Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons
Open accessAbstract
Dnmt1 and Dnmt3a are important DNA methyltransferases that are expressed in postmitotic neurons, but their function in the CNS is unclear. We generated conditional mutant mice that lack Dnmt1, Dnmt3a or both exclusively in forebrain excitatory neurons and found that only double knockout (DKO) mice showed abnormal long-term plasticity in the hippocampal CA1 region together with deficits in learning and memory. Although we found no neuronal loss, hippocampal neurons in DKO mice were smaller than in the wild type; furthermore, DKO neurons showed deregulated expression of genes, including the class I MHC genes and Stat1, that are known to contribute to synaptic plasticity. In addition, we observed a significant decrease in DNA methylation in DKO neurons. We conclude that Dnmt1 and Dnmt3a are required for synaptic plasticity, learning and memory through their overlapping roles in maintaining DNA methylation and modulating neuronal gene expression in adult CNS neurons.
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?
The development of the brain and the functional abilities of the brain such as memory formation, learning, motivation and reward are all regulated by epigenetic regulation of gene expression.
“Recent animal studies have demonstrated that the development of the brain and the functional abilities of the brain such as memory formation, learning, motivation and reward are all regulated by epigenetic regulation of gene expression 16, 17.”
From Resilience in mental health: linking psychological and neurobiological perspectives. (2013) · cites this paper as [17]
Mice lacking Dnmt1 and Dnmt3a in postmitotic neurons show abnormal long-term plasticity in CA1 hippocampal neurons along with deficits in learning and memory.
“Mice lacking Dnmt1 and Dnmt3a in postmitotic neurons show abnormal long-term plasticity in CA1 hippocampal neurons along with deficits in learning and memory [ 75 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [75]
STAT1 and STAT3 have roles in hippocampal plasticity.
“STAT1 and STAT3 have roles in hippocampal plasticity178,179.”
From Immune mediators in the brain and peripheral tissues in autism spectrum disorder (2015) · cites this paper as [179]
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
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Okano, M., Bell, D. W., Haber, D. A., & Li, E. (1999) · Cell · doi:10.1016/s0092-8674(00)81656-6 · Cited by 6,143 · see citing works
Self-citationConversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., et al. (2009) · Science · doi:10.1126/science.1170116 · Cited by 5,836 · see citing works
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality
Li, E., Bestor, T. H., & Jaenisch, R. (1992) · Cell · doi:10.1016/0092-8674(92)90611-f · Cited by 3,984 · see citing works
Self-citationThe Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
Synaptic Activity and the Construction of Cortical Circuits
Katz, L. C., & Shatz, C. J. (1996) · Science · doi:10.1126/science.274.5290.1133 · Cited by 3,048 · see citing works
The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain
Kriaucionis, S., & Heintz, N. (2009) · Science · doi:10.1126/science.1169786 · Cited by 2,700 · see citing works
HDAC2 negatively regulates memory formation and synaptic plasticity
Guan, J.-S., Haggarty, S. J., Giacometti, E., Dannenberg, J.-H., Joseph, N., Gao, J., Nieland, T. J. F., Zhou, Y., Wang, X., Mazitschek, R., et al. (2009) · Nature · doi:10.1038/nature07925 · Cited by 1,644 · see citing works
Self-citationDNA Methylation-Related Chromatin Remodeling in Activity-Dependent <i>Bdnf</i> Gene Regulation
Martinowich, K., Hattori, D., Wu, H., Fouse, S., He, F., Hu, Y., Fan, G., & Sun, Y. E. (2003) · Science · doi:10.1126/science.1090842 · Cited by 1,405 · see citing works
Self-citationEpigenetic regulation in psychiatric disorders
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2132 · Cited by 1,400 · see citing works
