HDAC4 Governs a Transcriptional Program Essential for Synaptic Plasticity and Memory
Open accessAbstract
Neuronal activity influences genes involved in circuit development and information processing. However, the molecular basis of this process remains poorly understood. We found that HDAC4, a histone deacetylase that shuttles between the nucleus and cytoplasm, controls a transcriptional program essential for synaptic plasticity and memory. The nuclear import of HDAC4 and its association with chromatin is negatively regulated by NMDA receptors. In the nucleus, HDAC4 represses genes encoding constituents of central synapses, thereby affecting synaptic architecture and strength. Furthermore, we show that a truncated form of HDAC4 encoded by an allele associated with mental retardation is a gain-of-function nuclear repressor that abolishes transcription and synaptic transmission despite the loss of the deacetylase domain. Accordingly, mice carrying a mutant that mimics this allele exhibit deficits in neurotransmission, spatial learning, and memory. These studies elucidate a mechanism of experience-dependent plasticity and define the biological role of HDAC4 in the brain.
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Nuclear HDAC4 functions as a transcriptional repressor, downregulating plasticity-related genes, and may mediate learning and memory impairment in mice.
“Nuclear HDAC4 functions as a transcriptional repressor, downregulating the expression of numerous plasticity-related genes, that may mediate effects on learning and memory impairment in mice.143,144”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [143]
The amount of synaptic proteins is regulated by transcription, splicing, mRNA transport, translation and degradation.
“the amount of synaptic proteins is regulated by transcription 102 , splicing 103 , mRNA transport 104 , translation 105 and degradation 106”
From Progress toward treatments for synaptic defects in autism (2013) · cites this paper as [102]
The subcellular localization of HDAC4 is regulated by NMDA receptors, as application of the NMDA receptor antagonist AP5 induces nuclear accumulation of HDAC4.
“The subcellular localization of HDAC4 is thought to be regulated by NMDA receptors, as application of the NMDA receptor antagonist AP5 induces nuclear accumulation of HDAC4.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [60]
HDAC4 negatively regulates transcription required for synaptic transmission and information processing.
“In the brain, HDAC4 also negatively regulates transcription required for synaptic transmission and information processing.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [60]
Transgenic mice expressing mutant HDAC4 with constitutive nuclear localization showed reduced expression of genes essential for synaptic function, including Camk2a, Homer1, and Snap25.
“Transgenic mice expressing mutant HDAC4 with constitutive nuclear localization showed reduced expression of genes essential for synaptic function, including Camk2a, Homer1, and Snap25.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [60]
Transgenic mice expressing truncated HDAC4 retained in the nucleus showed abnormal acquisition and retention of memory.
“These mice in which nuclear HDAC4 functions as a gain-of-function suppressor of transcription showed abnormal acquisition and retention of memory.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [60]
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Cites
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658 · see citing works
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Haberland, M., Montgomery, R. L., & Olson, E. N. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2485 · Cited by 2,541 · see citing works
Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat.
