Differential methylation of enhancer at IGF2 is associated with abnormal dopamine synthesis in major psychosis

Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls...

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Published inNature communications Vol. 10; no. 1; pp. 2046 - 12
Main Authors Pai, Shraddha, Li, Peipei, Killinger, Bryan, Marshall, Lee, Jia, Peixin, Liao, Ji, Petronis, Arturas, Szabó, Piroska E., Labrie, Viviane
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 03.05.2019
Nature Publishing Group
Nature Portfolio
Subjects
38/91
45/23
59
631/208/177
631/208/200
631/337/100/101
631/378/1689/1761
631/378/2583
64/60
82/58
Abnormalities
Adult
Aged
Animals
Bipolar disorder
Bipolar Disorder - genetics
Bipolar Disorder - pathology
Chromatin
Deoxyribonucleic acid
DNA
DNA Methylation
Dopamine
Dopamine - biosynthesis
Enhancer Elements, Genetic - genetics
Epigenesis, Genetic
Epigenetics
Female
Gene Expression Profiling
Growth factors
Humanities and Social Sciences
Humans
Hydroxylase
Insulin
Insulin-like growth factor II
Insulin-Like Growth Factor II - genetics
Male
Mental disorders
Mice
Mice, Knockout
Middle Aged
multidisciplinary
Neostriatum
Neurons
Neurons - pathology
Pathogenesis
Prefrontal cortex
Prefrontal Cortex - cytology
Prefrontal Cortex - pathology
Proteins
Proteomics
Psychosis
Schizophrenia
Schizophrenia - genetics
Schizophrenia - pathology
Science
Science (multidisciplinary)
Synthesis
Transcription
Transcriptome - genetics
Tyrosine
Tyrosine 3-monooxygenase
Tyrosine 3-Monooxygenase - genetics
Tyrosine 3-Monooxygenase - metabolism
Young Adult
Online AccessGet full text

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Abstract Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 ( IGF2 ) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase ( TH ) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis. Dopamine dysregulation is centrally linked to major psychosis. Here, the authors characterise the hypomethylation of an enhancer within the insulin-like growth factor 2 gene in neurons of patients with major psychosis and provide evidence that this enhancer targets the tyrosine hydroxylase gene, responsible for dopamine synthesis.
AbstractList Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 (IGF2) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase (TH) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis.Dopamine dysregulation is centrally linked to major psychosis. Here, the authors characterise the hypomethylation of an enhancer within the insulin-like growth factor 2 gene in neurons of patients with major psychosis and provide evidence that this enhancer targets the tyrosine hydroxylase gene, responsible for dopamine synthesis.
Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 ( IGF2 ) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase ( TH ) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis. Dopamine dysregulation is centrally linked to major psychosis. Here, the authors characterise the hypomethylation of an enhancer within the insulin-like growth factor 2 gene in neurons of patients with major psychosis and provide evidence that this enhancer targets the tyrosine hydroxylase gene, responsible for dopamine synthesis.
Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 (IGF2) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase (TH) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis.Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 (IGF2) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase (TH) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis.
Dopamine dysregulation is centrally linked to major psychosis. Here, the authors characterise the hypomethylation of an enhancer within the insulin-like growth factor 2 gene in neurons of patients with major psychosis and provide evidence that this enhancer targets the tyrosine hydroxylase gene, responsible for dopamine synthesis.
Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 (IGF2) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase (TH) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis.
Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we perform a multi-omics study of neurons isolated from the prefrontal cortex in schizophrenia and bipolar disorder (n = 55 cases and 27 controls). DNA methylation, transcriptomic, and genetic-epigenetic interactions in major psychosis converged on pathways of neurodevelopment, synaptic activity, and immune functions. We observe prominent hypomethylation of an enhancer within the insulin-like growth factor 2 ( IGF2 ) gene in major psychosis neurons. Chromatin conformation analysis revealed that this enhancer targets the nearby tyrosine hydroxylase ( TH ) gene responsible for dopamine synthesis. In patients, we find hypomethylation of the IGF2 enhancer is associated with increased TH protein levels. In mice, Igf2 enhancer deletion disrupts the levels of TH protein and striatal dopamine, and induces transcriptional and proteomic abnormalities affecting neuronal structure and signaling. Our data suggests that epigenetic activation of the enhancer at IGF2 may enhance dopamine synthesis associated with major psychosis.
ArticleNumber 2046
Author Liao, Ji
Petronis, Arturas
Jia, Peixin
Labrie, Viviane
Killinger, Bryan
Pai, Shraddha
Szabó, Piroska E.
Li, Peipei
Marshall, Lee
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  fullname: Labrie, Viviane
  email: viviane.labrie@vai.org
  organization: Center for Neurodegenerative Science, Van Andel Research Institute, Krembil Family Epigenetics Laboratory, Centre for Addiction and Mental Health, Division of Psychiatry and Behavioral Medicine, College of Human Medicine, Michigan State University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31053723$$D View this record in MEDLINE/PubMed
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Snippet Impaired neuronal processes, including dopamine imbalance, are central to the pathogenesis of major psychosis, but the molecular origins are unclear. Here we...
Dopamine dysregulation is centrally linked to major psychosis. Here, the authors characterise the hypomethylation of an enhancer within the insulin-like growth...
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Abnormalities
Adult
Aged
Animals
Bipolar disorder
Bipolar Disorder - genetics
Bipolar Disorder - pathology
Chromatin
Deoxyribonucleic acid
DNA
DNA Methylation
Dopamine
Dopamine - biosynthesis
Enhancer Elements, Genetic - genetics
Epigenesis, Genetic
Epigenetics
Female
Gene Expression Profiling
Growth factors
Humanities and Social Sciences
Humans
Hydroxylase
Insulin
Insulin-like growth factor II
Insulin-Like Growth Factor II - genetics
Male
Mental disorders
Mice
Mice, Knockout
Middle Aged
multidisciplinary
Neostriatum
Neurons
Neurons - pathology
Pathogenesis
Prefrontal cortex
Prefrontal Cortex - cytology
Prefrontal Cortex - pathology
Proteins
Proteomics
Psychosis
Schizophrenia
Schizophrenia - genetics
Schizophrenia - pathology
Science
Science (multidisciplinary)
Synthesis
Transcription
Transcriptome - genetics
Tyrosine
Tyrosine 3-monooxygenase
Tyrosine 3-Monooxygenase - genetics
Tyrosine 3-Monooxygenase - metabolism
Young Adult
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Title Differential methylation of enhancer at IGF2 is associated with abnormal dopamine synthesis in major psychosis
URI https://link.springer.com/article/10.1038/s41467-019-09786-7
https://www.ncbi.nlm.nih.gov/pubmed/31053723
https://www.proquest.com/docview/2219596797
https://www.proquest.com/docview/2229230438
https://pubmed.ncbi.nlm.nih.gov/PMC6499808
https://doaj.org/article/92406a1645fa465a86fc451c78740010
Volume 10
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