DNMT1 and DNMT3b cooperate to silence genes in human cancer cells
Rhee, I. P., Bachman, K. E., Park, B. H., Jair, K.-W., Yen, R.-W. C., Schuebel, K. E., Cui, H., Feinberg, A. P., Christoph Lengauer, C., Kinzler, K. W., et al. (2002) · Nature · doi:10.1038/416552a · Cited by 1,243 · see citing works
Derepression of BDNF Transcription Involves Calcium-Dependent Phosphorylation of MeCP2
Chen, W. G., Chang, Q., Lin, Y., Meissner, A., West, A. E., Griffith, E. C., Jaenisch, R., & Greenberg, M. E. (2003) · Science · doi:10.1126/science.1086446 · Cited by 1,232 · see citing works
Recovery of learning and memory is associated with chromatin remodelling
Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., & Tsai, L.-H. (2007) · Nature · doi:10.1038/nature05772 · Cited by 1,227 · see citing works
Xu, G., Bestor, T. H., Bourc’his, D., Hsieh, C., Tommerup, N., Bugge, M., Hultén, M. A., Qu, X., Russo, J. J., & Viégas-Pèquignot, E. (1999) · Nature · doi:10.1038/46052 · Cited by 1,204 · see citing works
Covalent Modification of DNA Regulates Memory Formation
Miller, C. A., & Sweatt, J. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.022 · Cited by 1,180 · see citing works
Self-citationRegulation of histone acetylation during memory formation in the hippocampus
Levenson, J. M., O'Riordan, K. J., Brown, K. D., Trinh, M. A., Molfese, D. L., & Sweatt, J. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402229200 · Cited by 1,131 · see citing works
Self-citationDNA 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
Cui, L., Jeong, H., Borovecki, F., Parkhurst, C. N., Tanese, N., & Krainc, D. (2006) · Cell · doi:10.1016/j.cell.2006.09.015 · Cited by 1,012 · see citing works
Neuronal Activity–Induced Gadd45b Promotes Epigenetic DNA Demethylation and Adult Neurogenesis
Dengke, K., Jang, M., Guo, J. U., Kitabatake, Y., Chang, M.-L., Pow-anpongkul, N., Flavell, R. A., Lu, B., Ming, G., & Song, H. (2009) · Science · doi:10.1126/science.1166859 · Cited by 929 · see citing works
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
Functional requirement for class I MHC in CNS development and plasticity
Huh, G. S., Boulanger, L. M., Du, H., Riquelme, P. A., Brotz, T. M., & Shatz, C. J. (2000) · Science · doi:10.1126/science.290.5499.2155 · Cited by 828 · see citing works
Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation
Barreto, G., Schäfer, A., Marhold, J., Stach, D., Swaminathan, S. K., Handa, V., Doederlein, G., Maltry, N., Wu, W., Lyko, F., et al. (2007) · Nature · doi:10.1038/nature05515 · Cited by 758 · see citing works
Chen, T., Ueda, Y., Dodge, J. E., Wang, Z., & Li, E. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.16.5594-5605.2003 · Cited by 751 · see citing works
Self-citationLoss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation
Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E., et al. (2001) · Nature Genetics · doi:10.1038/83730 · Cited by 694 · see citing works
Jüttermann, R., Li, E., & Jaenisch, R. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11797 · Cited by 679 · see citing works
Self-citationA mammalian protein with specific demethylase activity for mCpG DNA
Bhattacharya, S. K., Ramchandani, S., Cervoni, N., & Moshe Szyf, A. (1999) · Nature · doi:10.1038/17533 · Cited by 616 · see citing works
Evidence That DNA (Cytosine-5) Methyltransferase Regulates Synaptic Plasticity in the Hippocampus
Levenson, J. M., Roth, T. L., Lubin, F. D., Miller, C. A., Huang, I.-C., Desai, P., Malone, L. M., & Sweatt, J. D. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m511767200 · Cited by 615 · see citing works
Self-citationCooperativity between DNA Methyltransferases in the Maintenance Methylation of Repetitive Elements
Liang, G., Chan, M. F., Tomigahara, Y., Tsai, Y., Gonzales, F. A., Li, E., Laird, P. W., & Jones, P. A. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.2.480-491.2002 · Cited by 570 · see citing works
Self-citationCalmodulin-kinases: modulators of neuronal development and plasticity.
