Global hypomethylation of peripheral leukocyte DNA in male patients with schizophrenia: A potential link between epigenetics and schizophrenia
Abstract
Genetic and epigenetic factors can potentially alter susceptibility to psychiatric disorders such as schizophrenia. In order to explore the effect of epigenetics on the pathogenesis of schizophrenia, we examined the global methylation level of leukocyte DNA from 210 patients with schizophrenia (124 males and 86 females) and 237 healthy subjects (108 males and 129 females). Methylated deoxycytidine (mC) content in peripheral leukocyte DNA was measured by high performance liquid chromatography (HPLC). We confirmed in the healthy subjects our previous finding that there are sex-dependent differences in mC content (males>females; beta=0.319, p<0.001), in addition to the effect of age (beta=-0.141, p=0.022). We therefore used multiple regression to analyze the data from all subjects by sex, with age as a co-variant. In males, a tendency was observed toward lower mC content in patients than in controls (beta=-0.115, p=0.075), with a significant effect of age (beta=-0.212, p<0.001). This difference was more prominent in younger individuals. In females, no effect of age or disease status on mC content was observed. These results established that there is significant sex-dependent difference in the mC content of human peripheral leukocyte DNA, and raise the possibility that alterations in DNA methylation state are present in patients with schizophrenia.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In both human and animal models, treatment with haloperidol induces sex-specific DNA methylation differences.
“In both human and animal models, it has been observed treatment with haloperidol induces sex-specific DNA methylation differences [71, 72].”
From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [72]
Cites
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Epigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602 · see citing works
Cancer-epigenetics comes of age
Jones, P. A., & Laird, P. W. (1999) · Nature Genetics · doi:10.1038/5947 · Cited by 2,334 · see citing works
Cytosine methylation and the ecology of intragenomic parasites
Yoder, J. A., Walsh, C. P., & Bestor, T. H. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01181-5 · Cited by 1,941 · see citing works
Epigenetic inheritance at the agouti locus in the mouse
Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K., & Whitelaw, E. (1999) · Nature Genetics · doi:10.1038/15490 · Cited by 1,476 · see citing works
Transcription of IAP endogenous retroviruses is constrained by cytosine methylation
Walsh, C. P., Chaillet, J. R., & Bestor, T. H. (1998) · Nature Genetics · doi:10.1038/2413 · Cited by 1,105 · see citing works
DNA methylation in health and disease
Robertson, K. D., & Wolffe, A. P. (2000) · Nature Reviews Genetics · doi:10.1038/35049533 · Cited by 1,056 · see citing works
A decrease of reelin expression as a putative vulnerability factor in schizophrenia
Impagnatiello, F., Guidotti, A. R., Pesold, C., Dwivedi, Y., Caruncho, H. J., Pisu, M. G., Uzunov, D. P., Smalheiser, N. R., Davis, J. M., Pandey, G. N., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15718 · Cited by 753 · see citing works
DNA Methylation Decreases in Aging But Not in Immortal Cells
Wilson, V. L., & Jones, P. A. (1983) · Science · doi:10.1126/science.6844925 · Cited by 649 · see citing works
Genomic 5-methyldeoxycytidine decreases with age.
