Cell-specific histone modification maps in the human frontal lobe link schizophrenia risk to the neuronal epigenome
Open accessAbstract
Risk variants for schizophrenia affect more than 100 genomic loci, yet cell- and tissue-specific roles underlying disease liability remain poorly characterized. We have generated for two cortical areas implicated in psychosis, the dorsolateral prefrontal cortex and anterior cingulate cortex, 157 reference maps from neuronal, neuron-depleted and bulk tissue chromatin for two histone marks associated with active promoters and enhancers, H3-trimethyl-Lys4 (H3K4me3) and H3-acetyl-Lys27 (H3K27ac). Differences between neuronal and neuron-depleted chromatin states were the major axis of variation in histone modification profiles, followed by substantial variability across subjects and cortical areas. Thousands of significant histone quantitative trait loci were identified in neuronal and neuron-depleted samples. Risk variants for schizophrenia, depressive symptoms and neuroticism were significantly over-represented in neuronal H3K4me3 and H3K27ac landscapes. Our Resource, sponsored by PsychENCODE and CommonMind, highlights the critical role of cell-type-specific signatures at regulatory and disease-associated noncoding sequences in the human frontal lobe. This PsychENCODE resource presents 157 reference maps for open-chromatin-associated histone methylation and acetylation in prefrontal and anterior cingulate cortex, linking the neuronal epigenome to the genetic risk architecture of schizophrenia.
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Two histone markers associated with transcriptional activation (H3K4me3 and H3K27ac) are enriched at SZ genetic risk variants.
“two histone markers associated with transcriptional activation (H3K4me3 and H3K27ac) are enriched at SZ genetic risk variants 198.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [198]
The majority of NeuN+ and NeuN− FIREs overlap with NeuN+ and NeuN− differential H3K27ac peaks, respectively.
“We found that the majority of NeuN+ and NeuN− FIREs overlapped with NeuN+ and NeuN− differential H3K27ac peaks, respectively, displaying remarkable cell-type-specificity (Fig. 1c, d).”
From Neuronal and glial 3D chromatin architecture informs the cellular etiology of brain disorders (2021) · cites this paper as [27]
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Mich, J. K., Graybuck, L. T., Hess, E. E., Mahoney, J. T., Kojima, Y., Ding, Y., Somasundaram, S., Miller, J. A., Kalmbach, B. E., Radaelli, C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108754 · Cited by 193 · see citing works
Neuronal and glial 3D chromatin architecture informs the cellular etiology of brain disorders
Hu, B., Won, H., Mah, W., Park, R. B., Kassim, B., Spiess, K., Kozlenkov, A., Crowley, C. A., Pochareddy, S., The PsychENCODE Consortium, et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24243-0 · Cited by 103 · see citing works
Self-citation
- Authors
- Girdhar, K., Hoffman, G. E., Jiang, Y., Brown, L., Kundakovic, M., Hauberg, M. E., Francoeur, N. J., Wang, Y.-C., Shah, H., Kavanagh, D. H., Zharovsky, E., Jacobov, R., Wiseman, J. R., Park, R., Johnson, J. S., Kassim, B. S., Sloofman, L., Mattei, E., Weng, Z., Sieberts, S. K., Peters, M. A., Harris, B. T., Lipska, B. K., Sklar, P., Roussos, P., & Akbarian, S.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Aarhus University (DK)
- University of Massachusetts Chan Medical School (US)
- Sage Bionetworks (US)
- Georgetown University (US)
- National Institute of Mental Health (US)
- James J. Peters VA Medical Center (US)
- Corresponding author
- Hoffman, Gabriel E.
- Roussos, Panos
- Akbarian, Schahram
- ORCID
- Girdhar, Kiran
- Hoffman, Gabriel E.
- Jiang, Yan
- Brown, Leanne
- Hauberg, Mads E.
- Francoeur, Nancy J.
- Wang, Ying-chih
- Shah, Hardik
- Zharovsky, Elizabeth
- Wiseman, Jennifer R.
- Park, Royce
- Johnson, Jessica S.
- Sloofman, Laura
- Mattei, Eugenio
- Weng, Zhiping
- Sieberts, Solveig K.
- Peters, Mette A.
- Harris, Brent T.
- Sklar, Pamela
- Roussos, Panos
- Akbarian, Schahram
- Venue
- Nature Neuroscience
- Published
- 2018-07-23
- Volume
- 21
- Issue
- 8
- Pages
- 1126-1136
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6063773
- OpenAlex
- W2883810206
- Cited by
- 139
- References
- 75
- Citations by year
- 2026: 5 · 2025: 17 · 2024: 13 · 2023: 13 · 2022: 23 · 2021: 24 · 2020: 24 · 2019: 17 · 2018: 3
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01BX002395)
- Wellcome Trust (082604)
- Agence Nationale de la Recherche (ANR-11-LABX-0009)
- Lundbeckfonden (R248‐2017‐2003)
- National Institutes of Health (5r01mh080405-05, 5r01mh094714-04)
- National Institute on Aging (U01AG016976, P50AG005138, U01AG032984, R01AG033193, P01AG002219, R01AG050986, U24AG021886)
- National Heart, Lung, and Blood Institute (R01HL105756)
- National Institute of Mental Health (P50MH084053, R01 MH‐080405, R01MH093725, U01MH103339, R01-MH094714, P50MH066392, R21MH105881, U01MH103365, R01MH109677, R01MH075916, R01MH085542, R37MH057881, R01MH106056, U01MH103340, R21MH102791, R01MH105472, R01MH097276, P50MH106934, U01MH103392, R01MH105898, R21MH103877, U01MH103346)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- schizophrenia, histone modifications, H3K4me3, H3K27ac, dorsolateral prefrontal cortex, anterior cingulate cortex, cell type-specific chromatin, open chromatin, depressive symptoms, neuroticism, PsychENCODE
- MeSH terms
- Alzheimer Disease, Brain Mapping, Chromatin, Depression, Educational Status, Frontal Lobe, Gyrus Cinguli, Histones, Humans, Neurotic Disorders, Risk, Schizophrenia, Genetic Variation, Prefrontal Cortex, Genetic Predisposition to Disease, Epigenesis, Genetic, Genome-Wide Association Study
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