Genome-wide DNA Methylation Changes in a Mouse Model of Infection-Mediated Neurodevelopmental Disorders
Open accessAbstract
Background Prenatal exposure to infectious or inflammatory insults increases the risk of neurodevelopmental disorders. Using a well-established mouse model of prenatal viral-like immune activation, we examined whether this pathological association involves genome-wide DNA methylation differences at single nucleotide resolution.Methods Prenatal immune activation was induced by maternal treatment with the viral mimetic polyriboinosinic-polyribocytidylic acid in middle or late gestation. Following behavioral and cognitive characterization of the adult offspring (n = 12 per group), unbiased capture array bisulfite sequencing was combined with subsequent matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and quantitative real-time polymerase chain reaction analyses to quantify DNA methylation changes and transcriptional abnormalities in the medial prefrontal cortex of immune-challenged and control offspring. Gene ontology term enrichment analysis was used to explore shared functional pathways of genes with differential DNA methylation.Results Adult offspring of immune-challenged mothers displayed hyper- and hypomethylated CpGs at numerous loci and at distinct genomic regions, including genes relevant for gamma-aminobutyric acidergic differentiation and signaling (e.g., Dlx1, Lhx5, Lhx8), Wnt signaling (Wnt3, Wnt8a, Wnt7b), and neural development (e.g., Efnb3, Mid1, Nlgn1, Nrxn2). Altered DNA methylation was associated with transcriptional changes of the corresponding genes. The epigenetic and transcriptional effects were dependent on the offspring's age and were markedly influenced by the precise timing of prenatal immune activation.Conclusions Prenatal viral-like immune activation is capable of inducing stable DNA methylation changes in the medial prefrontal cortex. These long-term epigenetic modifications are a plausible mechanism underlying the disruption of prefrontal gene transcription and behavioral functions in subjects with prenatal infectious histories.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Such effects likely involve epigenetic dysregulation of transcriptional programs that are sensitive to environmental changes or insults.
“Such effects likely involve the epigenetic dysregulation of transcriptional programs that are sensitive to environmental changes or insults [135–137].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [136]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Functions of DNA methylation: islands, start sites, gene bodies and beyond
Jones, P. A. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3230 · Cited by 6,061 · see citing works
Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies
Brown, A. S., & Derkits, E. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09030361 · Cited by 1,269 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
The Cerebellum, Sensitive Periods, and Autism
Wang, S. S. ‐., Kloth, A. D., & Badura, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.016 · Cited by 829 · see citing works
Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B. K., & Feldon, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0099-06.2006 · Cited by 774 · see citing works
Self-citationMalkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J., & Patterson, P. H. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.011 · Cited by 662 · see citing works
Prenatal Poly(I:C) Exposure and Other Developmental Immune Activation Models in Rodent Systems
Meyer, U. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.011 · Cited by 626 · see citing works
Self-citationMapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex
Jaffe, A. E., Gao, Y., Deep-Soboslay, A., Tao, R., Hyde, T. M., Weinberger, D. R., & Kleinman, J. E. (2016) · Nature Neuroscience · doi:10.1038/nn.4181 · Cited by 511 · see citing works
Epigenetic and transgenerational reprogramming of brain development
Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505 · see citing works
Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia
Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.012 · Cited by 494 · see citing works
Self-citationSocial interaction and sensorimotor gating abnormalities in mice lacking Dvl1
Lijam, N., Paylor, R., McDonald, M. P., Crawley, J. N., Deng, C.-X., Herrup, K., Stevens, K. E., Maccaferri, G., McBain, C. J., Sussman, D. J., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80354-2 · Cited by 470 · see citing works
Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., & Feldon, J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.09.012 · Cited by 457 · see citing works