Barnes, C. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077579 · Cited by 2,088 · see citing works
Germline Transmission and Tissue-Specific Expression of Transgenes Delivered by Lentiviral Vectors
Lois, C., Hong, E. J., Pease, S., Brown, E. J., & Baltimore, D. (2002) · Science · doi:10.1126/science.1067081 · Cited by 1,974 · see citing works
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · see citing works
MeCP2, a Key Contributor to Neurological Disease, Activates and Represses Transcription
Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T. C., Qin, J., & Zoghbi, H. Y. (2008) · Science · doi:10.1126/science.1153252 · Cited by 1,823 · see citing works
Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders
Hardingham, G. E., & Bading, H. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2911 · Cited by 1,644 · 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
Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes
Chao, H.-T., Chen, H., Samaco, R. C., Xue, M., Chahrour, M., Yoo, J., Neul, J. L., Gong, S., Lu, H.-C., Heintz, N., et al. (2010) · Nature · doi:10.1038/nature09582 · Cited by 1,168 · see citing works
Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation
McKinsey, T. A., Zhang, C., Lu, J., & Olson, E. N. (2000) · Nature · doi:10.1038/35040593 · Cited by 1,051 · see citing works
Class II Histone Deacetylases Act as Signal-Responsive Repressors of Cardiac Hypertrophy
Zhang, C. L., McKinsey, T. A., Chang, S., Antos, C. L., Hill, J. A., & Olson, E. N. (2002) · Cell · doi:10.1016/s0092-8674(02)00861-9 · Cited by 973 · see citing works
Flavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832 · see citing works
Histone Deacetylase 4 Controls Chondrocyte Hypertrophy during Skeletogenesis
Vega, R. B., Matsuda, K., Oh, J., Barbosa, A. C. C., Yang, X., Meadows, E., McAnally, J., Pomajzl, C., Shelton, J. M., Richardson, J. A., et al. (2004) · Cell · doi:10.1016/j.cell.2004.10.024 · Cited by 805 · see citing works
Crawley, J. N. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01258-x · Cited by 762 · see citing works
Saura, C. A., Choi, S.-Y., Beglopoulos, V., Malkani, S., Zhang, D., Rao, B. S. S., Chattarji, S., Kelleher, R. J., Kandel, E. R., Duff, K., et al. (2004) · Neuron · doi:10.1016/s0896-6273(04)00182-5 · Cited by 757 · see citing works
RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis
Hong, F., Rainer Breitling, A., McEntee, C., Wittner, B. S., Nemhauser, J. L., & Chory, J. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl476 · Cited by 753 · see citing works
MicroRNA-206 Delays ALS Progression and Promotes Regeneration of Neuromuscular Synapses in Mice
Williams, A. H., Valdez, G., Moresi, V., Qi, X., McAnally, J., Elliott, J. L., Bassel‐Duby, R., Sanes, J. R., & Olson, E. N. (2009) · Science · doi:10.1126/science.1181046 · Cited by 738 · see citing works
Neuronal MeCP2 Is Expressed at Near Histone-Octamer Levels and Globally Alters the Chromatin State
Skene, P. J., Illingworth, R. S., Webb, S., Kerr, A. R. W., James, K. D., Turner, D. J., Andrews, R., & Bird, A. P. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.030 · Cited by 688 · see citing works
Hebb and homeostasis in neuronal plasticity
Turrigiano, G. G., & Nelson, S. B. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00091-x · Cited by 687 · see citing works
SNARE Function Analyzed in Synaptobrevin/VAMP Knockout Mice
Schoch, S., Deák, F., Königstorfer, A., Mozhayeva, M. G., Sara, Y., Südhof, T. C., & Kavalali, E. T. (2001) · Science · doi:10.1126/science.1064335 · Cited by 664 · see citing works
Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes
Bantscheff, M., Hopf, C., Savitski, M. M., Dittmann, A., Grandi, P., Michon, A.-M., Schlegl, J., Abraham, Y., Becher, I., Bergamini, G., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1759 · Cited by 659 · see citing works
Regulation of gene expression and cocaine reward by CREB and ΔFosB
McClung, C. A., & Nestler, E. J. (2003) · Nature Neuroscience · doi:10.1038/nn1143 · Cited by 625 · see citing works
Chubykin, A. A., Atasoy, D., Etherton, M. R., Brose, N., Kavalali, E. T., Gibson, J. R., & Südhof, T. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.029 · Cited by 594 · see citing works
Activity-Dependent Regulation of MEF2 Transcription Factors Suppresses Excitatory Synapse Number