Wilson, V. L., Smith, R. A., Ma, S., & Cutler, R. G. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61057-9 · Cited by 521 · see citing works
Metastable epialleles in mammals
Rakyan, V. K., Blewitt, M. E., Druker, R., Preis, J. I., & Whitelaw, E. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02709-9 · Cited by 499 · see citing works
Gibbons, R. J., McDowell, T. L., Raman, S., O’Rourke, D., Garrick, D., Ayyub, H., & Higgs, D. R. (2000) · Nature Genetics · doi:10.1038/74191 · Cited by 495 · see citing works
Fuke, C., Shimabukuro, M., Petronis, A., Sugimoto, J., Oda, T., Miura, K., Miyazaki, T., Ogura, C., Okazaki, Y., & Jinno, Y. (2004) · Annals of Human Genetics · doi:10.1046/j.1529-8817.2004.00081.x · Cited by 399 · see citing works
Self-citationTremolizzo, L., Carboni, G., Ruzicka, W. B., Mitchell, C. P., Sugaya, I., Tueting, P. A., Sharma, R. P., Grayson, D. R., Costa, E., & Guidotti, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.262658999 · Cited by 381 · see citing works
Szymanski, S., Lieberman, J. A., Alvir, J. M., Mayerhoff, D. I., Loebel, A., Geisler, S., Chakos, M., Koreen, A., Jody, D. N., & Kane, J. M. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.5.698 · Cited by 319 · see citing works
Epigenetic inheritance in the mouse
Römer, I., Reik, W., Dean, W., & Klose, J. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00124-2 · Cited by 248 · see citing works
The origin of schizophrenia: genetic thesis, epigenetic antithesis, and resolving synthesis
Petronis, A. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.02.005 · Cited by 225 · see citing works
Rett Syndrome and MeCP2: Linking Epigenetics and Neuronal Function
Shahbazian, M. D., & Zoghbi, H. Y. (2002) · The American Journal of Human Genetics · doi:10.1086/345360 · Cited by 201 · see citing works
Genetics of Schizophrenia and the New Millennium: Progress and Pitfalls
Baron, M. (2001) · The American Journal of Human Genetics · doi:10.1086/318212 · Cited by 184 · see citing works
Reynolds, E. H., Carney, M. W. P., & Toone, B. (1984) · The Lancet · doi:10.1016/s0140-6736(84)90482-3 · Cited by 158 · see citing works
Epigenomics: Mapping the Methylome
Wilson, I. M., Davies, J. J., Weber, M., Brown, C. J., Alvarez, C. E., MacAulay, C. E., Schübeler, D., & Lam, W. L. (2005) · Cell Cycle · doi:10.4161/cc.5.2.2367 · Cited by 122 · see citing works
Rao, M. L., & Kölsch, H. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00126-9 · Cited by 121 · see citing works
Dynamics of DNA methylation pattern
Hsieh, C. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00064-2 · Cited by 99 · see citing works
Huber, T. J., Tettenborn, C., Leifke, E., & Emrich, H. M. (2004) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.05.010 · Cited by 91 · see citing works
Quantitative changes in T cell DNA methylation occur during differentiation and ageing
Golbus, J., Palella, T. D., & Richardson, B. C. (1990) · European Journal of Immunology · doi:10.1002/eji.1830200836 · Cited by 91 · see citing works
Psychotic disorders and gonadal function: evidence supporting the oestrogen hypothesis
Huber, T. J., Borsutzky, M., Schneider, U., & Emrich, H. M. (2004) · Acta Psychiatrica Scandinavica · doi:10.1046/j.1600-0447.2003.00251.x · Cited by 86 · see citing works
Psychiatric genetics: back to the future
Owen, M. J., Cardno, A. G., & O’Donovan, M. C. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000702 · Cited by 81 · see citing works
MATERNAL NUTRITION AND LOW BIRTH-WEIGHT
Susser, M. W., & STEIN, Z. A. (1976) · The Lancet · doi:10.1016/s0140-6736(76)91302-7 · Cited by 79 · see citing works
Drinkwater, R. D., Blake, T. J. A., Morley, A. A., & Turner, D. R. (1989) · Mutation Research/DNAging · doi:10.1016/0921-8734(89)90038-6 · Cited by 78 · see citing works
Reactivation of heritably silenced gene expression in mice