Self-citationAutism After Infection, Febrile Episodes, and Antibiotic Use During Pregnancy: An Exploratory Study
Atladóttir, H. Ó., Henriksen, T. B., Schendel, D. E., & Parner, E. T. (2012) · Pediatrics · doi:10.1542/peds.2012-1107 · Cited by 369 · see citing works
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works
Self-citationEpidemiology-driven neurodevelopmental animal models of schizophrenia
Meyer, U., & Feldon, J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.018 · Cited by 366 · see citing works
Self-citationQuaderi, N. A., Schweiger, S., Gaudenz, K., Franco, B., Rugarli, E. I., Berger, W., Feldman, G. J., Volta, M., Andolfi, G., Gilgenkrantz, S., et al. (1997) · Nature Genetics · doi:10.1038/ng1197-285 · Cited by 363 · see citing works
Elevated maternal C-reactive protein and autism in a national birth cohort
Brown, A. S., Sourander, A., Hinkka-Yli-Salomäki, S., McKeague, I. W., Sundvall, J., & Surcel, H.-M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2012.197 · Cited by 343 · see citing works
Epigenetic basis of mental illness
Nestler, E. J., Peña, C. J., Kundakovic, M., Mitchell, A., & Akbarian, S. (2016) · The Neuroscientist · doi:10.1177/1073858415608147 · Cited by 342 · see citing works
Schizophrenia: a tale of two critical periods for prefrontal cortical development
Selemon, L. D., & Zecevic, N. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.115 · Cited by 336 · see citing works
Molecular insights into transgenerational non-genetic inheritance of acquired behaviours
Bohacek, J., & Mansuy, I. M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3964 · Cited by 318 · see citing works
DNA methylation dynamics during the mammalian life cycle
Hackett, J. A., & Surani, M. A. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0328 · Cited by 317 · see citing works
Jaaro-Peled, H., Hayashi‐Takagi, A., Seshadri, S., Kamiya, A., Brandon, N. J., & Sawa, A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.007 · Cited by 315 · see citing works
Developmental neuroinflammation and schizophrenia
Meyer, U. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2011.11.003 · Cited by 300 · see citing works
Self-citationEpigenetic Mechanisms in Inflammation
Bayarsaihan, D. (2010) · Journal of Dental Research · doi:10.1177/0022034510378683 · Cited by 290 · see citing works
Truncating mutations in NRXN2 and NRXN1 in autism spectrum disorders and schizophrenia
Gauthier, J., Siddiqui, T. J., Huashan, P., Yokomaku, D., Hamdan, F. F., Champagne, N., Lapointe, M., Spiegelman, D., Noreau, A., Lafrenière, R. G., et al. (2011) · Human Genetics · doi:10.1007/s00439-011-0975-z · Cited by 286 · see citing works
The Dynamics of DNA Methylation in Schizophrenia and Related Psychiatric Disorders
Grayson, D. R., & Guidotti, A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.125 · Cited by 267 · see citing works
Tan, H.-Y., Callicott, J. H., & Weinberger, D. R. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm069 · Cited by 266 · see citing works
Fatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 259 · see citing works
Winter, C., Djodari-Irani, A., Sohr, R., Morgenstern, R., Feldon, J., Juckel, G., & Meyer, U. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009206 · Cited by 242 · see citing works
Self-citationBitanihirwe, B. K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., & Meyer, U. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.129 · Cited by 237 · see citing works
Samartzis, L., Dima, D., Fusar‐Poli, P., & Kyriakopoulos, M. (2014) · Journal of Neuroimaging · doi:10.1111/j.1552-6569.2012.00779.x · Cited by 236 · see citing works
Gestational Influenza and Bipolar Disorder in Adult Offspring
Parboosing, R., Bao, Y., Shen, L., Schaefer, C. A., & Brown, A. S. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.896 · Cited by 224 · see citing works
Epigenetic GABAergic targets in schizophrenia and bipolar disorder
Guidotti, A., Auta, J., Chen, Y., Davis, J. M., Dong, E., Gavin, D. P., Grayson, D. R., Matrisciano, F., Pinna, G., Satta, R., et al. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.10.021 · Cited by 220 · see citing works
Vuillermot, S., Weber, L., Feldon, J., & Meyer, U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5408-09.2010 · Cited by 217 · see citing works
Self-citationCanetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., Gordon, J. A., Brown, A., & Kellendonk, C. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.222 · Cited by 201 · see citing works
Kenny, E. M., Cormican, P., Furlong, S., Heron, E. A., Kenny, G., Fahey, C., Kelleher, E., Ennis, S., Tropea, D., Anney, R., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.127 · Cited by 190 · see citing works
