Cited by 166Epigenetics and DNA MethylationGenomics and Chromatin DynamicsGenetic Associations and Epidemiology

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Neuronal brain-region-specific DNA methylation and chromatin accessibility are associated with neuropsychiatric trait heritability

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Rizzardi, Lindsay F., Hickey, Peter F., Rodriguez DiBlasi, Varenka, Tryggvadóttir, Rakel, Callahan, Colin M., Idrizi, Adrian, Hansen, Kasper D., Feinberg, Andrew P.·2019·Nature Neuroscience

DOI 10.1038/s41593-018-0297-8PMC PMC6348048

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Abstract

Epigenetic modifications confer stable transcriptional patterns in the brain, and both normal and abnormal brain function involve specialized brain regions. We examined DNA methylation by whole-genome bisulfite sequencing in neuronal and non-neuronal populations from four brain regions (anterior cingulate gyrus, hippocampus, prefrontal cortex, and nucleus accumbens) as well as chromatin accessibility in the latter two. We find pronounced differences in both CpG and non-CpG methylation (CG-DMRs and CH-DMRs) only in neuronal cells across brain regions. Neuronal CH-DMRs were highly associated with differential gene expression, whereas CG-DMRs were consistent with chromatin accessibility and enriched for regulatory regions. These CG-DMRs comprise ~12 Mb of the genome that is highly enriched for genomic regions associated with heritability of neuropsychiatric traits including addictive behavior, schizophrenia, and neuroticism, thus suggesting a mechanistic link between pathology and differential neuron-specific epigenetic regulation in distinct brain regions.

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Additional file 10 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471409
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Additional file 9 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471463
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Additional file 8 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471460
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Additional file 2 of Partial erosion on under-methylated regions and chromatin reprogramming contribute to oncogene activation in IDH mutant gliomas
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Additional file 17 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471430
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Additional file 3 of Partial erosion on under-methylated regions and chromatin reprogramming contribute to oncogene activation in IDH mutant gliomas
Wang, X., Dai, L., Liu, Y., Li, C., Fan, D., Zhou, Y., Li, P., Kong, Q., & Su, J. (2023) · Figshare · doi:10.6084/m9.figshare.22721492
Additional file 11 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471412
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Additional file 5 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471451
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Additional file 13 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471418
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Additional file 14 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471421
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Additional file 2 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471442
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Additional file 7 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471457
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Additional file 18 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471433
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Additional file 6 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471454
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Additional file 15 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471424
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Additional file 3 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471445
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Additional file 4 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471448
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Additional file 16 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471427
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Additional file 12 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471415
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Additional file 1 of Hemispheric asymmetry in the human brain and in Parkinson’s disease is linked to divergent epigenetic patterns in neurons
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Additional file 5 of Identification of cell type-specific methylation signals in bulk whole genome bisulfite sequencing data
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Additional file 1 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K. E., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471439
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Additional file 12 of Hemispheric asymmetry in the human brain and in Parkinson’s disease is linked to divergent epigenetic patterns in neurons
Li, P., Ensink, E., Lang, S., Marshall, L., Schilthuis, M., Lamp, J. A., Vega, I. E., & Labrie, V. (2020) · Figshare · doi:10.6084/m9.figshare.11960274
Additional file 1 of Partial erosion on under-methylated regions and chromatin reprogramming contribute to oncogene activation in IDH mutant gliomas
Wang, X., Dai, L., Liu, Y., Li, C., Fan, D., Zhou, Y., Li, P., Kong, Q., & Su, J. (2023) · Figshare · doi:10.6084/m9.figshare.22721486
Additional file 1 of PCA outperforms popular hidden variable inference methods for molecular QTL mapping
Zhou, H. J., Li, L., Li, Y., Li, W., & Li, J. J. (2022) · Figshare · doi:10.6084/m9.figshare.21314198
Additional file 2 of PCA outperforms popular hidden variable inference methods for molecular QTL mapping
Zhou, H. J., Li, L., Li, Y., Li, W., & Li, J. J. (2022) · Figshare · doi:10.6084/m9.figshare.21314204
Additional file 6 of Identification of cell type-specific methylation signals in bulk whole genome bisulfite sequencing data
Scott, C. A., Duryea, J., Mackay, H. A., Baker, M. S., Laritsky, E., Gunasekara, C., Coarfa, C., & Waterland, R. A. (2020) · Figshare · doi:10.6084/m9.figshare.12593130
Additional file 19 of Human brain region-specific variably methylated regions are enriched for heritability of distinct neuropsychiatric traits
Rizzardi, L. F., Hickey, P. F., Idrizi, A., Tryggvadóttir, R., Callahan, C. M., Stephens, K. E., Taverna, S. D., Zhang, H., Ramazanoglu, S., Hansen, K. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14471436
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Authors: Rizzardi, L. F., Hickey, P. F., Rodriguez DiBlasi, V., Tryggvadóttir, R., Callahan, C. M., Idrizi, A., Hansen, K. D., & Feinberg, A. P.
Affiliations: Johns Hopkins University (US)
Corresponding author: Hansen, Kasper D.
Feinberg, Andrew P.
ORCID: Rizzardi, Lindsay F.
Hickey, Peter F.
Tryggvadóttir, Rakel
Callahan, Colin M.
Idrizi, Adrian
Hansen, Kasper D.
Feinberg, Andrew P.
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2019-01-14
Volume: 22
Issue: 2
Pages: 307-316
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/s41593-018-0297-8
PMC: PMC6348048
OpenAlex: W2951502983
Cited by: 146
References: 82
Citations by year: 2026: 9 · 2025: 13 · 2024: 15 · 2023: 15 · 2022: 26 · 2021: 21 · 2020: 31 · 2019: 12
FWCI: 8.85
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (1s10od016315-01)
National Institute of Mental Health (U01MH104393)
National Cancer Institute (U24CA180996)
National Institute of Allergy and Infectious Diseases (P30AI094189)
Division of Materials Research
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Keywords: DNA methylation, chromatin accessibility, neuropsychiatric traits, heritability, non-CpG methylation, hippocampus, prefrontal cortex, nucleus accumbens, anterior cingulate cortex, schizophrenia, addictive behavior, neuroticism, differential gene expression, regulatory elements, DNA variants
MeSH terms: Neuroticism, Brain, Chromatin, Humans, Neurons, Schizophrenia, Genome, Behavior, Addictive, CpG Islands, DNA Methylation, Epigenesis, Genetic

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Neuronal brain-region-specific DNA methylation and chromatin accessibility are associated with neuropsychiatric trait heritability

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