Sutherland, H. G. E., Kearns, M., Morgan, H. D., Headley, A. P., Morris, C., Martin, D. I. K., & Whitelaw, E. (2000) · Mammalian Genome · doi:10.1007/s003350010066 · Cited by 73 · see citing works
Gogos, A., & van den Buuse, M. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.061432 · Cited by 71 · see citing works
Genomic Discordance Between Monozygotic Twins Discordant for Schizophrenia
Tsujita, T., Niikawa, N., Yamashita, H., Imamura, A., Hamada, A., Nakane, Y., & Okazaki, Y. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.3.422 · Cited by 63 · see citing works
Self-citationHomocysteinemia and schizophrenia as a case of methylation deficiency
Regland, B., Johansson, B. V., & Gottfries, C. G. (1994) · Journal of Neural Transmission · doi:10.1007/bf01277017 · Cited by 54 · see citing works
Molecular genetic studies of schizophrenia: challenges and insights
Kato, C., Petronis, A., Okazaki, Y., Tochigi, M., Umekage, T., & Sasaki, T. (2002) · Neuroscience Research · doi:10.1016/s0168-0102(02)00064-0 · Cited by 38 · see citing works
Self-citationSmythies, J., Alarcón, R. D., Morere, D. A., Monti, J. A., Steele, M., Tolbert, L. C., & Walter-Ryan, W. G. (1986) · Biological Psychiatry · doi:10.1016/0006-3223(86)90330-6 · Cited by 35 · see citing works
Kelsoe, J. R., Tolbert, L. C., Crews, E. L., & Smythies, J. (1982) · Journal of Neuroscience Research · doi:10.1002/jnr.490080113 · Cited by 30 · see citing works
Human endogenous retroviruses with transcriptional potential in the brain
Nakamura, A., Okazaki, Y., Sugimoto, J., Oda, T., & Jinno, Y. (2003) · Journal of Human Genetics · doi:10.1007/s10038-003-0081-8 · Cited by 28 · see citing works
Self-citationShen, H., Nakamura, A. M., Sugimoto, J., Sakumoto, N., Oda, T., Jinno, Y., & Okazaki, Y. (2006) · Journal of Human Genetics · doi:10.1007/s10038-006-0382-9 · Cited by 15 · see citing works
Self-citationMedication Effects on One-Carbon Metabolism in
Morere, D. A., Alarcón, R. D., Monti, J. A., Walter-Ryan, W. G., Bancroft, A. A., Smythies, J., & Tolbert, L. C. (1986) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-198606000-00006 · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 40 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Environmental chemical exposures and human epigenetics
Hou, L., Zhang, X., Wang, D., & Baccarelli, A. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr154 · Cited by 489 · see citing works
DNA methylation in white blood cells
Terry, M. B., Delgado‐Cruzata, L., Vin‐Raviv, N., Wu, H. C., & Santella, R. M. (2011) · Epigenetics · doi:10.4161/epi.6.7.16500 · Cited by 318 · see citing works
El‐Maarri, O., Becker, T., Junen, J., Manzoor, S. S., Diaz-Lacava, A. N., Schwaab, R., Wienker, T. F., & Oldenburg, J. (2007) · Human Genetics · doi:10.1007/s00439-007-0430-3 · Cited by 271 · see citing works
Unternaehrer, E., Luers, P., Mill, J., Dempster, E., Meyer, A. H., Staehli, S., Lieb, R., Hellhammer, D. H., & Meinlschmidt, G. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.77 · Cited by 250 · see citing works
DNA hypomethylation in the origin and pathogenesis of human diseases
Pogribny, I., & Beland, F. A. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0015-5 · Cited by 227 · see citing works
Epigenetics and atherosclerosis
Turunen, M. P., Aavik, E., & Ylä‐Herttuala, S. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.02.008 · Cited by 218 · see citing works
Predictors of global methylation levels in blood DNA of healthy subjects: a combined analysis
Zhu, Z.-Z., Hou, L., Bollati, V., Tarantini, L., Marinelli, B., Cantone, L., Yang, A. S., Vokonas, P., Lissowska, J., Fustinoni, S., et al. (2010) · International Journal of Epidemiology · doi:10.1093/ije/dyq154 · Cited by 218 · see citing works
Melas, P. A., Rogdaki, M., Ösby, U., Schalling, M., Lavebratt, C., & Ekström, T. J. (2012) · The FASEB Journal · doi:10.1096/fj.11-202069 · Cited by 186 · see citing works
DNA methylation: conducting the orchestra from exposure to phenotype?
