A Whole Methylome CpG-SNP Association Study of Psychosis in Blood and Brain Tissue
Open accessAbstract
Mutated CpG sites (CpG-SNPs) are potential hotspots for human diseases because in addition to the sequence variation they may show individual differences in DNA methylation. We performed methylome-wide association studies (MWAS) to test whether methylation differences at those sites were associated with schizophrenia. We assayed all common CpG-SNPs with methyl-CpG binding domain protein-enriched genome sequencing (MBD-seq) using DNA extracted from 1408 blood samples and 66 postmortem brain samples (BA10) of schizophrenia cases and controls. Seven CpG-SNPs passed our FDR threshold of 0.1 in the blood MWAS. Of the CpG-SNPs methylated in brain, 94% were also methylated in blood. This significantly exceeded the 46.2% overlap expected by chance (P-value < 1.0×10(-8)) and justified replicating findings from blood in brain tissue. CpG-SNP rs3796293 in IL1RAP replicated (P-value = .003) with the same direction of effects. This site was further validated through targeted bisulfite pyrosequencing in 736 independent case-control blood samples (P-value < 9.5×10(-4)). Our top result in the brain MWAS (P-value = 8.8×10(-7)) was CpG-SNP rs16872141 located in the potential promoter of ENC1. Overall, our results suggested that CpG-SNP methylation may reflect effects of environmental insults and can provide biomarkers in blood that could potentially improve disease management.
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It is known that schizophrenia patients have upregulated genes for inflammatory cytokines, and downregulated Bdnf gene transcription.
“It is known that schizophrenia patients have upregulated genes for inflammatory cytokines [122, 123], and downregulated Bdnf gene transcription [124, 125].”
From Brain-Derived Neurotrophic Factor in Brain Disorders: Focus on Neuroinflammation (2019) · cites this paper as [123]
Cites
Principal components analysis corrects for stratification in genome-wide association studies
Price, A. L., Patterson, N. J., Plenge, R. M., Weinblatt, M. E., Shadick, N. A., & Reich, D. (2006) · Nature Genetics · doi:10.1038/ng1847 · Cited by 10,248 · see citing works
Biological insights from 108 schizophrenia-associated genetic loci
Schizophrenia Working Group of the Psychiatric Genomics Consortium (2014) · Nature · doi:10.1038/nature13595 · Cited by 7,577 · see citing works
Self-citationCpG islands and the regulation of transcription
Deaton, A. M., & Bird, A. (2011) · Genes & Development · doi:10.1101/gad.2037511 · Cited by 3,187 · see citing works
DNA methylation arrays as surrogate measures of cell mixture distribution
Houseman, E. A., Accomando, W. P., Koestler, D. C., Christensen, B. C., Marsit, C. J., Nelson, H. H., Wiencke, J. K., & Kelsey, K. T. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-86 · Cited by 3,175 · see citing works
(2013) · The Lancet · doi:10.1016/s0140-6736(12)62129-1 · Cited by 3,010 · see citing works
Conserved role of intragenic DNA methylation in regulating alternative promoters
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., Johnson, B. E., Hong, C., Nielsen, C., Zhao, Y., et al. (2010) · Nature · doi:10.1038/nature09165 · Cited by 1,743 · see citing works
Fast and accurate genotype imputation in genome-wide association studies through pre-phasing
Howie, B., Fuchsberger, C., Stephens, M., Marchini, J., & Abecasis, G. R. (2012) · Nature Genetics · doi:10.1038/ng.2354 · Cited by 1,737 · see citing works
Phenotypic plasticity and the epigenetics of human disease
Feinberg, A. P. (2007) · Nature · doi:10.1038/nature05919 · Cited by 1,613 · see citing works
Genome-wide association analysis identifies 13 new risk loci for schizophrenia
Multicenter Genetic Studies of Schizophrenia Consortium, Ripke, S., Psychosis Endophenotypes International Consortium, Wellcome Trust Case Control Consortium 2, O'Dushlaine, C., Chambert, K., Moran, J. L., Kähler, A. K., Akterin, S., Bergen, S. E., et al. (2013) · Nature Genetics · doi:10.1038/ng.2742 · Cited by 1,496 · see citing works