Wayman, G. A., Lee, Y.-S., Tokumitsu, H., Silva, A., & Soderling, T. R. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.021 · Cited by 567 · see citing works
Self-citationHedgehog signaling and primary cilia are required for the formation of adult neural stem cells
Han, Y.-G., Spassky, N., Romaguera-Ros, M., Garcia-Verdugo, J.-M., Aguilar, A., Schneider-Maunoury, S., & Alvarez-Buylla, A. (2008) · Nature Neuroscience · doi:10.1038/nn2059 · Cited by 547 · see citing works
The Colorful History of Active DNA Demethylation
Ooi, S. K. T., & Bestor, T. H. (2008) · Cell · doi:10.1016/j.cell.2008.06.009 · Cited by 537 · see citing works
Fouse, S. D., Shen, Y., Pellegrini, M. A., Cole, S. W., Meissner, A., Neste, L. V., Jaenisch, R., & Fan, G. (2008) · Cell stem cell · doi:10.1016/j.stem.2007.12.011 · Cited by 452 · see citing works
Self-citationInduction of MHC Class I Genes in Neurons
Neumann, H., Cavalié, A., Jenne, D. E., & Wekerle, H. (1995) · Science · doi:10.1126/science.7624779 · Cited by 449 · see citing works
Bachman, K. E., Rountree, M. R., & Baylin, S. B. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104661200 · Cited by 438 · see citing works
DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling
Fan, G., Martinowich, K., Chin, M. H., He, F., Fouse, S. D., Hutnick, L. K., Hattori, D., Ge, W., Shen, Y., Wu, H., et al. (2005) · Development · doi:10.1242/dev.01912 · Cited by 420 · see citing works
Self-citationDynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system
Feng, J., Chang, H., Li, E., & Fan, G. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20404 · Cited by 401 · see citing works
Self-citationDNA Hypomethylation Perturbs the Function and Survival of CNS Neurons in Postnatal Animals
Fan, G., Beard, C., Chen, R. Z., Csankovszki, G., Sun, Y., Siniaia, M. S., Biniszkiewicz, D., Bates, B., Lee, P. P., Kühn, R., et al. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-03-00788.2001 · Cited by 368 · see citing works
Self-citationImmune signalling in neural development, synaptic plasticity and disease
Boulanger, L. M., & Shatz, C. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1428 · Cited by 334 · see citing works
DNA Methyltransferase Contributes to Delayed Ischemic Brain Injury
Endres, M., Meisel, A., Biniszkiewicz, D., Namura, S., Prass, K., Ruscher, K., Lipski, A., Jaenisch, R., Moskowitz, M. A., & Dirnagl, U. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03175.2000 · Cited by 310 · see citing works
EphB/syndecan-2 signaling in dendritic spine morphogenesis
Ethell, I. M., Irie, F., Kalo, M. S., Couchman, J. R., Pasquale, E. B., & Yamaguchi, Y. (2001) · Neuron · doi:10.1016/s0896-6273(01)00440-8 · Cited by 309 · see citing works
Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain.
