Epigenetic Regulation of Learning and Memory by Drosophila EHMT/G9a
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The epigenetic modification of chromatin structure and its effect on complex neuronal processes like learning and memory is an emerging field in neuroscience. However, little is known about the "writers" of the neuronal epigenome and how they lay down the basis for proper cognition. Here, we have dissected the neuronal function of the Drosophila euchromatin histone methyltransferase (EHMT), a member of a conserved protein family that methylates histone 3 at lysine 9 (H3K9). EHMT is widely expressed in the nervous system and other tissues, yet EHMT mutant flies are viable. Neurodevelopmental and behavioral analyses identified EHMT as a regulator of peripheral dendrite development, larval locomotor behavior, non-associative learning, and courtship memory. The requirement for EHMT in memory was mapped to 7B-Gal4 positive cells, which are, in adult brains, predominantly mushroom body neurons. Moreover, memory was restored by EHMT re-expression during adulthood, indicating that cognitive defects are reversible in EHMT mutants. To uncover the underlying molecular mechanisms, we generated genome-wide H3K9 dimethylation profiles by ChIP-seq. Loss of H3K9 dimethylation in EHMT mutants occurs at 5% of the euchromatic genome and is enriched at the 5' and 3' ends of distinct classes of genes that control neuronal and behavioral processes that are corrupted in EHMT mutants. Our study identifies Drosophila EHMT as a key regulator of cognition that orchestrates an epigenetic program featuring classic learning and memory genes. Our findings are relevant to the pathophysiological mechanisms underlying Kleefstra Syndrome, a severe form of intellectual disability caused by mutations in human EHMT1, and have potential therapeutic implications. Our work thus provides novel insights into the epigenetic control of cognition in health and disease.
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In Drosophila, ehmt coordinates epigenetic changes important in regulating cognition.
“Intriguingly, in Drosophila, ehmt coordinates epigenetic changes important in regulating cognition.33”
From De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia (2012) · cites this paper as [33]
In Drosophila, the orthologue of DLG2 (dlg1) is directly regulated by the orthologue of EHMT1 (ehmt/G9a).
“Remarkably, the orthologue of DLG2 in Drosophila (dlg1) is directly regulated by the orthologue of EHMT1 (emht also known as G9a).33”
From De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia (2012) · cites this paper as [33]
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Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510 · see citing works
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845 · see citing works
Habituation: a model phenomenon for the study of neuronal substrates of behavior
Thompson, R. F., & Spencer, W. A. (1966) · Psychological Review · doi:10.1037/h0022681 · Cited by 2,608 · cited 1× · see citing works
“Habituation is a form of non-associative learning where an initial response to a repeated stimulus gradually wanes [26].”
BackgroundTachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., Fukuda, M., Takeda, N., Niida, H., Kato, H., et al. (2002) · Genes & Development · doi:10.1101/gad.989402 · Cited by 1,261 · see citing works
Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons
Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., Silva, A. J., & Fan, G. (2010) · Nature Neuroscience · doi:10.1038/nn.2514 · Cited by 1,019 · see citing works
Tachibana, M., Ueda, J., Fukuda, M., Takeda, N., Ohta, T., Iwanari, H., Sakihama, T., Kodama, T., Hamakubo, T., & Shinkai, Y. (2005) · Genes & Development · doi:10.1101/gad.1284005 · Cited by 853 · see citing works
A Complex with Chromatin Modifiers That Occupies E2F- and Myc-Responsive Genes in G 0 Cells
Ogawa, H., Ishiguro, K., Gaubatz, S., Livingston, D. M., & Nakatani, Y. (2002) · Science · doi:10.1126/science.1069861 · Cited by 769 · see citing works
A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genomePreprint
Mavrich, T. N., Ioshikhes, I. P., Venters, B. J., Jiang, C., Tomsho, L. P., Qi, J., Schuster, S. C., Albert, I. U., & Pugh, B. F. (2008) · Genome Research · doi:10.1101/gr.078261.108 · Cited by 673 · see citing works
Dnmt3a-Dependent Nonpromoter DNA Methylation Facilitates Transcription of Neurogenic Genes
Wu, H., Coskun, V., Tao, J., Xie, W., Ge, W., Yoshikawa, K., Li, E., Zhang, Y., & Sun, Y. E. (2010) · Science · doi:10.1126/science.1190485 · Cited by 604 · see citing works
Advances in the Treatment of Fragile X Syndrome
Hagerman, R. J., Berry-Kravis, E., Kaufmann, W. E., Ono, M. Y., Tartaglia, N., Lachiewicz, A., Kronk, R., Delahunty, C., Hessl, D., Visootsak, J., et al. (2009) · Pediatrics · doi:10.1542/peds.2008-0317 · Cited by 596 · see citing works
Tiling of theDrosophilaepidermis by multidendritic sensory neurons
Grueber, W. B., Jan, L. Y., & Jan, Y. N. (2002) · Development · doi:10.1242/dev.129.12.2867 · Cited by 589 · see citing works