Weber-Stadlbauer, U., Richetto, J., Labouesse, M. A., Bohacek, J., Mansuy, I. M., & Meyer, U. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.41 · Cited by 170 · see citing works
Self-citationCellular Patterns of Transcription Factor Expression in Developing Cortical Interneurons
Cobos, I., Long, J. E., Thwin, M. T., & Rubenstein, J. L. R. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk003 · Cited by 167 · see citing works
Dong, E., Dzitoyeva, S., Matrisciano, F., Tueting, P. A., Grayson, D. R., & Guidotti, A. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.08.012 · Cited by 162 · see citing works
Wnt signalling in neuronal differentiation and development
Inestrosa, N. C., & Varela‐Nallar, L. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1996-4 · Cited by 162 · see citing works
Wischhof, L., Irrsack, E., Osorio, C., & Koch, M. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.004 · Cited by 158 · see citing works
Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration
Sentürk, A., Pfennig, S., Weiss, A., Burk, K., & Acker‐Palmer, A. (2011) · Nature · doi:10.1038/nature09874 · Cited by 157 · see citing works
Viral infection, inflammation and schizophrenia
Kneeland, R. E., & Fatemi, S. H. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.02.001 · Cited by 152 · see citing works
Schubert, D., Martens, G. J. M., & Kolk, S. M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.147 · Cited by 149 · see citing works
Harvey, L., & Boksa, P. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22043 · Cited by 149 · see citing works
Li, Q., Cheung, C., Wei, R., Hui, E. S. K., Feldon, J., Meyer, U., Chung, S. K., Chua, S. E., Sham, P. C., Wu, E. X., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006354 · Cited by 149 · see citing works
Self-citationSerological Documentation of Maternal Influenza Exposure and Bipolar Disorder in Adult Offspring
Canetta, S., Bao, Y., Co, M. D. T., Ennis, F. A., Cruz, J., Terajima, M., Shen, L., Kellendonk, C., Schaefer, C. A., & Brown, A. S. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.13070943 · Cited by 147 · see citing works
Lipina, T. V., Zai, C. C. H., Hlousek, D., Roder, J., & Wong, A. H. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0091-13.2013 · Cited by 146 · see citing works
Abnormal Asymmetry of Brain Connectivity in Schizophrenia
Ribolsi, M., Daskalakis, Z. J., Siracusano, A., & Koch, G. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.01010 · Cited by 146 · see citing works
Abnormal Trajectories of Neurodevelopment and Behavior Following In Utero Insult in the Rat
Piontkewitz, Y., Arad, M., & Weiner, I. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.06.007 · Cited by 144 · see citing works
Labouesse, M. A., Dong, E., Grayson, D. R., Guidotti, A., & Meyer, U. (2015) · Epigenetics · doi:10.1080/15592294.2015.1114202 · Cited by 138 · see citing works
Self-citationMeyer, U., Engler, A., Weber, L., Schedlowski, M., & Feldon, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.031 · Cited by 135 · see citing works
Self-citationRichetto, J., Calabrese, F., Riva, M. A., & Meyer, U. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs195 · Cited by 134 · see citing works
Self-citationSchizophrenia: susceptibility genes, dendritic-spine pathology and gray matter loss
Bennett, M. R. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.08.003 · Cited by 126 · see citing works
Prenatal inflammation and neurodevelopment in schizophrenia: A review of human studies
Miller, B. J., Culpepper, N. H., Rapaport, M. H., & Buckley, P. F. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.03.010 · Cited by 124 · see citing works
Jakovcevski, I., Mayer, N., & Zecevic, N. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq245 · Cited by 124 · see citing works
Giovanoli, S., Notter, T., Richetto, J., Labouesse, M. A., Vuillermot, S., Riva, M. A., & Meyer, U. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0437-y · Cited by 124 · see citing works
Self-citationEpigenetic Regulation of Inflammatory Cytokines and Associated Genes in Human Malignancies
Yasmin, R., Siraj, S., Hassan, A., Khan, A. R., Abbasi, R., & Ahmad, N. (2015) · Mediators of Inflammation · doi:10.1155/2015/201703 · Cited by 118 · see citing works
Prenatal maternal immune activation causes epigenetic differences in adolescent mouse brain
Basil, P., Li, Q., Dempster, E. L., Mill, J., Sham, P.-C., Wong, C. C. Y., & McAlonan, G. M. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.80 · Cited by 116 · see citing works
WNTs in synapse formation and neuronal circuitry
Park, M., & Shen, K. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.145 · Cited by 106 · see citing works
Sanderson, D. J., & Bannerman, D. M. (2010) · Hippocampus · doi:10.1002/hipo.20896 · Cited by 103 · see citing works