Ouimet, C. C., McGuinness, T. L., & Greengard, P. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.17.5604 · Cited by 293 · see citing works
Neumann, H., Schmidt, H., Cavalié, A., Jenne, D. E., & Wekerle, H. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.2.305 · Cited by 288 · see citing works
Dodge, J. E., Okano, M., Dick, F. A., Tsujimoto, N., Chen, T., Wang, S., Ueda, Y., Dyson, N. J., & Li, E. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413246200 · Cited by 277 · see citing works
Self-citation[42] Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry
Crain, P. F. (1990) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(90)93450-y · Cited by 265 · see citing works
Epigenetic Regulation of Neural Gene Expression and Neuronal Function
Feng, J., Fouse, S. D., & Fan, G. (2007) · Pediatric Research · doi:10.1203/pdr.0b013e3180457635 · Cited by 263 · see citing works
Self-citationNelson, E. D., Kavalali, E. T., & Monteggia, L. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3796-07.2008 · Cited by 254 · see citing works
Song, L., James, S. R., Kazim, L., & Karpf, A. R. (2004) · Analytical Chemistry · doi:10.1021/ac0489420 · Cited by 242 · see citing works
Goto, K., Numata, M., Komura, J., Ono, T., Bestor, T. H., & Kondo, H. (1994) · Differentiation · doi:10.1046/j.1432-0436.1994.56120039.x · Cited by 235 · see citing works
Tropea, D., Kreiman, G., Lyckman, A., Mukherjee, S., Yu, H., Horng, S., & Sur, M. (2006) · Nature Neuroscience · doi:10.1038/nn1689 · Cited by 226 · see citing works
Nguyen, S. P., Meletis, K., Fu, D., Jhaveri, S., & Jaenisch, R. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21176 · Cited by 195 · see citing works
Isolation of neuronal chromatin from brain tissue
Jiang, Y., Matevossian, A., Huang, H.-S., Straubhaar, J., & Akbarian, S. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-42 · Cited by 193 · see citing works
Hutnick, L. K., Golshani, P., Namihira, M., Xue, Z., Matynia, A., Yang, X. W., Silva, A. J., Schweizer, F. E., & Fan, G. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp222 · Cited by 181 · see citing works
Self-citationInteractions between the NR2B Receptor and CaMKII Modulate Synaptic Plasticity and Spatial Learning
Zhou, Y., Takahashi, E., Li, W., Halt, A., Wiltgen, B., Ehninger, D., Li, G.-D., Hell, J. W., Kennedy, M. B., & Silva, A. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4486-07.2007 · Cited by 179 · see citing works
Self-citationLu, X., Fleming, S. M., Meurers, B. H., Ackerson, L. C., Mortazavi, F., Lo, V., Hernandez, D., Sulzer, D., Jackson, G. R., Maidment, N. T., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5351-08.2009 · Cited by 177 · see citing works
DNA excision repair proteins and Gadd45 as molecular players for active DNA demethylation
Dengke, K., Guo, J. U., Ming, G., & Song, H. (2009) · Cell Cycle · doi:10.4161/cc.8.10.8500 · Cited by 171 · see citing works
Neuronal plasticity and cellular immunity: shared molecular mechanisms
Boulanger, L. M., Huh, G. S., & Shatz, C. J. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00251-8 · Cited by 171 · see citing works
DNA mismatch repair and DNA methylation in adult brain neurons
Brooks, P. J., Marietta, C. A., & Goldman, D. A. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-03-00939.1996 · Cited by 145 · see citing works
Epigenetic Mechanisms and Gene Networks in the Nervous System
Colvis, C. M., Pollock, J. D., Goodman, R. H., Impey, S., Dunn, J. J., Mandel, G., Champagne, F. A., Mayford, M. R., Korzus, E., Kumar, A., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4119-05.2005 · Cited by 139 · see citing works
Epigenetic regulation of X-linked cancer/germline antigen genes by DNMT1 and DNMT3b
James, S. R., Link, P. A., & Karpf, A. R. (2006) · Oncogene · doi:10.1038/sj.onc.1209678 · Cited by 120 · see citing works
Effects of cerebral ischemia in mice lacking DNA methyltransferase 1 in post-mitotic neurons
Endres, M., Fan, G., Meisel, A., Dirnagl, U., & Jaenisch, R. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00032 · Cited by 111 · see citing works
Self-citationC1q: the perfect complement for a synaptic feast?