Histone Methylation Regulates Memory Formation
Gupta, S., Kim, S. Y., Artis, S., Molfese, D. L., Schumacher, A., Sweatt, J. D., Paylor, R. E., & Lubin, F. D. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3732-09.2010 · Cited by 562 · see citing works
Robinow, S., & White, K. (1991) · Journal of Neurobiology · doi:10.1002/neu.480220503 · Cited by 507 · see citing works
Conditioned responses in courtship behavior of normal and mutant Drosophila
Siegel, R. W., & Hall, J. C. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.7.3430 · Cited by 488 · see citing works
McBride, S. M. J., Choi, C. H., Wang, Y., Liebelt, D. A., Braunstein, E. M., Ferreiro, D., Sehgal, A., Siwicki, K. K., Dockendorff, T. C., Nguyen, H. T., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.038 · Cited by 473 · see citing works
Kleefstra, T., Brunner, H. G., Amiel, J., Oudakker, A. R., Nillesen, W. M., Magee, A. C., Geneviève, D., Cormier‐Daire, V., Esch, H. V., Fryns, J., et al. (2006) · The American Journal of Human Genetics · doi:10.1086/505693 · Cited by 395 · see citing works
GOToolBox: functional analysis of gene datasets based on Gene Ontology
Martin, D. P., Brun, C., Rémy, É., Mouren, P., Thieffry, D., & Jacq, B. (2004) · Genome biology · doi:10.1186/gb-2004-5-12-r101 · Cited by 387 · see citing works
Two strategies for gene regulation by promoter nucleosomesPreprint
Tirosh, I., & Barkai, N. (2008) · Genome Research · doi:10.1101/gr.076059.108 · Cited by 383 · see citing works
Gene loops juxtapose promoters and terminators in yeast
O'Sullivan, J. M., Tan‐Wong, S. M., Morillon, A., Lee, B., Coles, J., Mellor, J., & Proudfoot, N. J. (2004) · Nature Genetics · doi:10.1038/ng1411 · Cited by 346 · see citing works
Sequence Finishing and Mapping of Drosophila melanogaster Heterochromatin
Hoskins, R. A., Carlson, J. W., Kennedy, C., Acevedo, D., Evans-Holm, M. E., Frise, E., Wan, K. H., Park, S. H., Méndez-Lago, M., Rossi, F., et al. (2007) · Science · doi:10.1126/science.1139816 · Cited by 318 · see citing works
Control of Cognition and Adaptive Behavior by the GLP/G9a Epigenetic Suppressor Complex
Schaefer, A., Sampath, S. C., Intrator, A., Min, A., Gertler, T. S., Surmeier, D. J., Tarakhovsky, A., & Greengard, P. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.019 · Cited by 317 · see citing works
Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J.-L., & Giangrande, A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00354-4 · Cited by 316 · see citing works
Self-citationGrueber, W. B., Jan, L. Y., & Jan, Y. N. (2003) · Cell · doi:10.1016/s0092-8674(03)00160-0 · Cited by 315 · see citing works
Foraging strategies ofDrosophila melanogaster: A chromosomal analysis
Sokolowski, M. B. (1980) · Behavior Genetics · doi:10.1007/bf01067774 · Cited by 312 · see citing works
Self-citationLocalized Domains of G9a-Mediated Histone Methylation Are Required for Silencing of Neuronal Genes
Roopra, A., Qazi, R., Schoenike, B. A., Daley, T. J., & Morrison, J. F. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.05.026 · Cited by 282 · see citing works
Function of the Drosophila CPEB protein Orb2 in long-term courtship memory
Keleman, K., Krüttner, S., Alenius, M., & Dickson, B. J. (2007) · Nature Neuroscience · doi:10.1038/nn1996 · Cited by 266 · see citing works
Self-citationMcBride, S. M. J., Giuliani, G., Choi, C. H., Krause, P., Correale, D., Watson, K. K., Baker, G., & Siwicki, K. K. (1999) · Neuron · doi:10.1016/s0896-6273(00)81043-0 · Cited by 261 · see citing works
Tan‐Wong, S. M., Wijayatilake, H. D., & Proudfoot, N. J. (2009) · Genes & Development · doi:10.1101/gad.1823209 · Cited by 260 · see citing works
Campbell, G. L., Göring, H. H. H., Lin, T., Spana, E. P., Andersson, S. G. E., Doe, C. Q., & Tomlinson, A. (1994) · Development · doi:10.1242/dev.120.10.2957 · Cited by 257 · see citing works
Identification of small molecules rescuing fragile X syndrome phenotypes in Drosophila
Chang, S., Bray, S. M., Li, Z., Zarnescu, D. C., He, C., Jin, P., & Warren, S. T. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.78 · Cited by 254 · see citing works
Kleefstra, T., van Zelst-Stams, W. A., Nillesen, W. M., Cormier-Daire, V, Houge, G., Foulds, N., van Dooren, M., Willemsen, M. H., Pfundt, R., Turner, A., et al. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2008.062950 · Cited by 252 · see citing works
Mediator Links Epigenetic Silencing of Neuronal Gene Expression with X-Linked Mental Retardation
Ding, N., Zhou, H., Estève, P., Chin, H. G., Kim, S., Xu, X., Joseph, S., Friez, M. J., Schwartz, C. E., Pradhan, S., et al. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.023 · Cited by 238 · see citing works
Self-citationOpen-Label Treatment Trial of Lithium to Target the Underlying Defect in Fragile X Syndrome
Berry-Kravis, E., Sumis, A., Hervey, C., Nelson, M., Porges, S. W., Weng, N., Weiler, I. J., & Greenough, W. T. (2008) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e31817dc447 · Cited by 215 · see citing works
Genetic Feminization of Pheromones and Its Behavioral Consequences in Drosophila Males