Self-citationDNA methylation profiling of human chromosomes 6, 20 and 22
Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V. K., Attwood, J., Burger, M., Burton, J. H., Cox, T. V., Davies, R., Down, T. A., et al. (2006) · Nature Genetics · doi:10.1038/ng1909 · Cited by 1,350 · see citing works
Christensen, B. C., Houseman, E. A., Marsit, C. J., Zheng, S., Wrensch, M., Wiemels, J. L., Nelson, H. H., Karagas, M. R., Padbury, J. F., Bueno, R., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000602 · Cited by 1,062 · see citing works
Inflammatory Cytokine Alterations in Schizophrenia: A Systematic Quantitative Review
Potvin, S., Stip, É., Sepehry, A. A., Gendron, A., Bah, R., & Kouassi, É. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.024 · Cited by 989 · see citing works
Liu, Y., Aryee, M. J., Padyukov, L., Fallin, M. D., Hesselberg, E., Rúnarsson, Á. R., Reinius, L. E., Acevedo, N., Taub, M. A., Ronninger, M., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2487 · Cited by 974 · see citing works
CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing
Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., Kashlev, M., Oberdoerffer, P., Sandberg, R., & Oberdoerffer, S. (2011) · Nature · doi:10.1038/nature10442 · Cited by 973 · see citing works
Gardening the genome: DNA methylation in Arabidopsis thaliana
Chan, S. W.-L., Henderson, I. R., & Jacobsen, S. E. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1601 · Cited by 892 · see citing works
5-Methylcytosine in Eukaryotic DNA
Ehrlich, M., & Wang, R. Y. ‐. (1981) · Science · doi:10.1126/science.6262918 · Cited by 745 · see citing works
Harris, R. A., Wang, T., Coarfa, C., Nagarajan, R. P., Hong, C., Downey, S. L., Johnson, B., Fouse, S. D., Delaney, A. D., Zhao, Y., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1682 · Cited by 713 · see citing works
Davies, M. N., Volta, M., Pidsley, R., Lunnon, K., Dixit, A., Lovestone, S., Coarfa, C., Harris, R. A., Milosavljevic, A., Troakes, C., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-6-r43 · Cited by 630 · see citing works
Quantitative comparison of genome-wide DNA methylation mapping technologies
Bock, C., Tomazou, E. M., Brinkman, A. B., Müller, F., Simmer, F., Gu, H., Jäger, N., Gnirke, A., Stunnenberg, H. G., & Meissner, A. (2010) · Nature Biotechnology · doi:10.1038/nbt.1681 · Cited by 587 · see citing works
Methylation-Sensitive Sequence-Specific DNA Binding by the c-Myc Basic Region
Prendergast, G. C., & Ziff, E. B. (1991) · Science · doi:10.1126/science.1987636 · Cited by 565 · see citing works
The Stanley Foundation brain collection and Neuropathology Consortium
Torrey, Ε. F., Webster, M. J., Knable, M. B., Johnston, N., & Yolken, R. H. (2000) · Schizophrenia Research · doi:10.1016/s0920-9964(99)00192-9 · Cited by 533 · see citing works
Maeder, M. L., Angstman, J. F., Richardson, M. E., Linder, S. J., Cascio, V. M., Tsai, S. Q., Ho, Q. V., Sander, J. D., Reyon, D., Bernstein, B., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2726 · Cited by 498 · see citing works
Serre, D., Lee, B. H., & Ting, A. H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp992 · Cited by 404 · see citing works
Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome
Shoemaker, R., Deng, J., Wang, W., & Zhang, K. (2010) · Genome Research · doi:10.1101/gr.104695.109 · Cited by 380 · see citing works
Dependence of transcriptional repression on CpG methylation density
Hsieh, C.-L. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5487-5494.1994 · Cited by 321 · see citing works
Psychoneuroimmunology and the cytokine action in the CNS: Implications for psychiatric disorders
Müller, N., & Ackenheil, M. (1998) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(97)00179-6 · Cited by 304 · see citing works
Dependence of Transcriptional Repression on CpG Methylation Density
Hsieh, C. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5487 · Cited by 300 · see citing works