Flavell, S. W., Cowan, C. W., Kim, T.-K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., & Greenberg, M. E. (2006) · Science · doi:10.1126/science.1122511 · Cited by 573 · see citing works
Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases
Lahm, A., Paolini, C., Pallaoro, M., Nardi, M. C., Jones, P., Neddermann, P., Sambucini, S., Bottomley, M. J., Lo Surdo, P., Carfı́, A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706487104 · Cited by 566 · see citing works
Mihaylova, M. M., Vasquez, D. S., Ravnskjær, K., Denechaud, P., Yu, R. T., Alvarez, J. G. A., Downes, M., Evans, R. M., Montminy, M., & Shaw, R. J. (2011) · Cell · doi:10.1016/j.cell.2011.03.043 · Cited by 554 · see citing works
MeCP2 Controls Excitatory Synaptic Strength by Regulating Glutamatergic Synapse Number
Chao, H.-T., Zoghbi, H. Y., & Rosenmund, C. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.018 · Cited by 511 · see citing works
Wojcik, S. M., Rhee, J. S., Herzog, É., Sigler, A., Jahn, R., Takamori, S., Brose, N., & Rosenmund, C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401764101 · Cited by 510 · see citing works
AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Makino, H., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.035 · Cited by 501 · see citing works
Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
Dittgen, T., Nimmerjahn, A., Komai, S., Licznerski, P., Waters, J., Margrie, T. W., Helmchen, F., Denk, W., Brecht, M., & Osten, P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407976101 · Cited by 485 · see citing works
Bach, M. E., Hawkins, R. D., Osman, M., Kandel, E. R., & Mayford, M. R. (1995) · Cell · doi:10.1016/0092-8674(95)90010-1 · Cited by 475 · see citing works
CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models
Benito, E., & Barco, Á. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.02.001 · Cited by 450 · see citing works
The many faces of REST oversee epigenetic programming of neuronal genes
Ballas, N., & Mandel, G. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.015 · Cited by 441 · see citing works
Flavell, S. W., Kim, T.-K., Gray, J. M., Harmin, D. A., Hemberg, M., Hong, E. J., Markenscoff-Papadimitriou, E., Bear, D. M., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.11.029 · Cited by 440 · see citing works
Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases
Sin, W. C., Haas, K. Z., Ruthazer, E. S., & Cline, H. T. (2002) · Nature · doi:10.1038/nature00987 · Cited by 433 · see citing works
Corepressor-Dependent Silencing of Chromosomal Regions Encoding Neuronal Genes
Lunyak, V. V., Burgess, R., Prefontaine, G. G., Nelson, C., Sze, S.-H., Chenoweth, J., Schwartz, P., Pevzner, P. A., Glass, C., Mandel, G., et al. (2002) · Science · doi:10.1126/science.1076469 · Cited by 416 · see citing works
Differential Control of the Releasable Vesicle Pools by SNAP-25 Splice Variants and SNAP-23
Sørensen, J. B., Nagy, G., Varoqueaux, F., Nehring, R. B., Brose, N., Wilson, M. C., & Neher, E. (2003) · Cell · doi:10.1016/s0092-8674(03)00477-x · Cited by 364 · see citing works
The postsynaptic density proteins Homer and Shank form a polymeric network structure
Hayashi, M. K., Tang, C., Verpelli, C., Narayanan, R., Stearns, M. H., Xu, R.-M., Li, H., Sala, C., & Hayashi, Y. (2009) · Cell · doi:10.1016/j.cell.2009.01.050 · Cited by 356 · see citing works
V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking
Zhang, Y., Narayan, S., Geiman, E. J., Lanuza, G. M., Velasquez, T., Shanks, B., Akay, T., Dyck, J. R. B., Pearson, K. G., Gosgnach, S., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.027 · Cited by 350 · see citing works
Signaling from synapse to nucleus: the logic behind the mechanisms
Deisseroth, K. A., Mermelstein, P. G., Xia, H., & Tsien, R. W. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00076-x · Cited by 350 · see citing works
Disruption of LGI1–linked synaptic complex causes abnormal synaptic transmission and epilepsy
Fukata, Y., Lovero, K. L., Iwanaga, T., Watanabe, A., Yokoi, N., Tabuchi, K., Shigemoto, R., Nicoll, R. A., & Fukata, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914537107 · Cited by 341 · see citing works
Complexin Controls the Force Transfer from SNARE Complexes to Membranes in Fusion
Maximov, A., Tang, J., Yang, X., Pang, Z. P., & Südhof, T. C. (2009) · Science · doi:10.1126/science.1166505 · Cited by 339 · see citing works
Self-citationSchenck, 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
Gephyrin: where do we stand, where do we go?