Ferveur, J., Savarit, F., O’Kane, C. J., Sureau, G., Greenspan, R. J., & Jallon, J. M. (1997) · Science · doi:10.1126/science.276.5318.1555 · Cited by 213 · see citing works
Enhanced Locomotion Caused by Loss of the Drosophila DEG/ENaC Protein Pickpocket1
Ainsley, J. A., Pettus, J. M., Bosenko, D. V., Gerstein, C. E., Zinkevich, N. S., Anderson, M. G., Adams, C. M., Welsh, M. J., & Johnson, W. A. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00596-7 · Cited by 204 · see citing works
Kleefstra, T., Smidt, M. P., Banning, M. J. G., Oudakker, A. R., Esch, H. V., de Brouwer, A. P. M., Nillesen, W., Sistermans, E. A., Hamel, B. C. J., de Bruijn, D., et al. (2005) · Journal of Medical Genetics · doi:10.1136/jmg.2004.028464 · Cited by 198 · see citing works
Reversing Neurodevelopmental Disorders in Adults
Ehninger, D., Li, W., Fox, K., Stryker, M. P., & Silva, A. J. (2008) · Neuron · doi:10.1016/j.neuron.2008.12.007 · Cited by 196 · see citing works
A Transcription-Independent Role for TFIIB in Gene Looping
Singh, B. N., & Hampsey, M. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.07.013 · Cited by 174 · see citing works
Song, W., Onishi, M., Jan, L. Y., & Jan, Y. N. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700895104 · Cited by 169 · see citing works
Nishio, H., & Walsh, M. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401343101 · Cited by 150 · see citing works
Dynamic interactions between the promoter and terminator regions of the mammalian BRCA1 gene
Tan‐Wong, S. M., French, J. D., Proudfoot, N. J., & Brown, M. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801048105 · Cited by 146 · see citing works
High-resolution analysis of epigenetic changes associated with X inactivationPreprint
Marks, H., Chow, J., Denissov, S., Françoijs, K., Brockdorff, N., Heard, É., & Stunnenberg, H. G. (2009) · Genome Research · doi:10.1101/gr.092643.109 · Cited by 140 · see citing works
Self-citationA physiological role for gene loops in yeastPreprint
Lainé, J., Singh, B. N., Krishnamurthy, S., & Hampsey, M. (2009) · Genes & Development · doi:10.1101/gad.1823609 · Cited by 140 · see citing works
Regulation of chromatin structure in memory formation
Roth, T. L., & Sweatt, J. D. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.011 · Cited by 138 · see citing works
Altered Habituation of an Identified Escape Circuit inDrosophilaMemory Mutants
Engel, J. E., & Wu, C. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03486.1996 · Cited by 137 · see citing works
The epigenetic bottleneck of neurodegenerative and psychiatric diseases
Sananbenesi, F., & Fischer, A. (2009) · Biological Chemistry · doi:10.1515/bc.2009.131 · Cited by 106 · see citing works
Rho-linked genes and neurological disorders
Kasri, N. N., & Aelst, L. V. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0385-1 · Cited by 103 · see citing works
Oncogenes on my mind: ERK and MTOR signaling in cognitive diseases.
Krab, L. C., Goorden, S., & Elgersma, Y. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.07.005 · Cited by 93 · see citing works
Global effects of histone modifications
He, H. (2003) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/2.3.234 · Cited by 86 · see citing works
Brower-Toland, B., Riddle, N. C., Jiang, H., Huisinga, K. L., & Elgin, S. C. R. (2009) · Genetics · doi:10.1534/genetics.108.100271 · Cited by 86 · see citing works
Subtelomeric deletions of chromosome 9q: A novel microdeletion syndrome
Stewart, D. R., Huang, A., Faravelli, F., Anderlid, B., Medne, L., Ciprero, K. L., Kaur, M., Rossi, E. G., Tenconi, R., Nordenskjöld, M., et al. (2004) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.30136 · Cited by 75 · see citing works
Trimarchi, J. R., & Schneiderman, A. M. (1995) · Journal of Experimental Biology · doi:10.1242/jeb.198.5.1099 · Cited by 66 · see citing works
Neurogenetic approaches to habituation and dishabituation in Drosophila
Engel, J. E., & Wu, C. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.08.003 · Cited by 66 · see citing works
Stabell, M., Eskeland, R., Bjørkmo, M., Larsson, J., Aalen, R. B., Imhof, A., & Lambertsson, A. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl640 · Cited by 61 · see citing works
Mis, J., Ner, S. S., & Grigliatti, T. A. (2006) · Molecular Genetics and Genomics · doi:10.1007/s00438-006-0116-x · Cited by 61 · see citing works
Overlapping pathways dictate termination of RNA polymerase II transcription
Lykke‐Andersen, S., & Jensen, T. H. (2007) · Biochimie · doi:10.1016/j.biochi.2007.05.007 · Cited by 56 · see citing works
Disruption of the epigenetic code: An emerging mechanism in mental retardation
van Bokhoven, H., & Kramer, J. M. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.03.010 · Cited by 56 · see citing works
Self-citationO’Reilly, D., & Greaves, D. R. (2007) · Genomics · doi:10.1016/j.ygeno.2007.04.010 · Cited by 51 · see citing works
Ainsley, J. A., Kim, M., Wegman, L. J., Pettus, J. M., & Johnson, W. A. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.07.003 · Cited by 50 · see citing works
Drosophila G9a Is a Nonessential Gene