Cell type–specific DNA methylation at intragenic CpG islands in the immune systemPreprint
Deaton, A. M., Webb, S., Kerr, A. R. W., Illingworth, R. S., Guy, J., Andrews, R., & Bird, A. P. (2011) · Genome Research · doi:10.1101/gr.118703.110 · Cited by 285 · see citing works
Tost, J., Dunker, J., & Gut, I. G. (2003) · BioTechniques · doi:10.2144/03351md02 · Cited by 250 · see citing works
Aberg, K. A., McClay, J. L., Nerella, S., Clark, S., Kumar, G., Chen, W., Khachane, A. N., Xie, L., Hudson, A., Gao, G., et al. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.3730 · Cited by 248 · see citing works
Self-citationEvaluation of diagnostic procedures in Swedish patients with schizophrenia and related psychoses
Ekholm, B., Ekholm, A., Adolfsson, R., Vares, M., Ösby, U., Sedvall, G. C., & Jönsson, E. G. (2005) · Nordic Journal of Psychiatry · doi:10.1080/08039480500360906 · Cited by 242 · see citing works
Methylated DNA Immunoprecipitation (MeDIP)
Mohn, F., Weber, M., Schübeler, D., & Roloff, T. C. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-522-0_5 · Cited by 239 · see citing works
Bergen, S. E., O'Dushlaine, C. T., Ripke, S., Lee, P. H., Ruderfer, D. M., Akterin, S., Moran, J. L., Chambert, K. D., Handsaker, R. E., Backlund, L., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.73 · Cited by 239 · see citing works
Self-citationEllman, L. M., Deicken, R. F., Vinogradov, S., Kremen, W. S., Poole, J. H., Kern, D. M., Tsai, W. Y., Schaefer, C. A., & Brown, A. S. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.05.014 · Cited by 225 · see citing works
Nair, S. S., Coolen, M. W., Stirzaker, C., Song, J. Z., Statham, A. L., Strbenac, D., Robinson, M. D., & Clark, S. J. (2011) · Epigenetics · doi:10.4161/epi.6.1.13313 · Cited by 210 · see citing works
Self-citationFineberg, A. M., & Ellman, L. M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.001 · Cited by 201 · see citing works
Dayeh, T. A., Olsson, A. H., Volkov, P., Almgren, P., Rönn, T., & Ling, C. (2013) · Diabetologia · doi:10.1007/s00125-012-2815-7 · Cited by 199 · see citing works
Young cases of schizophrenia identified in a national inpatient register
Dalman, C., Broms, J., Cullberg, J., & Allebeck, P. (2002) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s00127-002-0582-3 · Cited by 192 · see citing works
Whole genome DNA methylation analysis based on high throughput sequencing technology
Li, N., Ye, M., Li, Y., Yan, Z., Butcher, L. M., Sun, J., Han, X., Chen, Q., zhang, X., & Wang, J. (2010) · Methods · doi:10.1016/j.ymeth.2010.04.009 · Cited by 191 · see citing works
Cytokine and growth factor involvement in schizophrenia—support for the developmental model
Nawa, H., Takahashi, M., & Patterson, P. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000730 · Cited by 189 · see citing works
Oxidative stress and schizophrenia
Emiliani, F. E., Sedlak, T. W., & Sawa, A. (2014) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000054 · Cited by 168 · see citing works
Induced DNA demethylation by targeting Ten-Eleven Translocation 2 to the human ICAM-1 promoter
Chen, H., Kazemier, H. G., de Groote, M. L., Ruiters, M. H. J., Xu, G., & Rots, M. G. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1019 · Cited by 164 · see citing works
Structural insights into the assembly and activation of IL-1β with its receptors
Wang, D., Zhang, S., Li, L., Liu, X., Mei, K., & Wang, X. (2010) · Nature Immunology · doi:10.1038/ni.1925 · Cited by 162 · see citing works
McClay, J. L., Åberg, K. A., Clark, S. L., Nerella, S., Kumar, G., Xie, L. Y., Hudson, A. D., Harada, A., Hultman, C. M., Magnusson, P. K. E., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt511 · Cited by 162 · see citing works
Self-citationSahin, E., Haubenwallner, S., Kuttke, M., Kollmann, I., Halfmann, A., Dohnal, A. M., Chen, L., Cheng, P. P., Hoesel, B., Einwallner, E., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302167 · Cited by 155 · see citing works
False discoveries and models for gene discovery