Leenen, F. A. D., Muller, C. P., & Turner, J. D. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0256-8 · Cited by 186 · see citing works
Smigielski, L., Jagannath, V., Rössler, W., Walitza, S., & Grünblatt, E. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0601-3 · Cited by 168 · see citing works
Biomarkers in schizophrenia: A focus on blood based diagnostics and theranostics
Lai, C.-Y., Scarr, E., Udawela, M., Everall, I., Chen, W. J., & Dean, B. (2016) · World Journal of Psychiatry · doi:10.5498/wjp.v6.i1.102 · Cited by 153 · see citing works
Carter, C. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn054 · Cited by 137 · see citing works
Methylation Patterns in Whole Blood Correlate With Symptoms in Schizophrenia Patients
Liu, J., Chen, J., Ehrlich, S., Walton, E., White, T. J. H., Perrone‐Bizzozero, N. I., Bustillo, J., Turner, J. A., & Calhoun, V. D. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbt080 · Cited by 134 · see citing works
Epigenetics in polycystic ovary syndrome: a pilot study of global DNA methylation
Xu, N., Azziz, R., & Goodarzi, M. O. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.10.020 · Cited by 121 · see citing works
Nishioka, M., Bundo, M., Koike, S., Takizawa, R., Kakiuchi, C., Araki, T., Kasai, K., & Iwamoto, K. (2013) · Journal of Human Genetics · doi:10.1038/jhg.2012.140 · Cited by 101 · see citing works
Brown, J. S. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm147 · Cited by 100 · see citing works
Rusiecki, J. A., Byrne, C., Galdzicki, Z., Srikantan, V., Chen, L., Poulin, M., Yan, L., & Baccarelli, A. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00056 · Cited by 99 · see citing works
Global DNA methylation in old subjects is correlated with frailty
Bellizzi, D., D'Aquila, P., Montesanto, A., Corsonello, A., Mari, V., Mazzei, B., Lattanzio, F., & Passarino, G. (2012) · AGE · doi:10.1007/s11357-011-9216-6 · Cited by 97 · see citing works
NMDA receptor hypofunction for schizophrenia revisited: Perspectives from epigenetic mechanisms
Snyder, M. A., & Gao, W. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.03.010 · Cited by 93 · see citing works
DNA methylation in schizophrenia: progress and challenges of epigenetic studies
Nishioka, M., Bundo, M., Kasai, K., & Iwamoto, K. (2012) · Genome Medicine · doi:10.1186/gm397 · Cited by 90 · see citing works
DNA methylation in peripheral tissue of schizophrenia and bipolar disorder: a systematic review
Teroganova, N., Girshkin, L., Suter, C. M., & Green, M. J. (2016) · BMC Genetics · doi:10.1186/s12863-016-0332-2 · Cited by 86 · see citing works
One-carbon metabolism and schizophrenia: current challenges and future directions
Krebs, M., Bellon, A., Mainguy, G., Jay, T. M., & Frieling, H. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.10.001 · Cited by 87 · see citing works
DNA Methylation and Psychiatric Disorders
Liu, C., Jiao, C., Wang, K., & Yuan, N. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.006 · Cited by 85 · see citing works
Hayashi‐Takagi, A., Vawter, M. P., & Iwamoto, K. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.09.035 · Cited by 80 · see citing works
Saradalekshmi, K. R., Vellichirammal, N. N., Sathyan, S., Nair, I. V., Nair, C. M., & Banerjee, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098182 · Cited by 78 · see citing works
Misiak, B., Szmida, E., Karpiński, P., Loska, O., Sąsiadek, M. M., & Frydecka, D. (2015) · Epigenomics · doi:10.2217/epi.15.68 · Cited by 77 · see citing works
An Update on the Epigenetics of Psychotic Diseases and Autism
Abdolmaleky, H. M., Zhou, J., & Thiagalingam, S. (2015) · Epigenomics · doi:10.2217/epi.14.85 · Cited by 75 · see citing works
Srivastava, A., Dada, O. O., Qian, J., Al-Chalabi, N., Fatemi, A. B., Gerretsen, P., Graff, A., & Luca, V. D. (2021) · Psychiatry Research · doi:10.1016/j.psychres.2021.114218 · Cited by 71 · see citing works
Understanding epigenetics of schizophrenia in the backdrop of its antipsychotic drug therapy
Swathy, B., & Banerjee, M. (2017) · Epigenomics · doi:10.2217/epi-2016-0106 · Cited by 69 · see citing works
Evidence for a role of nicotinic acetylcholine receptors in schizophrenia
Catherine, E. A. (2007) · Frontiers in bioscience · doi:10.2741/2424 · Cited by 63 · see citing works
Shimabukuro, M., Jinno, Y., Fuke, C., & Okazaki, Y. (2006) · Behavioral and Brain Functions · doi:10.1186/1744-9081-2-37 · Cited by 64 · see citing works
Self-citationAdult global DNA methylation in relation to pre-natal nutrition
Lumey, L. H., Terry, M. B., Delgado‐Cruzata, L., Liao, Y., Wang, Q., Susser, E., McKeague, I. W., & Santella, R. M. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr137 · Cited by 63 · see citing works
Plasma total homocysteine is associated with DNA methylation in patients with schizophrenia
Kinoshita, M., Numata, S., Tajima, A., Shimodera, S., Imoto, I., & Ohmori, T. (2013) · Epigenetics · doi:10.4161/epi.24621 · Cited by 62 · see citing works
Bromberg, A., Levine, J., Nemetz, B., Belmaker, R. H., & Agam, G. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.01.009 · Cited by 60 · see citing works
Sex-specific DNA methylation differences in Alzheimer’s disease pathology
Zhang, L., Young, J. I., Gomez, L., Silva, T. C., Schmidt, M. A., Cai, J., Chen, X., Martin, E. R., & Wang, L. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01177-8 · Cited by 58 · see citing works
“In both human and animal models, it has been observed treatment with haloperidol induces sex-specific DNA methylation differences [71, 72].”