Seum, C., Bontron, S., Reo, E., Delattre, M., & Spierer, P. (2007) · Genetics · doi:10.1534/genetics.107.078220 · Cited by 40 · see citing works
Neal, S. J., Gibson, M., So, A. K.-C., & Westwood, J. T. (2003) · Genome · doi:10.1139/g03-056 · Cited by 36 · see citing works
Self-citationnemy encodes a cytochrome b561 that is required for Drosophila learning and memory
Iliadi, K. G., Avivi, A., Iliadi, N. N., Knight, D., Korol, A. B., Nevo, E., Taylor, P. P., Moran, M. F., Камышев, Н. Г., & Boulianne, G. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810698105 · Cited by 35 · see citing works
Manipulating the brain with epigenetics
Korzus, E. (2010) · Nature Neuroscience · doi:10.1038/nn0410-405 · Cited by 32 · see citing works
benFunctions withScampduring Synaptic Transmission and Long-Term Memory Formation inDrosophila
Zhao, H., Zheng, X., Yuan, X., Wang, L., Wang, X., Zhong, Y., Xie, Z., & Tully, T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5036-07.2009 · Cited by 15 · see citing works
Chapter 16 Measuring mRNA Stability During Early Drosophila Embryogenesis
Semotok, J. L., Westwood, J. T., Goldman, A. L., Cooperstock, R. L., & Lipshitz, H. D. (2008) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(08)02616-5 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Kirov, G., Pocklington, A. J., Holmans, P., Ivanov, D., Ikeda, M., Ruderfer, D., Moran, J., Chambert, K., Toncheva, D., Georgieva, L., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.154 · Cited by 844 · see citing works
“33 Our findings at this locus thus suggest a role for epigenetic mechanisms in at least some cases of schizophrenia, and potentially point the way to novel therapeutic opportunities as the developmental effects of ehmt mutation on cognition are reversible.”
BackgroundStessman, H. A. F., Xiong, B., Coe, B. P., Wang, T., Hoekzema, K., Fenckova, M., Kvarnung, M., Gerdts, J., Trinh, S., Cosemans, N., et al. (2017) · Nature Genetics · doi:10.1038/ng.3792 · Cited by 559 · see citing works
Self-citationH3K9 methyltransferase G9a and the related molecule GLPPreprint
Shinkai, Y., & Tachibana, M. (2011) · Genes & Development · doi:10.1101/gad.2027411 · Cited by 557 · 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 memory formation and maintenancePreprint
Zovkic, I. B., Karlsson, M. G., & Sweatt, J. D. (2013) · Learning & Memory · doi:10.1101/lm.026575.112 · Cited by 362 · see citing works
The Role of Histone Acetylation in Memory Formation and Cognitive Impairments
Peixoto, L., & Abel, T. G. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.86 · Cited by 336 · see citing works
SET for life: biochemical activities and biological functions of SET domain-containing proteins
Herz, H.-M., Garruss, A., & Shilatifard, A. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.09.004 · Cited by 314 · see citing works
Disruption of an EHMT1-Associated Chromatin-Modification Module Causes Intellectual Disability
Kleefstra, T., Kramer, J. M., Neveling, K., Willemsen, M. H., Koemans, T. S., Vissers, L. E. L. M., Wissink-Lindhout, W. M., Fencková, M., van den Akker, W. M. R., Kasri, N. N., et al. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.05.003 · Cited by 264 · see citing works
Self-citationIntellectual disability and autism spectrum disorders: Causal genes and molecular mechanisms
Srivastava, A. K., & Schwartz, C. E. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.02.015 · Cited by 251 · 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 Autophagy by the Methyltransferase G9a
de Narvajas, A. A.-M., Gomez, T. S., Zhang, J., Mann, A. O., Taoda, Y., Gorman, J. A., Herreros‐Villanueva, M., Gress, T. M., Ellenrieder, V., Bujanda, L., et al. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00813-13 · Cited by 217 · see citing works
Targeting histone lysine methylation in cancer
McGrath, J. P., & Trojer, P. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.01.002 · Cited by 188 · see citing works
Willemsen, M. H., Vulto-van Silfhout, A. T., Nillesen, W. M., Wissink-Lindhout, W. M., van Bokhoven, H., Philip, N., Berry-Kravis, E. M., Kini, U., van Ravenswaaij-Arts, C. M. A., Delle Chiaie, B., et al. (2011) · Molecular Syndromology · doi:10.1159/000335648 · Cited by 185 · see citing works
Inhibition of EHMT1/2 rescues synaptic and cognitive functions for Alzheimer’s disease
Zheng, Y., Liu, A., Wang, Z.-J., Cao, Q., Wang, W., Lin, L., Ma, K., Zhang, F., Wei, J., Matas, E., et al. (2019) · Brain · doi:10.1093/brain/awy354 · Cited by 168 · see citing works
Epigenetic Alterations in Alzheimer’s Disease
Sanchez-Mut, J. V., & Gräff, J. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00347 · Cited by 168 · see citing works
Genetic syndromes caused by mutations in epigenetic genes
Berdasco, M., & Esteller, M. (2013) · Human Genetics · doi:10.1007/s00439-013-1271-x · Cited by 165 · see citing works
Epigenetic Regulation of Chronic Pain
Liang, L., Lutz, B. M., Bekker, A., & Tao, Y. (2015) · Epigenomics · doi:10.2217/epi.14.75 · Cited by 163 · see citing works