van den Oord, E. J. C. G., & Sullivan, P. F. (2003) · Trends in Genetics · doi:10.1016/j.tig.2003.08.003 · Cited by 149 · see citing works
Smith, D. E., Lipsky, B. P., Russell, C. B., Ketchem, R. R., Kirchner, J., Hensley, K. M., Huang, Y., Friedman, W., Boissonneault, V., Plante, M.-M., et al. (2009) · Immunity · doi:10.1016/j.immuni.2009.03.020 · Cited by 135 · see citing works
Taqi, M. M., Bazov, I., Watanabe, H., Sheedy, D. L., Harper, C. G., Alkass, K., Druid, H., Wentzel, P., Nyberg, F., Yakovleva, T., et al. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00323.x · Cited by 132 · see citing works
Nrf2 Regulates Neurogenesis and Protects Neural Progenitor Cells Against Aβ Toxicity
Kärkkäinen, V., Pomeshchik, Y., Savchenko, E., Dhungana, H., Kurronen, A., Lehtonen, Š., Naumenko, N. V., Tavi, P., Levonen, A., Yamamoto, M. P., et al. (2014) · Stem Cells · doi:10.1002/stem.1666 · Cited by 128 · see citing works
Akiyama, K. (1999) · Schizophrenia Research · doi:10.1016/s0920-9964(98)00140-6 · Cited by 109 · see citing works
Katila, H., Appelberg, B., Hurme, M., & Rimón, R. (1994) · Schizophrenia Research · doi:10.1016/0920-9964(94)90081-7 · Cited by 109 · see citing works
Hogart, A., Lichtenberg, J., Ajay, S. S., Anderson, S., NIH Intramural Sequencing Center, Margulies, E. H., & Bodine, D. M. (2012) · Genome Research · doi:10.1101/gr.132878.111 · Cited by 101 · see citing works
RECOGNITION AND SILENCING OF REPEATED DNA
Hsieh, J., & Fire, A. Z. (2000) · Annual Review of Genetics · doi:10.1146/annurev.genet.34.1.187 · Cited by 97 · see citing works
Aberg, K. A., McClay, J. L., Nerella, S., Xie, L. Y., Clark, S. L., Hudson, A. D., Bukszár, J., Adkins, D., Swedish Schizophrenia Consortium, Hultman, C. M., et al. (2012) · Epigenomics · doi:10.2217/epi.12.59 · Cited by 93 · see citing works
Self-citationGenome-wide expression profiling of schizophrenia using a large combined cohort
Mistry, M., Gillis, J. A., & Pavlidis, P. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.172 · Cited by 92 · see citing works
Kristjansson, E., Allebeck, P., & Wistedt, B. (1987) · Nordic Journal of Psychiatry · doi:10.3109/08039488709103182 · Cited by 80 · see citing works
High Resolution Detection and Analysis of CpG Dinucleotides Methylation Using MBD-Seq Technology
Lan, X., Adams, C., Landers, M. A., Dudas, M., Krissinger, D., Marnellos, G., Bonneville, R., Xu, M., Wang, J., Huang, T. H. ‐., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022226 · Cited by 79 · see citing works
Tohmi, M., Tsuda, N., Watanabe, Y., Kakita, A., & Nawa, H. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.05.010 · Cited by 78 · see citing works
Preventing transcriptional gene silencing by active DNA demethylation
Kapoor, A., Agius, F., & Zhu, J. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.08.039 · Cited by 75 · see citing works
Sun, Y. V., Turner, S. T., Smith, J. A., HAMMOND, P. I., Zagel, A. L., Rostyne, J. L. V. D., Cunningham, J. M., & Kardia, S. L. R. (2010) · Human Genetics · doi:10.1007/s00439-010-0810-y · Cited by 65 · see citing works
Whole-genome association mapping of gene expression in the human prefrontal cortex
Liu, C., Cheng, L., Badner, J. A., Zhang, D., Craig, D. W., Redman, M., & Gershon, E. S. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.128 · Cited by 63 · see citing works
Aparicio, A. M., North, B., Barske, L. A., Wang, X., Bollati, V., Weisenberger, D. J., Yoo, C. B., Tannir, N. M., Horne, E., Groshen, S. G., et al. (2009) · Epigenetics · doi:10.4161/epi.4.3.8694 · Cited by 58 · see citing works
The Dinucleotide CG as a Genomic Signalling Module
Bird, A. P. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.01.056 · Cited by 58 · see citing works
Evaluation of Methyl-Binding Domain Based Enrichment Approaches Revisited
Åberg, K. A., Xie, L., Chan, R. F., Zhao, M., Pandey, A. K., Kumar, G., Clark, S. L., & van den Oord, E. J. C. G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132205 · Cited by 28 · see citing works