BackgroundHypomethylation of LINE-1 elements in schizophrenia and bipolar disorder
Li, S., Yang, Q., Hou, Y., Jiang, T., Zong, L., Wang, Z., Luo, X., Liang, W., Zhao, H., Ning, Y., et al. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.10.009 · Cited by 57 · see citing works
Toward the Identification of Peripheral Epigenetic Biomarkers of Schizophrenia
Guidotti, A., Auta, J., Davis, J. M., Dong, E., Gavin, D. P., Grayson, D. R., Sharma, R. P., Smith, R. C., Tueting, P. A., & Zhubi, A. (2014) · Journal of Neurogenetics · doi:10.3109/01677063.2014.892485 · Cited by 54 · see citing works
Epigenetic Changes in Response to Tai Chi Practice: A Pilot Investigation of DNA Methylation Marks
Ren, H., Collins, V., Clarke, S., Han, J.-S., Lam, P., Clay, F. J., Williamson, L. M., & Choo, K. H. A. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/841810 · Cited by 53 · see citing works
Epigenetics and gene expression profile in first-episode psychosis: the role of childhood trauma
Tomassi, S., & Tosato, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.018 · Cited by 51 · see citing works
Methylation matters? Decreased methylation status of genomic DNA in the blood of schizophrenic twins
Bönsch, D., Wunschel, M., Lenz, B., Janssen, G., Weisbrod, M., & Sauer, H. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2011.09.004 · Cited by 51 · see citing works
Alelú‐Paz, R., Carmona, F. J., Sanchez-Mut, J. V., Cariaga-Martínez, A. E., González‐Corpas, A., Ashour, N., Orea, M. J., Escanilla, A., Monje, A., Márquez, C. G., et al. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01496 · Cited by 49 · see citing works
Swathy, B., Saradalekshmi, K. R., Nair, I. V., Nair, C. M., & Banerjee, M. (2018) · Epigenomics · doi:10.2217/epi-2017-0086 · Cited by 47 · see citing works
Li-Tempel, T., Larra, M. F., Sandt, E., Mériaux, S. B., Schote, A. B., Schächinger, H., Muller, C. P., & Turner, J. D. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0180-y · Cited by 46 · see citing works
Epigenetic profiling of human brain differential DNA methylation networks in schizophrenia
Lee, S.-A., & Huang, K.-C. (2016) · BMC Medical Genomics · doi:10.1186/s12920-016-0229-y · Cited by 46 · see citing works
Age-associated decrease in global DNA methylation in patients with major depression
Lin, P., Tseng, P., Lee, Y. Z., Hung, C., Lung, F., Chen, C., & Chong, M. (2014) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s71997 · Cited by 46 · see citing works
Epigenetic and Pharmacoepigenomic Studies of Major Psychoses and Potentials for Therapeutics
Abdolmaleky, H. M., Zhou, J., Thiagalingam, S., & Smith, C. L. (2008) · Pharmacogenomics · doi:10.2217/14622416.9.12.1809 · Cited by 45 · see citing works
Effects of MAOA promoter methylation on susceptibility to paranoid schizophrenia
Chen, Y., Zhang, J., Zhang, L., Shen, Y., & Xu, Q. (2011) · Human Genetics · doi:10.1007/s00439-011-1131-5 · Cited by 45 · see citing works
Masemola, M. L., van der Merwe, L., Lombard, Z., Viljoen, D. L., & Ramsay, M. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00085 · Cited by 44 · see citing works
Global DNA methylation and low-level exposure to benzene
Fustinoni, S., Rossella, F., Polledri, E., Bollati, V., Campo, L., Byun, H., Agnello, L., Consonni, D., Pesatori, A., Baccarelli, A., et al. (2012) · PubMed · doi:10.25405/ncl.34244430.v1 · Cited by 44 · see citing works
Micale, V., Bartolomeo, M. D., Martino, S. D., Štark, T., Dell’Osso, B. M., Drago, F., & D’Addario, C. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108279 · Cited by 40 · see citing works