Koemans, T. S., Kleefstra, T., Chubak, M. C., Stone, M. H., Reijnders, M. R. F., de Munnik, S., Willemsen, M. H., Fencková, M., Schrander-Stumpel, C. T. R. M., Bok, L. A., et al. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006864 · Cited by 159 · see citing works
Self-citationDisruption of POGZ Is Associated with Intellectual Disability and Autism Spectrum Disorders
Stessman, H. A. F., Willemsen, M. H., Fencková, M., Penn, O., Hoischen, A., Xiong, B., Wang, T., Hoekzema, K., Vives, L., Vogel, I., et al. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.02.004 · Cited by 155 · see citing works
Self-citationNeuronal network dysfunction in a model for Kleefstra syndrome mediated by enhanced NMDAR signaling
Frega, M., Linda, K., Keller, J. M., Gümüş-Akay, G., Mossink, B., van Rhijn, J.-R., Negwer, M., Klein Gunnewiek, T., Foreman, K., Kompier, N., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12947-3 · Cited by 137 · see citing works
Self-citationEpigenetic Etiology of Intellectual Disability
Iwase, S., Bérubé, N. G., Zhou, Z., Kasri, N. N., Battaglioli, E., Scandaglia, M., & Barco, Á. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1840-17.2017 · Cited by 137 · see citing works
The heat shock response restricts virus infection in Drosophila
Merkling, S. H., Overheul, G. J., van Mierlo, J. T., Arends, D. W., Gilissen, C., & van Rij, R. P. (2015) · Scientific Reports · doi:10.1038/srep12758 · Cited by 118 · see citing works
The genomic impact of 100 million years of social evolution in seven ant species
Gadau, J., Helmkampf, M., Nygaard, S., Roux, J., Simola, D. F., Smith, C. R., Suen, G., Wurm, Y., & Smith, C. D. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.08.005 · Cited by 109 · see citing works
Epigenetic memory: The Lamarckian brain
Fischer, A. (2014) · The EMBO Journal · doi:10.1002/embj.201387637 · Cited by 107 · see citing works
Walker, M. P., LaFerla, F. M., Oddo, S., & Brewer, G. J. (2012) · AGE · doi:10.1007/s11357-011-9375-5 · Cited by 106 · see citing works
van der Voet, M., Harich, B., Franke, B., & Schenck, A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.55 · Cited by 99 · see citing works
Self-citationThe genetics of cognitive epigenetics
Kleefstra, T., Schenck, A., Kramer, J. M., & van Bokhoven, H. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.12.025 · Cited by 99 · see citing works
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Merkling, S. H., Bronkhorst, A. W., Kramer, J. M., Overheul, G. J., Schenck, A., & van Rij, R. P. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004692 · Cited by 97 · see citing works
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Benevento, M., Iacono, G., Selten, M. M., Ba, W., Oudakker, A. R., Frega, M., Keller, J., Mancini, R., Lewerissa, E., Kleefstra, T., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.003 · Cited by 94 · see citing works
Self-citationAlternative Splicing of G9a Regulates Neuronal Differentiation
Fiszbein, A., Giono, L. E., Quaglino, A., Berardino, B. G., Sigaut, L., von Bilderling, C., Schor, I. E., Steinberg, J. H. E., Rossi, M., Pietrasanta, L. I., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.063 · Cited by 88 · see citing works
Understanding Epigenetics in the Neurodegeneration of Alzheimer’s Disease: SAMP8 Mouse Model
Griñán‐Ferré, C., Corpas, R., Puigoriol‐Illamola, D., Palomera‐Ávalos, V., Sanfeliu, C., & Pallàs, M. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170664 · Cited by 83 · see citing works
Wang, Z.-J., Zhong, P., Ma, K., Seo, J.-S., Yang, F., Hu, Z., Zhang, F., Lin, L., Wang, J., Liu, T., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0351-2 · Cited by 82 · see citing works
Centromeric and ectopic assembly of CENP-A chromatin in health and cancer: old marks and new tracks
Sharma, A. B., Dimitrov, S. I., Hamiche, A., & Dyck, E. V. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1298 · Cited by 78 · see citing works
Balemans, M. C. M., Kasri, N. N., Kopanitsa, M. V., Afinowi, N. O., Ramakers, G. J. A., Peters, T. A., Beynon, A. J., Janssen, S. M., van Summeren, R. C. J., Eeftens, J. M., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds490 · Cited by 76 · see citing works
Epigenetic mechanisms modulate differences in Drosophila foraging behavior
Anreiter, I., Kramer, J. M., & Sokolowski, M. B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710770114 · Cited by 75 · see citing works
Self-citationThe role of epigenetic regulation in learning and memory
Guan, J., Xie, H. B., & Ding, X. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.006 · Cited by 75 · see citing works
Balemans, M. C. M., Ansar, M., Oudakker, A. R., van Caam, A. P. M., Bakker, B., Vitters, E. L., van der Kraan, P. M., de Bruijn, D. R. H., Janssen, S. M., Kuipers, A. J., et al. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2013.12.016 · Cited by 72 · see citing works
Self-citationStraub, J., Konrad, E. D. H., Grüner, J., Toutain, A., Bok, L. A., Cho, M. T., Crawford, H. P., Dubbs, H. A., Douglas, G., Jobling, R. K., et al. (2017) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2017.11.008 · Cited by 72 · see citing works