Connor, C., Dincer, A., Straubhaar, J., Galler, J. R., Houston, I. B., & Akbarian, S. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.06.037 · Cited by 100 · see citing works
Maternal Immune Activation Disrupts Dopamine System in the Offspring
Luchicchi, A., Lecca, S., Melis, M., Felice, M. D., Cadeddu, F., Frau, R., Muntoni, A. L., Fadda, P., Devoto, P., & Pistis, M. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw007 · Cited by 96 · see citing works
Prospects for the development of epigenetic drugs for CNS conditions
Szyf, M. (2015) · Nature Reviews Drug Discovery · doi:10.1038/nrd4580 · Cited by 95 · see citing works
Self-citationEpigenetic changes at gene promoters in response to immune activation in utero
Tang, B., Jia, H., Kast, R. J., & Thomas, E. A. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2013.01.086 · Cited by 91 · see citing works
Volk, D. W., & Lewis, D. A. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu111 · Cited by 86 · see citing works
Richetto, J., Calabrese, F., Meyer, U., & Riva, M. A. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.07.006 · Cited by 84 · see citing works
Self-citationSchizophrenia-Like Attentional Deficits Following Blockade of Prefrontal Cortex GABAA Receptors
Paine, T. A., Slipp, L. E., & Carlezon, W. A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.51 · Cited by 83 · see citing works
Suchiman, H. E. D., Slieker, R. C., Kremer, D., Slagboom, P. E., Heijmans, B. T., & Tobi, E. W. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00287 · Cited by 80 · see citing works
Pérez‐Santiago, J., Dı́ez-Alarcia, R., Callado, L. F., Zhang, J. X., Chana, G., White, C., Glatt, S. J., Tsuang, M. T., Everall, I., Meana, J. J., et al. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.08.005 · Cited by 80 · see citing works
Hollins, S. L., Zavitsanou, K., Walker, F. R., & Cairns, M. J. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.99 · Cited by 78 · see citing works
Long-term pathological consequences of prenatal infection: beyond brain disorders
Labouesse, M. A., Langhans, W., & Meyer, U. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00087.2015 · Cited by 78 · see citing works
Self-citationA Role for WNT/β-Catenin Signaling in the Neural Mechanisms of Behavior
Maguschak, K. A., & Ressler, K. J. (2012) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9350-7 · Cited by 78 · see citing works
Tse, M., Piantadosi, P. T., & Floresco, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.007 · Cited by 73 · see citing works
Active DNA demethylation in post-mitotic neurons: A reason for optimism
Gavin, D. P., Chase, K. A., & Sharma, R. P. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.07.036 · Cited by 72 · see citing works
Sanderson, D. J., McHugh, S. B., Good, M. A., Sprengel, R., Seeburg, P. H., Rawlins, J. N. P., & Bannerman, D. M. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.03.018 · Cited by 72 · see citing works
Lancioni, A., Pizzo, M., Fontanella, B., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4196-09.2010 · Cited by 69 · see citing works
Bitanihirwe, B. K. Y., Weber, L., Feldon, J., & Meyer, U. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710000192 · Cited by 64 · see citing works
Self-citationPrefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons
Bissonette, G. B., Bae, M. H., Suresh, T., Jaffe, D. E., & Powell, E. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.051 · Cited by 61 · see citing works
L3/Lhx8 is involved in the determination of cholinergic or GABAergic cell fate
Manabe, T., Tatsumi, K., Inoue, M., Matsuyoshi, H., Makinodan, M., Yokoyama, S., & Wanaka, A. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03261.x · Cited by 59 · see citing works
Brain-specific epigenetic markers of schizophrenia
Wockner, L. F., Morris, C. P., Noble, E. P., Lawford, B. R., Whitehall, V., Young, R. M., & Voisey, J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.177 · Cited by 59 · see citing works
Prenatal ontogeny as a susceptibility period for cortical GABA neuron disturbances in schizophrenia
Volk, D. W., & Lewis, D. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.008 · Cited by 56 · see citing works
Li, Q., Cheung, C., Wei, R., Cheung, V., Hui, E. S. K., You, Y., Wong, P., Chua, S. E., McAlonan, G. M., & Wu, E. X. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.015 · Cited by 55 · see citing works
Epigenetic Mechanisms in Autism Spectrum Disorder
Zhubi, A., Cook, E. H., Guidotti, A., & Grayson, D. R. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801311-3.00006-8 · Cited by 51 · see citing works
Brain anatomy of autism spectrum disorders I. Focus on corpus callosum