Inverse changes in L1 retrotransposons between blood and brain in major depressive disorder
Liu, S., Du, T., Liu, Z., Shen, Y., Xiu, J., & Xu, Q. (2016) · Scientific Reports · doi:10.1038/srep37530 · Cited by 37 · see citing works
A Methionine-Induced Animal Model of Schizophrenia: Face and Predictive Validity
Wang, L., Alachkar, A., Sanathara, N. M., Belluzzi, J. D., Wang, Z., & Civelli, O. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv054 · Cited by 37 · see citing works
The epigenome and postnatal environmental influences in psychotic disorders
Pishva, E., Kenis, G., van den Hove, D., Lesch, K., Boks, M. P., van Os, J., & Rutten, B. P. F. (2014) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s00127-014-0831-2 · Cited by 35 · see citing works
Methylated Spirits: Epigenetic Hypotheses of Psychiatric Disorders
Stahl, S. M. (2010) · CNS Spectrums · doi:10.1017/s1092852900000055 · Cited by 30 · see citing works
Epigenetic Profiling in Schizophrenia and Major Mental Disorders
Iwamoto, K., & Kato, T. (2009) · Neuropsychobiology · doi:10.1159/000234811 · Cited by 27 · see citing works
Vryer, R., & Saffery, R. (2017) · Clinical Epigenetics · doi:10.1186/s13148-017-0311-0 · Cited by 28 · see citing works
Murata, Y., Ikegame, T., Koike, S., Saito, T., Ikeda, M., Sasaki, T., Iwata, N., Kasai, K., Bundo, M., & Iwamoto, K. (2020) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109855 · Cited by 25 · see citing works
Self-citationJones, J. R., Skinner, C. D., Friez, M. J., Schwartz, C. E., & Stevenson, R. E. (2008) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.32396 · Cited by 27 · see citing works
Schizophrenia as segmental progeria
Papanastasiou, E., Gaughran, F., & Smith, S. M. (2011) · Journal of the Royal Society of Medicine · doi:10.1258/jrsm.2011.110051 · Cited by 27 · see citing works
Variation in global DNA hydroxymethylation with age associated with schizophrenia
Jiang, T., Zong, L., Zhou, L., Hou, Y., Zhang, L., Zheng, X., Han, H., Li, S., Zhang, W., Zhang, J., et al. (2017) · Psychiatry Research · doi:10.1016/j.psychres.2017.08.022 · Cited by 26 · see citing works
Epigenetic regulation of AXL and risk of childhood asthma symptoms
Gao, L., Millstein, J., Siegmund, K. D., Dubeau, L., Maguire, R. L., Gilliland, F. D., Murphy, S. K., Hoyo, C., & Breton, C. V. (2017) · Clinical Epigenetics · doi:10.1186/s13148-017-0421-8 · Cited by 24 · see citing works
Kim, S. H., Lee, H. Y., Yi, H., Ahn, Y. M., & Kim, Y. S. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.10.002 · Cited by 21 · see citing works
Bosia, M., Pigoni, A., & Cavallaro, R. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2015.976552 · Cited by 20 · see citing works
Müller, D., Grevet, E. H., da Silva, N. A. F., Bandeira, C. E., Barbosa, E., Vitola, E. S., Charão, M. F., Linden, R., Rohde, L. A., Ramos, J. K. N., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01493-y · Cited by 19 · see citing works
The state of the art of nanopsychiatry for schizophrenia diagnostics and treatment
Radaic, A., & Martins‐de‐Souza, D. (2020) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2020.102222 · Cited by 19 · see citing works
The neuroendocrine modulation of global DNA methylation in neuropsychiatric disorders
Müller, D., Grevet, E. H., da Silva, B. S., Charão, M. F., Rovaris, D. L., & Bau, C. H. D. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00924-y · Cited by 19 · see citing works
Sex-specific epigenetic programming in renal fibrosis and inflammation