Perry, V. H., & O'Connor, V. M. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2394 · Cited by 101 · see citing works
Inano, K., Suetake, I., Ueda, T., Miyake, Y., Nakamura, M., Okada, M., & Tajima, S. (2000) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a022755 · Cited by 99 · see citing works
Epigenome Sequencing Comes of Age
Zhu, J. (2008) · Cell · doi:10.1016/j.cell.2008.04.016 · Cited by 78 · see citing works
Golshani, P., Hutnick, L. K., Schweizer, F. E., & Fan, G. (2005) · Thalamus & Related Systems · doi:10.1017/s1472928807000222 · Cited by 77 · see citing works
Self-citationReduced hippocampal neurogenesis and skill reaching performance in adult Emx1 mutant mice
Hong, S. M., Liu, Z., Fan, Y., Neumann, M., Won, S. J., Lac, D., Lum, X., Weinstein, P. R., & Liu, J. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.03.028 · Cited by 44 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
DNA methylation and its basic function
Moore, L. D., Le, T., & Fan, G. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.112 · Cited by 4,906 · see citing works
Self-citationGlobal epigenomic reconfiguration during mammalian brain development
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., Lucero, J., Huang, Y., Dwork, A. J., Schultz, M. D., et al. (2013) · Science · doi:10.1126/science.1237905 · Cited by 1,830 · see citing works
Reversing DNA Methylation: Mechanisms, Genomics, and Biological Functions
Wu, H., & Zhang, Y. (2014) · Cell · doi:10.1016/j.cell.2013.12.019 · Cited by 1,065 · see citing works
In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9
Swiech, L., Heidenreich, M., Banerjee, A., Habib, N., Li, Y., Trombetta, J., Sur, M., & Zhang, F. (2015) · Nature Biotechnology · doi:10.1038/nbt.3055 · Cited by 772 · see citing works
Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain
Guo, J. U., Su, Y., Shin, J. H., Shin, J., Li, H., Xie, B., Zhong, C., Hu, S., Le, T., Fan, G., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3607 · Cited by 714 · see citing works
Self-citationNeuronal activity modifies the DNA methylation landscape in the adult brain
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2900 · Cited by 669 · see citing works
Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens
LaPlant, Q., Vialou, V., Covington, H. E., Dumitriu, D., Feng, J., Warren, B. L., Maze, I., Dietz, D. M., Watts, E. L., Iñiguez, S. D., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2619 · Cited by 612 · see citing works
Self-citationPathogenesis of depression: Insights from human and rodent studies
Ménard, C., Hodes, G. E., & Russo, S. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.053 · Cited by 593 · see citing works
Immune mediators in the brain and peripheral tissues in autism spectrum disorder
Estes, M. L., & McAllister, A. K. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3978 · Cited by 514 · see citing works
Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513 · see citing works
Epigenetic mechanisms in cognition
Day, J. J., & Sweatt, J. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.019 · Cited by 510 · see citing works
Self-citationKundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490 · see citing works
High levels of AAV vector integration into CRISPR-induced DNA breaks
Hanlon, K. S., Kleinstiver, B. P., Garcia, S. P., Zaborowski, M. P., Volak, A., Spirig, S. E., Muller, A., Sousa, A. A., Tsai, S. Q., Bengtsson, N. E., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12449-2 · Cited by 431 · see citing works
Resilience in mental health: linking psychological and neurobiological perspectives.
