Cited by 106Epigenetics and DNA MethylationSchizophrenia research and treatmentGenetic Associations and Epidemiology

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Schizophrenia-associated methylomic variation: molecular signatures of disease and polygenic risk burden across multiple brain regions

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Viana, Joana, Hannon, Eilis, Dempster, Emma, Pidsley, Ruth, Macdonald, Ruby, Knox, Olivia, Spiers, Helen, Troakes, Claire, Al-Saraj, Safa, Turecki, Gustavo, Schalkwyk, Leonard C, Mill, Jonathan·2016·Human Molecular Genetics

DOI 10.1093/hmg/ddw373PMC PMC5351932

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Abstract

Genetic association studies provide evidence for a substantial polygenic component to schizophrenia, although the neurobiological mechanisms underlying the disorder remain largely undefined. Building on recent studies supporting a role for developmentally regulated epigenetic variation in the molecular aetiology of schizophrenia, this study aimed to identify epigenetic variation associated with both a diagnosis of schizophrenia and elevated polygenic risk burden for the disease across multiple brain regions. Genome-wide DNA methylation was quantified in 262 post-mortem brain samples, representing tissue from four brain regions (prefrontal cortex, striatum, hippocampus and cerebellum) from 41 schizophrenia patients and 47 controls. We identified multiple disease-associated and polygenic risk score-associated differentially methylated positions and regions, which are not enriched in genomic regions identified in genetic studies of schizophrenia and do not reflect direct genetic effects on DNA methylation. Our study represents the first analysis of epigenetic variation associated with schizophrenia across multiple brain regions and highlights the utility of polygenic risk scores for identifying molecular pathways associated with aetiological variation in complex disease.

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Figure 1. Forest plots showing the top-ranked schizophrenia-associated differentially methylated positions (DMPs). Shown are data for 12 DMPs associated with schizophrenia at a highly stringent significance threshold (P < 1.66E-07) derived using permutations to estimate the nominal P-value for 5% family-wise error. Additional information on these DMPs is given in Table 2. Colour depicts a brain region in which the schizophrenia-association was identified: prefrontal cortex = blue, striatum = green, hippocampus = red, and cerebellum = yellow.CC BY · PubMed Central

Figure 2. Differentially methylated regions (DMRs) associated with schizophrenia. Shown in chromosomal order are DMRs (Šidák-corrected P < 0.05, number of probes ≥ 2) associated with schizophrenia identified in any of the four tissues. Effect sizes for individual probes within each DMR are also shown for the other three brain regions (blue = hypomethylation, red = hypermethylation). Further details for individual DMRs are provided in Table 3.CC BY · PubMed Central

Figure 3. Increased polygenic burden for schizophrenia is associated with altered DNA methylation. (A) Schizophrenia samples included in our study scored significantly higher on a polygenic risk score derived from a recent large collaborative GWAS of schizophrenia. (B) The top-ranked PRS-associated DMP was cg20640266 (annotated to ZNF618) in the cerebellum. (C) The top-ranked multi-region PRS-associated DMP was cg04910228 (annotated to the TSNAX-DISC1 locus).CC BY · PubMed Central

Figure 4. Differentially methylated regions (DMRs) associated with schizophrenia polygenic risk score (PRS). Shown in chromosomal order are DMRs (Šidák-corrected P < 0.05, number of probes ≥2) associated with schizophrenia PRS identified in any of the four brain regions. Effect sizes for individual probes within each DMR are also shown for the other three brain regions (blue = hypomethylation, red = hypermethylation). Further details for individual DMRs are provided in Table 5.CC BY · PubMed Central

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Authors: Viana, J., Hannon, E., Dempster, E., Pidsley, R., Macdonald, R., Knox, O., Spiers, H., Troakes, C., Al-Saraj, S., Turecki, G., Schalkwyk, L. C., & Mill, J.
Affiliations: University of Exeter (GB)
Garvan Institute of Medical Research (AU)
King's College London (GB)
McGill University (CA)
University of Essex (GB)
Corresponding author: Mill, Jonathan
ORCID: Viana, Joana
Hannon, Eilis
Dempster, Emma
Pidsley, Ruth
Spiers, Helen
Troakes, Claire
Turecki, Gustavo
Schalkwyk, Leonard C
Mill, Jonathan
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2016-12-22
Volume: 26
Issue: 1
Pages: ddw373
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddw373
PMC: PMC5351932
OpenAlex: W2563293289
Cited by: 105
References: 67
Citations by year: 2025: 6 · 2024: 14 · 2023: 6 · 2022: 10 · 2021: 19 · 2020: 14 · 2019: 16 · 2018: 11 · 2017: 9
FWCI: 6.23
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: Human Molecular Genetics (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Open Research Exeter (University of Exeter) (publishedVersion, cc-by)
Open Access at Essex (University of Essex) (acceptedVersion)
Figshare (submittedVersion)
Royal Devon and Exeter Research Repository (Royal Devon and Exeter) (submittedVersion)
Funders: Research Councils UK (MR/K013807/1)
National Institutes of Health
Medical Research Council (MR/L016397/1, MR/K013807/1, K013807)
National Institute on Aging (R01AG036039)
H2020 European Research Council
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Keywords: schizophrenia, DNA methylation, epigenetics, polygenic risk score, differentially methylated regions, postmortem brain, prefrontal cortex, striatum, hippocampus, cerebellum, complex disease genetics
MeSH terms: Adult, Brain, Cadaver, Cerebellum, Corpus Striatum, Female, Hippocampus, Humans, Male, Middle Aged, Risk Factors, Schizophrenia, Biomarkers, Case-Control Studies, Prefrontal Cortex, DNA Methylation, Multifactorial Inheritance, Epigenesis, Genetic

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Schizophrenia-associated methylomic variation: molecular signatures of disease and polygenic risk burden across multiple brain regions

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