Fritschy, J., Harvey, R., & Schwarz, G. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.02.006 · Cited by 315 · see citing works
Calcium/calmodulin-dependent protein kinase II and synaptic plasticity
Colbran, R. J., & Brown, A. M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.05.008 · Cited by 307 · see citing works
Williams, S. R., Aldred, M. A., Der Kaloustian, V. M., Halal, F., Gowans, G., McLeod, D. R., Zondag, S., Toriello, H. V., Magenis, R. E., & Elsea, S. H. (2010) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2010.07.011 · Cited by 302 · see citing works
Neuronal activity‐dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5
Chawla, S., Vanhoutte, P., Arnold, F. J. L., Huang, C. L.-H., & Bading, H. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01648.x · Cited by 301 · see citing works
Signaling from cAMP/PKA to MAPK and Synaptic Plasticity
Waltereit, R., & Weller, M. (2003) · Molecular Neurobiology · doi:10.1385/mn:27:1:99 · Cited by 300 · see citing works
Cohen, S., Gabel, H. W., Hemberg, M., Hutchinson, A. N., Sadacca, L. A., Ebert, D. H., Harmin, D. A., Greenberg, R. S., Verdine, V. K., Zhou, Z., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.022 · Cited by 298 · see citing works
Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins
Elias, G. M., & Nicoll, R. A. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.07.005 · Cited by 288 · see citing works
Integration of biochemical signalling in spines
Kennedy, M. B., Beale, H. C., Carlisle, H. J., & Washburn, L. R. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1685 · Cited by 286 · see citing works
Identification of a Signal-Responsive Nuclear Export Sequence in Class II Histone Deacetylases
McKinsey, T. A., Zhang, C. L., & Olson, E. N. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.18.6312-6321.2001 · Cited by 285 · see citing works
SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons
Rumbaugh, G., Adams, J. P., Kim, J. H., & Huganir, R. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600084103 · Cited by 260 · see citing works
Adult Neural Function Requires MeCP2
McGraw, C. M., Samaco, R. C., & Zoghbi, H. Y. (2011) · Science · doi:10.1126/science.1206593 · Cited by 255 · see citing works
Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome
Ronesi, J. A., Collins, K. A., Hays, S. A., Tsai, N.-P., Guo, W., Birnbaum, S. G., Hu, J.-H., Worley, P. F., Gibson, J. R., & Huber, K. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3033 · Cited by 251 · see citing works
A Hormone-Dependent Module Regulating Energy Balance
Wang, B., Moya, N., Niessen, S., Hoover, H. S., Mihaylova, M. M., Shaw, R. J., Yates, J. R., Fischer, W. H., Thomas, J. B., & Montminy, M. (2011) · Cell · doi:10.1016/j.cell.2011.04.013 · Cited by 242 · see citing works
Self-citationPaolo, G. D., Sankaranarayanan, S., Wenk, M. R., DANIELL, L. W., Perucco, E., Caldarone, B. J., Flavell, R. A., Picciotto, M. R., Ryan, T. A., Cremona, O., et al. (2002) · Neuron · doi:10.1016/s0896-6273(02)00601-3 · 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
Platel, J., Dave, K. A., Gordon, V., Lacar, B., Rubio, M. E., & Bordey, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.009 · Cited by 225 · see citing works
Distinct FGFs promote differentiation of excitatory and inhibitory synapses
Terauchi, A., Johnson-Venkatesh, E., Toth, A. B., Javed, D., Sutton, M. A., & Umemori, H. (2010) · Nature · doi:10.1038/nature09041 · Cited by 214 · see citing works
Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia
Li, J., Chen, J., Ricupero, C. L., Hart, R. P., Schwartz, M. S., Kusnecov, A., & Herrup, K. (2012) · Nature Medicine · doi:10.1038/nm.2709 · Cited by 210 · see citing works
SynGAP regulates spine formation
Vazquez, L. E., Chen, H.-J., Sokolova, I., Knuesel, I., & Kennedy, M. B. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3213-04.2004 · Cited by 203 · see citing works
Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity
Schlüter, O. M., Basu, J., Südhof, T. C., & Rosenmund, C. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3553-05.2006 · Cited by 199 · see citing works
HDAC4 Regulates Neuronal Survival in Normal and Diseased Retinas
Chen, B., & Cepko, C. L. (2009) · Science · doi:10.1126/science.1166226 · Cited by 192 · see citing works
Intracellular Trafficking of Histone Deacetylase 4 Regulates Neuronal Cell Death
Bolger, T. A., & Yao, T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1826-05.2005 · Cited by 190 · see citing works
Synaptic Roles of Cdk5: Implications in Higher Cognitive Functions and Neurodegenerative Diseases
Cheung, Z. H., Fu, A. K. Y., & Ip, N. Y. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.024 · Cited by 182 · see citing works
Ng, D., Pitcher, G. M., Szilard, R. K., Sertie, A. L., Kanisek, M., Clapcote, S. J., Lipina, T. V., Kalia, L. V., Joo, D. T., McKerlie, C., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000041 · Cited by 180 · see citing works
Song, K., Backs, J., McAnally, J., Qi, X., Gerard, R. D., Richardson, J. A., Hill, J. A., Bassel‐Duby, R., & Olson, E. N. (2006) · Cell · doi:10.1016/j.cell.2006.02.048 · Cited by 179 · see citing works
SV2 Renders Primed Synaptic Vesicles Competent for Ca<sup>2+</sup>-Induced Exocytosis
Chang, W.-P., & Südhof, T. C. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4521-08.2009 · Cited by 176 · see citing works
Neurotransmission selectively regulates synapse formation in parallel circuits in vivo
Kerschensteiner, D., Morgan, J., Parker, E. D., Lewis, R. M., & Wong, R. (2009) · Nature · doi:10.1038/nature08236 · Cited by 175 · see citing works
A Neural Tetraspanin, Encoded by late bloomer , That Facilitates Synapse Formation
Kopczynski, C., Davis, G. W., & Goodman, C. S. (1996) · Science · doi:10.1126/science.271.5257.1867 · Cited by 170 · see citing works
Effects of visual experience on activity-dependent gene regulation in cortex
Majdan, M., & Shatz, C. J. (2006) · Nature Neuroscience · doi:10.1038/nn1674 · Cited by 158 · see citing works
Canzonetta, C., Mulligan, C., Deutsch, S., Ruf, S., O’Doherty, A., Lyle, R., Borel, C., Lin-Marq, N., Delom, F., Groet, J., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.08.012 · Cited by 158 · see citing works
Akhtar, M. W., Raingo, J., Nelson, E. D., Montgomery, R. L., Olson, E. N., Kavalali, E. T., & Monteggia, L. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0097-09.2009 · Cited by 151 · see citing works
Protein serine/threonine phosphatases in neuronal plasticity and disorders of learning and memory
Mansuy, I. M., & Shenolikar, S. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.10.004 · Cited by 151 · see citing works
Activity-Dependent IGF-1 Exocytosis is Controlled by the Ca2+-Sensor Synaptotagmin-10
Cao, P., Maximov, A., & Südhof, T. (2011) · Cell · doi:10.1016/j.cell.2011.03.034 · Cited by 149 · see citing works
Self-citationHaberland, M., Arnold, M., McAnally, J., Phan, D., Kim, Y., & Olson, E. N. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01415-06 · Cited by 149 · see citing works
Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4
Backs, J., Worst, B. C., Lehmann, L., Patrick, D. M., Jebessa, Z. H., Kreußer, M. M., Sun, Q., Chen, L., Heft, C., Katus, H. A., et al. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201105063 · Cited by 148 · see citing works
Raiker, S. J., Lee, H., Baldwin, K. T., Duan, Y., Shrager, P. G., & Giger, R. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0895-10.2010 · Cited by 145 · see citing works
Colbran, R. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3602-04.2004 · Cited by 139 · see citing works
HDAC4 inhibits cell‐cycle progression and protects neurons from cell death
Majdzadeh, N., Wang, L., Morrison, B. E., Bassel‐Duby, R., Olson, E. N., & D’Mello, S. R. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20637 · Cited by 134 · see citing works
Activity-dependent synaptogenesis in the adult Mammalian cortex