Rutten, B. P. F., Hammels, C., Geschwind, N., Menne‐Lothmann, C., Pishva, E., Schruers, K., van den Hove, D., Kenis, G., van Os, J., & Wichers, M. (2013) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12095 · Cited by 418 · see citing works
Hodes, G. E., Pfau, M. L., Purushothaman, I., Ahn, H. F., Golden, S. A., Christoffel, D. J., Magida, J., Brancato, A., Takahashi, A., Flanigan, M. E., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1392-15.2015 · Cited by 395 · see citing works
Self-citationThe epigenetics of aging and neurodegeneration
Lardenoije, R., Iatrou, A., Kenis, G., Kompotis, K., Steinbusch, H. W. M., Mastroeni, D., Coleman, P., Lemere, C. A., Hof, P. R., van den Hove, D. L. A., et al. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.05.002 · Cited by 381 · see citing works
Genetic and Epigenetic Networks in Intellectual Disabilities
van Bokhoven, H. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132512 · Cited by 382 · see citing works
Epigenetic regulation of gene expression in physiological and pathological brain processes
Gräff, J., Kim, D., Dobbin, M. M., & Tsai, L.-H. (2011) · Physiological Reviews · doi:10.1152/physrev.00012.2010 · Cited by 373 · see citing works
Gomez‐Pinilla, F., Zhuang, Y., Feng, J., Ying, Z., & Fan, G. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07508.x · Cited by 367 · see citing works
DNA methylation signatures in development and aging of the human prefrontal cortex
Numata, S., Ye, T., Hyde, T. M., Guitart-Navarro, X., Tao, R., Wininger, M., Colantuoni, C., Weinberger, D. R., Kleinman, J. E., & Lipska, B. K. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.12.020 · Cited by 364 · see citing works
The Emerging Field of Neuroepigenetics
Sweatt, J. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.023 · Cited by 324 · see citing works
Self-citationDNA methylation analysis of the autistic brain reveals multiple dysregulated biological pathways
Nardone, S., Sharan Sams, D., Reuveni, E., Getselter, D., Oron, O., Karpuj, M., & Elliott, E. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.70 · Cited by 266 · see citing works
Epigenetic Mechanisms of Depression and Antidepressant Action
Vialou, V., Feng, J., Robison, A. J., & Nestler, E. J. (2013) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134540 · Cited by 277 · see citing works
Self-citationKinde, B., Gabel, H. W., Gilbert, C. S., Griffith, E. C., & Greenberg, M. E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411269112 · Cited by 236 · see citing works
Kratsman, N., Getselter, D., & Elliott, E. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.11.003 · Cited by 239 · see citing works
Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond
Guo, J. U., Su, Y., Zhong, C., Ming, G.-L., & Song, H. (2011) · Cell Cycle · doi:10.4161/cc.10.16.17093 · Cited by 235 · see citing works
An epigenetic framework for neurodevelopmental disorders: From pathogenesis to potential therapy
Millan, M. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.11.015 · Cited by 229 · see citing works
Epigenetic Regulation of Learning and Memory by Drosophila EHMT/G9a
Kramer, J. M., Kochinke, K., Oortveld, M. A. W., Marks, H., Kramer, D., de Jong, E. K., Asztalos, Z., Westwood, J. T., Stunnenberg, H. G., Sokolowski, M. B., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000569 · Cited by 204 · see citing works
Epigenetics and the regulation of stress vulnerability and resilience
Zannas, A. S., & West, A. E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.003 · Cited by 211 · see citing works
Stefanska, B., Karlic, H., Varga, F., Fabianowska‐Majewska, K., & Haslberger, A. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02002.x · Cited by 200 · see citing works
Iwamoto, K., Bundo, M., Ueda, J., Oldham, M. C., Ukai, W., Hashimoto, E., Saito, T., Geschwind, D. H., & Kato, T. (2011) · Genome Research · doi:10.1101/gr.112755.110 · Cited by 189 · see citing works