Willemsen, M. H., Nijhof, B., Fencková, M., Nillesen, W. M., Bongers, E. M. H. F., Castells‐Nobau, A., Asztalos, L., Viràgh, E., van Bon, B. W. M., Tezel, E., et al. (2013) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2012-101490 · Cited by 68 · see citing works
Self-citationFencková, M., Blok, L. E. R., Asztalos, L., Goodman, D. P., Čížek, P., Singgih, E. L., Glennon, J. C., IntHout, J., Zweier, C., Eichler, E. E., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.029 · Cited by 66 · see citing works
Self-citationTwo definite cases of sudden unexpected death in epilepsy in a family with a DEPDC5 mutation
Nascimento, F. A., Borlot, F., Cossette, P., Minassian, B. A., & Andrade, D. M. (2015) · Neurology Genetics · doi:10.1212/nxg.0000000000000028 · Cited by 64 · see citing works
Drosophila models of early onset cognitive disorders and their clinical applications
van der Voet, M., Nijhof, B., Oortveld, M. A. W., & Schenck, A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.013 · Cited by 62 · see citing works
Self-citationNagy, J., Kobolák, J., Berzsenyi, S., Ábrahám, Z., Avci, H. X., Bock, I., Bekes, Z., Hodoscsek, B., Chandrasekaran, A., Téglási, A., et al. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.144 · Cited by 61 · see citing works
Histone Lysine Methylation and Neurodevelopmental Disorders
Kim, J., Lee, J., Lee, I., Lee, S. B., & Cho, K. S. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071404 · Cited by 61 · see citing works
Frega, M., Selten, M. M., Mossink, B., Keller, J. M., Linda, K., Moerschen, R., Qu, J., Koerner, P., Jansen, S. M. J., Bijvank, E., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.002 · Cited by 59 · see citing works
Self-citationHistone H3 lysine methylation in cognition and intellectual disability disordersPreprint
Parkel, S., López‐Atalaya, J. P., & Barco, Á. (2013) · Learning & Memory · doi:10.1101/lm.029363.112 · Cited by 59 · see citing works
Making headway with genetic diagnostics of intellectual disabilities
Willemsen, M. H., & Kleefstra, T. (2013) · Clinical Genetics · doi:10.1111/cge.12244 · Cited by 55 · see citing works
Intellectual disability and autism spectrum disorders ‘on the fly’: insights from Drosophila
Coll-Tané, M., Krebbers, A., Castells‐Nobau, A., Zweier, C., & Schenck, A. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.039180 · Cited by 55 · see citing works
Self-citationSui, B., Chen, D., Liu, W., Wu, Q. D., Tian, B., Li, Y., Hou, J., Liu, S., Xie, J., Jiang, H., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02150-9 · Cited by 54 · see citing works
Chase, K. A., & Sharma, R. P. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712001101 · Cited by 53 · see citing works
Benevento, M., van de Molengraft, M., van Westen, R., van Bokhoven, H., & Kasri, N. N. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.013 · Cited by 52 · see citing works
Subbanna, S., & Basavarajappa, B. S. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.07.003 · Cited by 49 · see citing works
Invertebrate Iridoviruses: A Glance over the Last Decade
İnce, İ. A., Özcan, O., Akülke, A. Z. İ., Scully, E. D., & Özgen, A. (2018) · Viruses · doi:10.3390/v10040161 · Cited by 49 · see citing works
Drosophila Courtship Conditioning As a Measure of Learning and Memory
Koemans, T. S., Oppitz, C., Donders, R. T., van Bokhoven, H., Schenck, A., Keleman, K., & Kramer, J. M. (2017) · Journal of Visualized Experiments · doi:10.3791/55808 · Cited by 47 · see citing works
Self-citationNonlinear disease tolerance curves reveal distinct components of host responses to viral infection
Gupta, V., & Vale, P. F. (2017) · Royal Society Open Science · doi:10.1098/rsos.170342 · Cited by 47 · see citing works
Lugtenberg, D., Reijnders, M. R. F., Fencková, M., Bijlsma, E. K., Bernier, R., van Bon, B. W. M., Smeets, E., Silfhout, A. T. V., Bosch, D. G. M., Eichler, E. E., et al. (2016) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.282 · Cited by 46 · see citing works
Self-citationEpigenetic regulation of starvation-induced autophagy in Drosophila by histone methyltransferase G9a
An, P. N. T., Shimaji, K., Tanaka, R., Yoshida, H., Kimurâ, H., Fukusaki, E., & Yamaguchi, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-07566-1 · Cited by 46 · see citing works
Human Intellectual Disability Genes Form Conserved Functional Modules in Drosophila
Oortveld, M. A. W., Keerthikumar, S., Oti, M., Nijhof, B., Fernandes, A. C., Kochinke, K., Castells‐Nobau, A., van Engelen, E., Ellenkamp, T., Eshuis, L., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003911 · Cited by 45 · see citing works
Self-citationmicroRNAs That Promote or Inhibit Memory Formation in Drosophila melanogaster
Busto, G. U., Guven-Ozkan, T., Fulga, T. A., Vactor, D. V., & Davis, R. L. (2015) · Genetics · doi:10.1534/genetics.114.169623 · Cited by 45 · see citing works
The histone methyltransferase G9a regulates tolerance to oxidative stress–induced energy consumption