Kumar, P., & Brooks, H. L. (2023) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00091.2023 · Cited by 18 · see citing works
Gavin, D. P., & Floreani, C. V. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801311-3.00005-6 · Cited by 17 · see citing works
Saxena, S., Choudhury, S., Maroju, P. A., Anne, A., Kumar, L., & Mohan, K. N. (2021) · Epigenomics · doi:10.2217/epi-2021-0133 · Cited by 16 · see citing works
Epigenetics and Chronic Diseases: An Overview
Smith, R. G., & Mill, J. (2011) · Springer eBooks · doi:10.1007/978-1-84882-644-1_1 · Cited by 13 · see citing works
Abdolmaleky, H. M., Glatt, S. J., & Tsuang, M. T. (2011) · Springer eBooks · doi:10.1007/978-1-84882-644-1_11 · Cited by 12 · see citing works
Fooling Mother Nature: Epigenetics and Novel Treatments for Psychiatric Disorders
Stahl, S. (2010) · CNS Spectrums · doi:10.1017/s1092852900029229 · Cited by 12 · see citing works
Bromberg, A., Levine, J., Belmaker, R., & Agam, G. (2010) · Journal of Psychopharmacology · doi:10.1177/0269881110388328 · Cited by 11 · see citing works
DNA Methylation Analysis in Human Cancer
O’Sullivan, E., & Goggins, M. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-287-2_7 · Cited by 11 · see citing works
Implications of petrochemical exposure and epigenetic alterations on human health
Jayaraman, S., Eswaran, A., Veeraraghavan, V. P., Fazal, M. A., Al-Rahbi, A., & Sirasanagandla, S. R. (2025) · Frontiers in Toxicology · doi:10.3389/ftox.2025.1542871 · Cited by 10 · see citing works
van Eekelen, J. A. M., Ellis, J. A., Pennell, C. E., Saffery, R., Mattes, E., Craig, J. M., & Olsson, C. A. (2012) · Mental Illness · doi:10.4081/mi.2012.e21 · Cited by 10 · see citing works
Palego, L. (2015) · Biochemistry & Pharmacology Open Access · doi:10.4172/2167-0501.1000159 · Cited by 7 · see citing works
The Relevance of Epigenetics to Major Psychosis
Mill, J. S., & Petronis, A. (2008) · Springer eBooks · doi:10.1007/978-1-4020-9187-2_23 · Cited by 7 · see citing works
Angelin, M., Gopinath, P., Raghavan, V., THARA, R., Ahmad, F., Munirajan, A. K., & Sudesh, R. (2024) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s466502 · Cited by 7 · see citing works
Rok-Bujko, P. (2022) · Postępy Psychiatrii i Neurologii · doi:10.5114/ppn.2022.117963 · Cited by 6 · see citing works
DNA methylation in schizophrenia: progress and challenges
Zong, X., Hu, M., Li, Z., Cao, H., Chen, X., & Tang, J. (2015) · 中国科学通报:英文版 · doi:10.1007/s11434-014-0690-y · Cited by 5 · see citing works
Flow Cytometric and Laser Scanning Microscopic Approaches in Epigenetics Research
Székvölgyi, L., Imre, L., Minh, D. X. Q., Hegedüs, É., Bacsó, Z., & Szabó, G. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-414-2_7 · Cited by 5 · see citing works
Pharmacoepigenetics of Antipsychotic Drugs
Swathy, B., Polakkattil, B. K., & Banerjee, M. (2019) · Pharmacoepigenetics · doi:10.1016/b978-0-12-813939-4.00025-5 · Cited by 3 · see citing works
Epigenetic Instability in Embryonic Stem Cells
Horii, T., & Hat, I. (2013) · InTech eBooks · doi:10.5772/54367 · Cited by 3 · see citing works
Global DNA methylation patterns in Alcohol Use Disorder
Schuch, J. B., Bandeira, C. E., Jorge, L. S., Müller, D., Charão, M. F., da Silva, B. S., Grevet, E. H., Kessler, F. H. P., DIEMEN, L. V., Rovaris, D. L., et al. (2023) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2023-0139 · Cited by 3 · 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
Abdolmaleky, H. M., Ahmadkhaniha, H., Nohesara, S., & Smith, C. L. (2008) · Iranian Journal of Psychiatry and Behavioral Sciences · Cited by 3 · see citing works