Self-citationVoigt, P., & Reinberg, D. (2013) · Nature Biotechnology · doi:10.1038/nbt.2756 · Cited by 27 · see citing works
Estimation of CpG coverage in whole methylome next-generation sequencing studies
van den Oord, E. J. C. G., Bukszár, J., Rudolf, G., Nerella, S., McClay, J. L., Xie, L. Y., & Åberg, K. A. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-50 · Cited by 26 · see citing works
Self-citationGenomeRunner: automating genome exploration
Dozmorov, M. G., Cara, L. R., Giles, C. B., & Wren, J. D. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr666 · Cited by 24 · see citing works
Self-citationEvaluation of tissue collection for postmortem studies of bipolar disorder
Deep‐Soboslay, A., Iglesias, B., Hyde, T. M., Bigelow, L. B., Imamovic, V., Herman, M. M., & Kleinman, J. E. (2008) · Bipolar Disorders · doi:10.1111/j.1399-5618.2008.00607.x · Cited by 22 · see citing works
MethylPCA: a toolkit to control for confounders in methylome-wide association studies
Chen, W., Gao, G., Nerella, S., Hultman, C. M., Magnusson, P. K. E., Sullivan, P. F., Åberg, K. A., & van den Oord, E. J. C. G. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-74 · Cited by 18 · see citing works
Self-citationSynergistic activation of the human choline acetyltransferase gene by c-Myb and C/EBPβ
Robert, I., Sutter, A., & Quirin‐Stricker, C. (2002) · Molecular Brain Research · doi:10.1016/s0169-328x(02)00419-9 · Cited by 14 · see citing works
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Richetto, J., & Meyer, U. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.03.008 · Cited by 183 · see citing works
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Watkeys, O. J., Cohen‐Woods, S., Quidé, Y., Cairns, M. J., Overs, B. J., Fullerton, J. M., & Green, M. J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109925 · Cited by 16 · see citing works
Early Detection and Prevention of Schizophrenic Psychosis—A Review
Westhoff, M. S., Ladwig, J., Heck, J., Schülke, R., Groh, A., Deest, M., Bleich, S., Frieling, H., & Jahn, K. (2021) · Brain Sciences · doi:10.3390/brainsci12010011 · Cited by 14 · see citing works
DNA Methylation in Animal Models of Psychosis
Grayson, D. R., & Guidotti, A. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.12.012 · Cited by 11 · see citing works
Nie, F., Zhang, M.-R., Shang, S.-S., Zhang, Q.-X., Zhang, R., Chen, P., & Ma, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110081 · Cited by 11 · see citing works
Le, A. T. P., Higuchi, Y., Sumiyoshi, T., Itoh, H., Sasabayashi, D., Takahashi, T., & Suzuki, M. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1188452 · Cited by 9 · see citing works
Epigenetic studies of schizophrenia: current status and future directions
Migdalska‐Richards, A., & Mill, J. S. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.12.003 · Cited by 9 · see citing works
DNA Methylation Differences in Cortical Grey and White Matter in Schizophrenia
van Berlekom, A. B., Notman, N., Sneeboer, M. A. M., Snijders, G. J. L., Houtepen, L. C., Nispeling, D. M., He, Y., Dracheva, S. M., Hol, E. M., Kahn, R. S., et al. (2021) · Epigenomics · doi:10.2217/epi-2021-0077 · Cited by 9 · see citing works
Kohshour, M. O., Kannaiyan, N. R., Falk, A. J., Papiol, S., Heilbronner, U., Budde, M., Kalman, J. L., Schulte, E. C., Rietschel, M., Witt, S. H., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02228-x · Cited by 8 · see citing works
Алфимова, М. В., Kondratyev, N. V., Golov, A. K., & Голимбет, В. Е. (2020) · Scientific Reports · doi:10.1038/s41598-020-61671-2 · Cited by 6 · see citing works
Cheng, P., Zhang, R., Shan, S., Yuan, B., Chen, J., Qiu, Z., & Du, Y. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136533 · Cited by 6 · see citing works
Genetics of Epigenome Might Hold the Clue for Determining the Threshold of Environmental Impact
Banerjee, M. (2019) · Epigenomics · doi:10.2217/epi-2019-0123 · Cited by 5 · see citing works
Kim, S., Shin, J. J., Kang, M., Yang, Y., Cho, Y. S., Paik, H., Kim, J., Yi, Y., Lee, S., Koo, H. Y., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59685-3 · Cited by 4 · see citing works