Riahi, H., Brekelmans, C., Foriel, S., Merkling, S. H., Lyons, T. A., Itskov, P. M., Kleefstra, T., Ribeiro, C., van Rij, R. P., Kramer, J. M., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.2006146 · Cited by 44 · see citing works
Self-citationConserved regulation of neurodevelopmental processes and behavior by FoxP in Drosophila
Castells‐Nobau, A., Eidhof, I., Fencková, M., Brenman‐Suttner, D. B., Gooyert, J. M. S.-D., Christine, S., Schellevis, R. L., van der Laan, K. J., Quentin, C., van Ninhuijs, L., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211652 · Cited by 42 · see citing works
Self-citationKramer, J. M. (2015) · Biochemistry and Cell Biology · doi:10.1139/bcb-2015-0017 · Cited by 40 · see citing works
Self-citationMaity, S., Jarome, T. J., Blair, J. P., Lubin, F. D., & Nguyen, P. (2015) · The Journal of Physiology · doi:10.1113/jp271432 · Cited by 40 · see citing works
Drosophila Studies on Autism Spectrum Disorders
Tian, Y., Zhang, Z. C., & Han, J. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0166-6 · Cited by 40 · see citing works
Jones, S. G., Nixon, K. C. J., Chubak, M. C., & Kramer, J. M. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200560 · Cited by 38 · see citing works
Self-citationZhang, R., Judson, R. N., Liu, D. Y., Kast, J., & Rossi, F. M. V. (2016) · Skeletal Muscle · doi:10.1186/s13395-016-0093-7 · Cited by 38 · see citing works
CEP89 is required for mitochondrial metabolism and neuronal function in man and fly
van Bon, B. W. M., Oortveld, M. A. W., Nijtmans, L. G. J., Fencková, M., Nijhof, B., Besseling, J., Vos, M. H., Kramer, J. M., de Leeuw, N., Castells‐Nobau, A., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt170 · Cited by 37 · see citing works
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Jit, B. P., Qazi, S., Arya, R. K., Srivastava, A., Gupta, N., & Sharma, A. K. (2021) · Epigenomics · doi:10.2217/epi-2020-0349 · Cited by 37 · see citing works
Drosophila Model for Studying Gut Microbiota in Behaviors and Neurodegenerative Diseases
Chiang, M.-H., Ho, S.-M., Wu, H.-Y., Lin, Y.-C., Tsai, W.-H., Wu, T., Lai, C., & Wu, C. (2022) · Biomedicines · doi:10.3390/biomedicines10030596 · Cited by 37 · see citing works
Euchromatin histone methyltransferase 1 regulates cortical neuronal network development
Martens, M. B., Frega, M., Classen, J., Epping, L., Bijvank, E., Benevento, M., van Bokhoven, H., Tiesinga, P. H. E., Schubert, D., & Kasri, N. N. (2016) · Scientific Reports · doi:10.1038/srep35756 · Cited by 37 · see citing works
Immunopathology and immune homeostasis during viral infection in insects
González‐González, A., & Wayne, M. L. (2020) · Advances in virus research · doi:10.1016/bs.aivir.2020.06.001 · Cited by 35 · see citing works
Fellous, A., Earley, R. L., & Silvestre, F. (2018) · Gene · doi:10.1016/j.gene.2018.11.046 · Cited by 34 · see citing works
BOD1 Is Required for Cognitive Function in Humans and Drosophila
Esmaeeli, S., Fencková, M., Porter, I. M., Motazacker, M. M., Nijhof, B., Castells‐Nobau, A., Asztalos, Z., Weißmann, R., Behjati, F., Tzschach, A., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006022 · Cited by 33 · see citing works
Self-citationIyer, J. S., & Girirajan, S. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv018 · Cited by 33 · see citing works
Sharma, M., Razali, N. B., & Sajikumar, S. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw170 · Cited by 32 · see citing works
Stamps, J. A., Saltz, J. B., & Krishnan, V. V. (2013) · Animal Behaviour · doi:10.1016/j.anbehav.2013.07.012 · Cited by 32 · see citing works
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Oey, N. E., Leung, H.-W., Rajaram, E., Zhou, L., Beuerman, R. W., VanDongen, H. M. A., & VanDongen, A. M. J. (2015) · eNeuro · doi:10.1523/eneuro.0020-14.2015 · Cited by 32 · see citing works
Winbush, A., Reed, D., Chang, P. L., Nuzhdin, S. V., Lyons, L. C., & Arbeitman, M. N. (2012) · G3 Genes Genomes Genetics · doi:10.1534/g3.112.004119 · Cited by 32 · see citing works
Histone demethylase PHF2 activates CREB and promotes memory consolidation
Kim, H., Hur, S. W., Park, J. B., Seo, J., Shin, J. J., Kim, M., Kim, M., Han, D. H., Park, J., Park, J. M., et al. (2019) · EMBO Reports · doi:10.15252/embr.201845907 · Cited by 31 · see citing works
Behavior Individuality: A Focus on Drosophila melanogaster
Mollá-Albaladejo, R., & Sánchez‐Alcañiz, J. A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.719038 · Cited by 30 · see citing works
Louwies, T., Ligon, C. O., Johnson, A. C., & Meerveld, B. G. (2018) · Neurogastroenterology & Motility · doi:10.1111/nmo.13500 · Cited by 30 · see citing works
Aberrant epigenetic landscape in intellectual disability
Sanchez-Mut, J. V., Huertas, D., & Esteller, M. (2012) · Progress in brain research · doi:10.1016/b978-0-444-54299-1.00004-2 · Cited by 30 · see citing works
Agrawal, P., Chung, P., Heberlein, U., & Kent, C. F. (2019) · BMC Biology · doi:10.1186/s12915-019-0646-4 · Cited by 29 · see citing works
Epigenetic treatment of behavioral and physiological deficits in a tauopathy mouse model
Wang, W., Cao, Q., Tan, T., Yang, F., Williams, J. B., & Yan, Z. (2021) · Aging Cell · doi:10.1111/acel.13456 · Cited by 29 · see citing works