Cucu, N. (2011) · doi:10.1002/9780470959824.ch2 · Cited by 3 · see citing works
Effect of Environmental Chemical Exposures on Epigenetics of Diseases: A Systematic Review
Ranjan, S., & Sharma, P. K. (2016) · SSR Institute of International Journal of Life Sciences · doi:10.21276/ijlssr.2016.2.4.11 · Cited by 2 · see citing works
Possible Biomarkers Modulating Haloperidol Efficacy and/or Tolerability
Porcelli, S., Crisafulli, C., Calabrò, M., Serretti, A., & Rujescu, D. (2016) · Pharmacogenomics · doi:10.2217/pgs.16.5 · Cited by 2 · see citing works
Epigenetics and Atherosclerosis
Aavik, E., Turunen, M. P., & Ylä‐Herttuala, S. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3345-3_13 · Cited by 2 · see citing works
Association between the copy number variations of Methyl-CpG binding domain family and schizophrenia
Sun, Z., Kou, C., Gao, Z., Guo, X., Han, B., Feng, Y., Ding, Q., & Bai, W. (2024) · Gene · doi:10.1016/j.gene.2024.148836 · Cited by 1 · see citing works
Epigenetic Epidemiology of Atherosclerosis
Aavik, E., Turunen, M. P., & Ylä‐Herttuala, S. (2011) · Springer eBooks · doi:10.1007/978-94-007-2495-2_21 · Cited by 1 · see citing works
Epidemiology, Epigenetics, and Psychopathology
Bustamante, A. C., & Uddin, M. (2014) · Medical Epigenetics · doi:10.1159/000362762 · Cited by 1 · see citing works
Transcriptome Analysis of Systems Biology for Schizophrenia
Huang, K.-C., Tsao, T. T.-H., Wang, T., & Lee, S. (2016) · InTech eBooks · doi:10.5772/66864 · Cited by 1 · see citing works
DNA Methylation Analysis: Providing New Insight into Human Disease
Cottrell, S. E., deVos, T., Distler, J., Haefliger, C., Lesche, R., Plum, A., & Schuster, M. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-369420-1.00011-1 · Cited by 1 · see citing works
Epigenetic involvement in psychiatric disorders and psychiatric drugs
de Jong, N. M. (2010) · Utrecht University Repository (Utrecht University)
Epigenetic Epidemiology of Psychiatric Disorders
Uddin, M., Bustamante, A. C., & Toyokawa, S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-417114-5.00006-1
Epigenomics in Neurobehavioral Diseases
Smith, C. L., & Huang, K. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-388415-2.00007-x
- Authors
- Shimabukuro, M., Sasaki, T., Imamura, A., Tsujita, T., Fuke, C., Umekage, T., Tochigi, M., Hiramatsu, K., Miyazaki, T., Oda, T., Sugimoto, J., Jinno, Y., & Okazaki, Y.
- Affiliations
- University of the Ryukyus (JP)
- The University of Tokyo (JP)
- Nagasaki University (JP)
- Mie University (JP)
- Corresponding author
- Jinno, Yoshihiro
- Venue
- Journal of Psychiatric Research
- Publisher
- Elsevier BV
- Published
- 2007-12
- Volume
- 41
- Issue
- 12
- Pages
- 1042-1046
- ISSN
- 0022-3956 (ISSN-L)
- OpenAlex
- W2148944032
- Cited by
- 108
- References
- 40
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 6 · 2016: 10 · 2015: 7 · 2014: 8 · 2013: 5 · 2012: 14
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Psychiatric Research (publishedVersion)
- PubMed (publishedVersion)
- 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 › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- schizophrenia, DNA methylation, global hypomethylation, peripheral blood leukocytes, epigenetics, sex differences, age effects
- MeSH terms
- Adolescent, Adult, Age Factors, Aged, Aged, 80 and over, Child, Chromatography, High Pressure Liquid, Female, Humans, Leukocytes, Male, Middle Aged, Schizophrenia, Sex Factors, DNA Methylation, Epigenesis, Genetic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review