Aftabı, Y., Khoshkam, Z., Amiri‐Sadeghan, A., Khalili, Y., & Ichihara, G. (2020) · Meta Gene · doi:10.1016/j.mgene.2020.100805 · Cited by 4 · see citing works
Epigenetic Control in Schizophrenia
D’Addario, C., & Bartolomeo, M. D. (2025) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-75980-2_5 · Cited by 3 · see citing works
Different Methylation of CpG-SNPs in Behcet’s Disease
Huang, Y., Tan, H., Cao, Q., Yuan, G., Su, G., & Yang, P. (2019) · BioMed Research International · doi:10.1155/2019/3489305 · Cited by 3 · see citing works
Kondratyev, N. V., Алфимова, М. В., & Голимбет, В. Е. (2017) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro20171178172-75 · Cited by 3 · see citing works
Алфимова, М. В., Kondratyev, N. V., Коровайцева, Г. И., Lezheiko, T., Plakunova, V., Габаева, М. В., & Голимбет, В. Е. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012629 · Cited by 2 · see citing works
Sharafshah, A., Blum, K., Lewandrowski, K., Elman, I., Fuehrlein, B. S., Baron, D., Pinhasov, A., Thanos, P. K., Fiorelli, R., Schmidt, S., et al. (2025) · Journal of Personalized Medicine · doi:10.3390/jpm15120579
The biology of schizophrenia as a neurodevelopmental disorder
van Berlekom, A. B. (2022) · doi:10.33540/1269 · Cited by 1 · see citing works
Melka, M. G., Castellani, C. A., & Singh, S. M. (2016) · InTech eBooks · doi:10.5772/65905
Kumar, G., Krishnasamy, K., Pasha, N., Naveenkumar, N., Mam, B., Kishinani, M., Vohra, V., Jain, R., & Morawala‐Patell, V. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.22.423778
Self-citationАлфимова, М. В., Kondratyev, N. V., Golov, A. K., Каледа, В. Г., Abramova, L. I., & Голимбет, В. Е. (2021) · Russian Journal of Genetics · doi:10.1134/s1022795421080019
Brain Derived Neurotrophic Factor (BDNF) Gene in Peripheral Blood Cells of Stable Schizophrenia
Zaifah, A. P. D. N. K., Tokhi, E., Rahim, N. E. H. A., Talib, N. A., & Noor, H. M. (2022) · IIUM Medical Journal Malaysia · doi:10.31436/imjm.v21i1.1840
Ran, M., Jin, M., Wang, Z., Zhang, H., Tao, Y., Xu, H., Zou, S., Deng, F., Zhang, H., Tang, X., et al. (2025) · Epigenetics · doi:10.1080/15592294.2025.2560339
Impacts of Polyenvironmental Factors on DNA Methylation in Patients With Psychosis
Rami, F., Kang, C., Li, L., Le, T.-H., Kim, S.-W., Won, S., Setiani, A., Yoon, B.-H., & Chung, Y.-C. (2025) · Schizophrenia Bulletin Open · doi:10.1093/schizbullopen/sgaf027
Li, C., Chen, Y., Yao, Y., & Shang, Y. (2026) · Current Medicinal Chemistry · doi:10.2174/0109298673377176251207133923
- Authors
- van den Oord, E. J. C. G., Clark, S. L., Xie, L. Y., Shabalin, A. A., Dozmorov, M. G., Kumar, G., Swedish Schizophrenia Consortium, Vladimirov, V. I., Magnusson, P. K. E., & Aberg, K. A.
- Affiliations
- Virginia Commonwealth University (US)
- Johns Hopkins University (US)
- Karolinska Institutet (SE)
- ORCID
- Venue
- Schizophrenia Bulletin
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-12-09
- Volume
- 42
- Issue
- 4
- Pages
- 1018-1026
- ISSN
- 0586-7614 (ISSN-L)
- 1745-1701
- PMC
- PMC4903046
- OpenAlex
- W2283549005
- Cited by
- 47
- References
- 69
- Citations by year
- 2026: 1 · 2025: 5 · 2023: 1 · 2022: 6 · 2021: 5 · 2020: 10 · 2019: 4 · 2018: 8 · 2017: 3 · 2016: 4
- FWCI
- 2.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Schizophrenia Bulletin (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Stanley Medical Research Institute
- Translational Genomics Research Institute
- National Institute on Alcohol Abuse and Alcoholism (K01AA021266)
- National Institute of Mental Health (R03MH102723, R01MH097283, RC2MH089996)
- 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
- MeSH terms
- Adult, Aged, Autopsy, Brain, Female, Humans, Male, Microfilament Proteins, Middle Aged, Neuropeptides, Nuclear Proteins, Psychotic Disorders, Schizophrenia, Biomarkers, Case-Control Studies, CpG Islands, DNA Methylation, Polymorphism, Single Nucleotide, Genome-Wide Association Study
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