Kao, G.-S., Cheng, L.-Y., Chen, L.-H., Tzeng, W.-Y., Cherng, C. G., Su, C.-C., Wang, C.-Y., & Yu, L. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.09.040 · Cited by 28 · see citing works
Seco, C. Z., Castells‐Nobau, A., Joo, S.-H., Schraders, M., Foo, J. N., van der Voet, M., Velan, S. S., Nijhof, B., Oostrik, J., de Vrieze, E., et al. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.026476 · Cited by 27 · see citing works
Self-citationGenomics and proteomics in solving brain complexity
Kadakkuzha, B. M., & Puthanveettil, S. V. (2013) · Molecular BioSystems · doi:10.1039/c3mb25391k · Cited by 27 · see citing works
Erban, T., Harant, K., Chalupnikova, J., Kocourek, F., & Stará, J. (2016) · Journal of Proteomics · doi:10.1016/j.jprot.2016.09.016 · Cited by 26 · see citing works
G9a Inhibition Promotes Neuroprotection through GMFB Regulation in Alzheimer’s Disease
Bellver‐Sanchís, A., Geng, Q., Navarro, G., Ávila-López, P. A., Companys‐Alemany, J., Marsal-García, L., Larramona‐Arcas, R., Miró, L., Pérez‐Bosque, A., Ortuño‐Sahagún, D., et al. (2024) · Aging and Disease · doi:10.14336/ad.2023.0424-2 · Cited by 26 · see citing works
Vandewalle, J., Langen, M., Zschaetzsch, M., Nijhof, B., Kramer, J. M., Brems, H., Bauters, M., Lauwers, E., Srahna, M., Marynen, P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081791 · Cited by 25 · see citing works
Self-citationHaploinsufficiency of EHMT1 improves pattern separation and increases hippocampal cell proliferation
Benevento, M., Oomen, C. A., Horner, A. E., Amiri, H., Jacobs, T., Pauwels, C., Frega, M., Kleefstra, T., Kopanitsa, M. V., Grant, S. G. N., et al. (2017) · Scientific Reports · doi:10.1038/srep40284 · Cited by 25 · see citing works
Pang, K. K. L., Sharma, M., & Sajikumar, S. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.01.013 · Cited by 25 · see citing works
O-GlcNAcase contributes to cognitive function in Drosophila
Muha, V., Fencková, M., Ferenbach, A. T., Catinozzi, M., Eidhof, I., Storkebaum, E., Schenck, A., & van Aalten, D. M. F. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.010312 · Cited by 24 · see citing works
Self-citationThe Making of Long-Lasting Memories: A Fruit Fly Perspective
Roselli, C., Ramaswami, M., Boto, T., & Cervantes-Sandoval, I. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.662129 · Cited by 23 · see citing works
Fencková, M., Muha, V., Mariappa, D., Catinozzi, M., Czajewski, I., Blok, L. E. R., Ferenbach, A. T., Storkebaum, E., Schenck, A., & van Aalten, D. M. F. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010159 · Cited by 23 · see citing works
Self-citationPrakash, A., Monteith, K. M., Bonnet, M., & Vale, P. F. (2023) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2023.104756 · Cited by 22 · see citing works
Genetics, molecular control and clinical relevance of habituation learning
Blok, L. E. R., Boon, M., van Reijmersdal, B., Höffler, K. D., Fencková, M., & Schenck, A. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104883 · Cited by 21 · see citing works
Self-citationApproach to epigenetic analysis in language disorders
Smith, S. D. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9099-y · Cited by 21 · see citing works
Kepler, L. D., McDiarmid, T. A., & Rankin, C. H. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107208 · Cited by 21 · see citing works
Histone methylation, alternative splicing and neuronal differentiation
Fiszbein, A., & Kornblihtt, A. R. (2016) · Neurogenesis · doi:10.1080/23262133.2016.1204844 · Cited by 21 · see citing works
- Authors
- 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., Keleman, K., Zhou, H., van Bokhoven, H., & Schenck, A.
- Affiliations
- Radboud University Nijmegen (NL)
- Radboud University Medical Center (NL)
- University of Toronto (CA)
- Research Institute of Molecular Pathology (AT)
- Corresponding author
- Schenck, Annette
- ORCID
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-01-04
- Volume
- 9
- Issue
- 1
- Pages
- e1000569
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC3014924
- OpenAlex
- W2075764106
- Cited by
- 204
- References
- 66
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 7 · 2023: 8 · 2022: 15 · 2021: 13 · 2020: 9 · 2019: 23 · 2018: 15 · 2017: 19 · 2016: 17 · 2015: 19 · 2014: 12 · 2013: 18 · 2012: 15
- FWCI
- 7.02
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- European Commission (241995)
- Bundesministerium für Bildung und Forschung
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- G9a, histone methyltransferase, H3K9 dimethylation, chromatin epigenetics, learning and memory, mushroom body neurons, dendrite formation, non-associative learning, cognitive restoration, intellectual disability, Kleefstra syndrome, EHMT1, Drosophila
- MeSH terms
- Animals, Courtship, Dendrites, DNA, Drosophila, Humans, Larva, Learning, Locomotion, Memory, Methylation, Nervous System, Phylogeny, Histone-Lysine N-Methyltransferase, Sequence Deletion, Gene Expression Profiling, Euchromatin, Epigenesis, Genetic
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