DNA methylation in social insects: how epigenetics can control behavior and longevity
Yan, H., Bonasio, R., Simola, D. F., Liebig, J., Berger, S. L., & Reinberg, D. (2015) · Annual Review of Entomology · doi:10.1146/annurev-ento-010814-020803 · Cited by 183 · see citing works
Blanch, M., Mosquera, J. L., Ansoleaga, B., Ferrer, I., & Barrachina, M. (2016) · The American Journal of Pathology · doi:10.1016/j.ajpath.2015.10.004 · Cited by 192 · see citing works
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Szyf, M. (2011) · Epigenetics · doi:10.4161/epi.6.8.16793 · Cited by 161 · see citing works
Melas, P. A., Rogdaki, M., Lennartsson, A., Björk, K., Qi, H., Witasp, A., Werme, M., Wegener, G., Mathé, A. A., Svenningsson, P., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711000940 · Cited by 157 · see citing works
Schneider, J. S., Kidd, S. K., & Anderson, D. W. (2013) · Toxicology Letters · doi:10.1016/j.toxlet.2012.12.004 · Cited by 115 · see citing works
DNA methylation regulates neuronal glutamatergic synaptic scaling
Meadows, J. P., Guzman-Karlsson, M. C., Phillips, S., Holleman, C., Posey, J. L., Day, J. J., Hablitz, J. J., & Sweatt, J. D. (2015) · Science Signaling · doi:10.1126/scisignal.aab0715 · Cited by 111 · see citing works
Self-citationEpigenetic memory: The Lamarckian brain
Fischer, A. (2014) · The EMBO Journal · doi:10.1002/embj.201387637 · Cited by 107 · see citing works
Global DNA Hypermethylation in Down Syndrome Placenta
Jin, S., Lee, Y. K., Lim, Y. C., Zheng, Z., Lin, X. M., Ng, D. P. Y., Holbrook, J. D., Law, H. Y., Kwek, K. Y. C., Yeo, G. S. H., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003515 · Cited by 99 · see citing works
Epigenomic strategies at the interface of genetic and environmental risk factors for autism
LaSalle, J. M. (2013) · Journal of Human Genetics · doi:10.1038/jhg.2013.49 · Cited by 95 · see citing works
Iron deficiency on neuronal function
Muñoz, P., & Humeres, A. (2012) · BioMetals · doi:10.1007/s10534-012-9550-x · Cited by 92 · see citing works
Chouliaras, L., L.A. van den Hove, D., Kenis, G., Keitel, S., R. Hof, P., van Os, J., W.M. Steinbusch, H., Schmitz, C., & P.F. Rutten, B. (2012) · Current Alzheimer Research · doi:10.2174/156720512800618035 · Cited by 91 · see citing works
Caloric restriction attenuates age-related changes of DNA methyltransferase 3a in mouse hippocampus
Chouliaras, L., van den Hove, D. L. A., Kenis, G., Dela Cruz, J., Lemmens, M. A. M., van Os, J., Steinbusch, H. W. M., Schmitz, C., & Rutten, B. P. F. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.11.016 · Cited by 89 · see citing works
Epigenetic mechanisms in fear conditioning: Implications for treating post-traumatic stress disorder
Kwapis, J. L., & Wood, M. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.005 · Cited by 87 · see citing works
Prevention of age-related changes in hippocampal levels of 5-methylcytidine by caloric restriction
Chouliaras, L., van den Hove, D. L. A., Kenis, G., Keitel, S., Hof, P. R., van Os, J., Steinbusch, H. W. M., Schmitz, C., & Rutten, B. P. F. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.06.003 · Cited by 78 · see citing works
Epigenetics, a key for unlocking complex CNS disorders? Therapeutic implications
Szyf, M. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.01.009 · Cited by 76 · see citing works
DNA Methylation and Its Implications and Accessibility for Neuropsychiatric Therapeutics
Day, J. J., Kennedy, A. J., & Sweatt, J. D. (2015) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124527 · Cited by 78 · see citing works
Self-citationWilliamson, C. M., Franks, B., & Curley, J. P. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00152 · Cited by 64 · see citing works
Tet1 in Nucleus Accumbens Opposes Depression- and Anxiety-Like Behaviors
