969 controls) to test the hypothesis that the subset of synaptic genes encoding localized transcripts is more strongly associated with each disorder than non-localized transcripts. We also postulated that this subset of synaptic genes is responsible for associations attributed to FMRP targets. Schizophrenia associations were enriched in genes encoding localized synaptic transcripts compared to the remaining synaptic genes, or to the remaining localized transcripts; this also applied to ASD associations, although only for transcripts observed after stimulation by fear conditioning. The genetic associations with either disorder captured by these gene sets were independent of those derived from FMRP targets. Schizophrenia association was related to FMRP interactions with mRNAs in somata, but not in dendrites, whilst ASD association was related to FMRP binding in either compartment. Our data suggest that synaptic transcripts capable of local translation are particularly relevant to the pathogenesis of schizophrenia and ASD, but do not characterize the associations attributed to current sets of FMRP targets.

Sections du résumé

BACKGROUND BACKGROUND
Genes encoding synaptic proteins or mRNA targets of the RNA binding protein, Fragile X mental retardation protein (FMRP), have been linked to schizophrenia and autism spectrum disorder (ASD) through the enrichment of genetic variants conferring risk to these disorders. FMRP binds many transcripts with synaptic functions and is thought to regulate their local translation, a process which enables rapid and compartmentalized protein synthesis required for development and plasticity.
METHODS METHODS
We used summary statistics from large-scale genome-wide association studies of schizophrenia (74,776 cases, 101,023 controls) and ASD (18,381 cases, 27,969 controls) to test the hypothesis that the subset of synaptic genes encoding localized transcripts is more strongly associated with each disorder than non-localized transcripts. We also postulated that this subset of synaptic genes is responsible for associations attributed to FMRP targets.
RESULTS RESULTS
Schizophrenia associations were enriched in genes encoding localized synaptic transcripts compared to the remaining synaptic genes, or to the remaining localized transcripts; this also applied to ASD associations, although only for transcripts observed after stimulation by fear conditioning. The genetic associations with either disorder captured by these gene sets were independent of those derived from FMRP targets. Schizophrenia association was related to FMRP interactions with mRNAs in somata, but not in dendrites, whilst ASD association was related to FMRP binding in either compartment.
CONCLUSIONS CONCLUSIONS
Our data suggest that synaptic transcripts capable of local translation are particularly relevant to the pathogenesis of schizophrenia and ASD, but do not characterize the associations attributed to current sets of FMRP targets.

Identifiants

pubmed: 38103876
pii: S0006-3223(23)01764-X
doi: 10.1016/j.biopsych.2023.12.006
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Auteurs

Nicholas E Clifton (NE)

Department of Clinical & Biomedical Sciences, Faculty of Health and Life Sciences, University of Exeter, Exeter, UK. Electronic address: n.clifton@exeter.ac.uk.

Julie Qiaojin Lin (JQ)

UK Dementia Research Institute, Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK; UK Dementia Research Institute, King's College London, London, UK.

Christine E Holt (CE)

Department of Physiology Development and Neuroscience, University of Cambridge, Cambridge, UK.

Michael C O'Donovan (MC)

Division of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff, United Kingdom.

Jonathan Mill (J)

Department of Clinical & Biomedical Sciences, Faculty of Health and Life Sciences, University of Exeter, Exeter, UK.

Classifications MeSH