Bellani, M., Calderoni, S., Muratori, F., & Brambilla, P. (2013) · Epidemiology and Psychiatric Sciences · doi:10.1017/s2045796013000139 · Cited by 48 · see citing works
Li, Q., Leung, Y., Zhou, I. Y., Ho, L. C., Kong, W., Basil, P., Wei, R., Lam, S. Y., Zhang, X., Law, A. C. K., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.126 · Cited by 48 · see citing works
X-linked microtubule-associated protein, Mid1, regulates axon development
Lu, T., Chen, R., Cox, T. C., Moldrich, R. X., Kurniawan, N. D., Tan, G., Perry, J. K., Ashworth, A., Bartlett, P. F., Xu, L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303687110 · Cited by 46 · see citing works
Richetto, J., Labouesse, M. A., Poe, M. M., Cook, J. M., Grace, A. A., Riva, M. A., & Meyer, U. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu055 · Cited by 38 · see citing works
Self-citationBehavioral Animal Models of Antipsychotic Drug Actions
Peleg‐Raibstein, D., Feldon, J., & Meyer, U. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25761-2_14 · Cited by 37 · see citing works
Self-citationThe MID1 protein is a central player during development and in disease
Krauß, S. (2015) · Frontiers in bioscience · doi:10.2741/4413 · Cited by 37 · see citing works
DNA modifications in the mammalian brain
Shin, J., Ming, G., & Song, H. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0512 · Cited by 32 · see citing works
Epigenetic Targets in GABAergic Neurons to Treat Schizophrenia
Costa, E., Dong, E., Grayson, D. R., Ruzicka, W. B., Simonini, M. V., Veldić, M., & Guidotti, A. (2006) · Advances in pharmacology · doi:10.1016/s1054-3589(06)54005-0 · Cited by 27 · see citing works
Social play with an unfamiliar group in weanling rats (Rattus norvegicus)
Kahana, A., Rozin, A., & Weller, A. (1997) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199703)30:2 · Cited by 9 · see citing works
Ephrin-B3 recruits PSD-95 to synapses
Fei, E., Xiong, W., & Mei, L. (2015) · Nature Neuroscience · doi:10.1038/nn.4147 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Maternal immune activation and neuroinflammation in human neurodevelopmental disorders
Han, V. X., Patel, S., Jones, H. F., & Dale, R. C. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00530-8 · Cited by 683 · see citing works
The ASD Living Biology: from cell proliferation to clinical phenotype
Courchesne, E., Pramparo, T., Gazestani, V. H., Lombardo, M. V., Pierce, K., & Lewis, N. E. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0056-y · Cited by 333 · see citing works
Neuronal activity increases translocator protein (TSPO) levels
Notter, T., Schalbetter, S. M., Clifton, N. E., Mattei, D., Richetto, J., Thomas, K., Meyer, U., & Hall, J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-0745-1 · Cited by 118 · see citing works
Self-citationVogel Ciernia, A., Careaga, M., LaSalle, J. M., & Ashwood, P. (2018) · Glia · doi:10.1002/glia.23261 · Cited by 69 · see citing works
Prenatal transportation stress alters genome-wide DNA methylation in suckling Brahman bull calves1,2
Littlejohn, B. P., Price, D. M., Neuendorff, D. A., Carroll, J. A., Vann, R. C., Riggs, P. K., Riley, D. G., Long, C. R., Welsh, T. H., & Randel, R. D. (2018) · Journal of Animal Science · doi:10.1093/jas/sky350 · Cited by 31 · see citing works
- Authors
- Richetto, J., Massart, R., Weber-Stadlbauer, U., Szyf, M., Riva, M. A., & Meyer, U.
- Affiliations
- University of Zurich (CH)
- Epigénétique et Destin Cellulaire (FR)
- University of Milan (IT)
- Corresponding author
- Meyer, Urs
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 81
- Issue
- 3
- Pages
- 265-276
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2518262616
- Cited by
- 148
- References
- 95
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 16 · 2023: 15 · 2022: 19 · 2021: 16 · 2020: 19 · 2019: 19 · 2018: 18 · 2017: 7 · 2016: 2
- FWCI
- 7.97
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Ministero dell'Università e della Ricerca
- Canadian Institutes of Health Research (MOP42411)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- DNA methylation, prenatal immune activation, neurodevelopmental disorders, polyriboinosinic-polyribocytidylic acid, maternal infection, medial prefrontal cortex, epigenetics, Wnt signaling, Dlx genes, neuroligin-1, MID1, gene expression
- MeSH terms
- Animals, Behavior, Animal, Disease Models, Animal, Female, Interpersonal Relations, Male, Mice, Inbred C57BL, Poly I-C, Pregnancy, Prenatal Exposure Delayed Effects, Genome, Prefrontal Cortex, Maze Learning, CpG Islands, DNA Methylation, Epigenesis, Genetic, Mice, GABAergic Neurons, Wnt Signaling Pathway, Prepulse Inhibition, Neurodevelopmental Disorders
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