Feng, J., Pena, C. J., Purushothaman, I., Engmann, O., Walker, D., Brown, A. N., Issler, O., Doyle, M., Harrigan, E., Mouzon, E., et al. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.6 · Cited by 58 · see citing works
Self-citationEpigenome-Wide Association Study of Cognitive Functioning in Middle-Aged Monozygotic Twins
Starnawska, A., Tan, Q., McGue, M., Mors, O., Børglum, A. D., Christensen, K., Nyegaard, M., & Christiansen, L. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00413 · Cited by 54 · see citing works
Role of MeCP2, DNA methylation, and HDACs in regulating synapse function
Kavalali, E. T., Nelson, E. D., & Monteggia, L. M. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9078-3 · Cited by 46 · see citing works
Single-Neuron Transcriptome and Methylome Sequencing for Epigenomic Analysis of Aging
Moroz, L. L., & Kohn, A. B. (2013) · Methods in Molecular Biology · doi:10.1007/978-1-62703-556-9_21 · Cited by 42 · see citing works
Warita, K., Mitsuhashi, T., Ohta, K.-I., Suzuki, S., Hoshi, N., Miki, T., & Takeuchi, Y. (2013) · The Journal of Toxicological Sciences · doi:10.2131/jts.38.285 · Cited by 41 · see citing works
Colquitt, B. M., Markenscoff-Papadimitriou, E., Duffié, R., & Lomvardas, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.013 · Cited by 38 · see citing works
Ciuculete, D. M., Voisin, S., Kular, L., Jonsson, J., Rask-Andersen, M., Mwinyi, J., & Schiöth, H. B. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00884-8 · Cited by 35 · see citing works
DNA Methyltransferases in Depression: An Update
Duan, Z., & Lu, J. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.538683 · Cited by 32 · see citing works
DNA Epigenetics in Addiction Susceptibility
Kaplan, G., Xu, H., Abreu, K., & Feng, J. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.806685 · Cited by 34 · see citing works
Self-citationScott, H., Smith, A. E., Barker, G. R., Uney, J. B., & Warburton, E. C. (2017) · Neuroepigenetics · doi:10.1016/j.nepig.2017.02.001 · Cited by 18 · see citing works
Nagakura, I., Van Wart, A., Petravicz, J., Tropea, D., & Sur, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0189-14.2014 · Cited by 18 · see citing works
Todorov, G., Mayilvahanan, K., Ashurov, D., & Cunha, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-45325-6 · Cited by 11 · see citing works
Retracted
- Authors
- Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., Silva, A. J., & Fan, G.
- Affiliations
- University of California, Los Angeles (US)
- Qingdao University (CN)
- University of Alabama at Birmingham (US)
- Corresponding author
- Fan, Guoping
- Venue
- Nature Neuroscience
- Published
- 2010-03-14
- Volume
- 13
- Issue
- 4
- Pages
- 423-430
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3060772
- OpenAlex
- W2115818350
- Cited by
- 1,019
- References
- 66
- Citations by year
- 2026: 23 · 2025: 51 · 2024: 37 · 2023: 38 · 2022: 52 · 2021: 63 · 2020: 58 · 2019: 69 · 2018: 54 · 2017: 79 · 2016: 84 · 2015: 72 · 2014: 83 · 2013: 84 · 2012: 75
- FWCI
- 33.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG031722, R37AG013622, R01AG013622, R01AG031722)
- National Institute of Mental Health (P50-MH0779720, MH 57014, R01MH057014, P50MH077972)
- National Institute of Neurological Disorders and Stroke (NS 057098, R01NS051411, R56NS051411, P30NS057098)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- DNMT1, DNMT3A, DNA methylation, synaptic plasticity, learning and memory, hippocampal CA1, excitatory neurons, postmitotic neurons, conditional knockout mice, neuronal gene expression, MHC class I, STAT1, epigenetics
- MeSH terms
- DNA (Cytosine-5-)-Methyltransferase 1, DNA Methyltransferase 3A, Age Factors, Animals, Cells, Cultured, DNA (Cytosine-5-)-Methyltransferases, Female, Learning, Male, Memory, Mice, Transgenic, Neuronal Plasticity, Neurons, Synapses, Prosencephalon, Mice, Knockout, Gene Expression Regulation, Developmental, DNA Methylation, Mice
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