Zito, K., & Svoboda, K. (2002) · Neuron · doi:10.1016/s0896-6273(02)00903-0 · Cited by 134 · see citing works
Activity-regulated genes as mediators of neural circuit plasticity
Leslie, J. H., & Nedivi, E. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.05.002 · Cited by 133 · see citing works
Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways
Saneyoshi, T., Fortin, D. A., & Soderling, T. R. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.09.013 · Cited by 133 · see citing works
A Calcium-Dependent Switch in a CREST-BRG1 Complex Regulates Activity-Dependent Gene Expression
Qiu, Z., & Ghosh, A. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.040 · Cited by 125 · see citing works
Smalla, K., Matthies, H. K., Langnäse, K., Shabir, S., Böckers, T. M., Wyneken, Ú., Staak, S., Krug, M., Beesley, P. W., & Gundelfinger, E. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.080389297 · Cited by 124 · see citing works
Alfonso, J., Fernández, M. E., Cooper, B. H., Flügge, G., & Frasch, A. C. C. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504262102 · Cited by 120 · see citing works
IgLON cell adhesion molecules regulate synaptogenesis in hippocampal neurons
Hashimoto, T., Maekawa, S., & Miyata, S. (2009) · Cell Biochemistry and Function · doi:10.1002/cbf.1600 · Cited by 117 · see citing works
cAMP Response Element-Binding Protein Is a Primary Hub of Activity-Driven Neuronal Gene Expression
Benito, E., Valor, L. M., Jimenez-Minchan, M., Huber, W. K., & Barco, Á. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4554-11.2011 · Cited by 117 · see citing works
α2-Chimaerin Is an Essential EphA4 Effector in the Assembly of Neuronal Locomotor Circuits
Beg, A. A., Sommer, J. E., Martin, J. H., & Scheiffele, P. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.036 · Cited by 115 · see citing works
A Conserved Role for Drosophila Neuroglian and Human L1-CAM in Central-Synapse Formation
Godenschwege, T. A., Kristiansen, L. V., Uthaman, S. B., Hortsch, M., & Murphey, R. K. (2006) · Current Biology · doi:10.1016/j.cub.2005.11.062 · Cited by 114 · see citing works
Maximov, A., Shin, O., Liu, X., & Südhof, T. C. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200607021 · Cited by 112 · see citing works
Self-citationImportin-mediated retrograde transport of CREB2 from distal processes to the nucleus in neurons
Lai, K.-O., Zhao, Y., Ch'ng, T. H., & Martin, K. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803906105 · Cited by 106 · see citing works
Copits, B. A., Robbins, J. S., Frausto, S. F., & Swanson, G. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0100-11.2011 · Cited by 104 · see citing works
Isoform specificity of protein kinase Cs in synaptic plasticityPreprint
Sossin, W. S. (2007) · Learning & Memory · doi:10.1101/lm.469707 · Cited by 102 · see citing works
Determinants of postsynaptic Ca2+ signaling in Purkinje neurons
Hartmann, J., & Konnerth, A. (2005) · Cell Calcium · doi:10.1016/j.ceca.2005.01.014 · Cited by 96 · see citing works
Sharma, S. K., & Carew, T. J. (2004) · Learning & Memory · doi:10.1101/lm.81104 · Cited by 95 · see citing works
Compton, A. G., Albrecht, D. E., Seto, J. T., Cooper, S. T., Ilkovski, B., Jones, K., Challis, D. E., Mowat, D. R., Ranscht, B., Bahlo, M., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.10.022 · Cited by 83 · see citing works
Mandel, G., Fiondella, C. G., Covey, M. V., Lu, D. D., LoTurco, J. J., & Ballas, N. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113486108 · Cited by 83 · see citing works
Presynaptic CaV2 calcium channel traffic requires CALF-1 and the α2δ subunit UNC-36
Saheki, Y., & Bargmann, C. I. (2009) · Nature Neuroscience · doi:10.1038/nn.2383 · Cited by 82 · see citing works
Neurobeachin Is Essential for Neuromuscular Synaptic Transmission
Su, Y., Balice‐Gordon, R. J., Hess, D. M., Landsman, D., Minarcik, J. C., Golden, J. A., Hurwitz, I., Liebhaber, S. A., & Cooke, N. E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4644-03.2004 · Cited by 82 · see citing works
Sun, J., Bronk, P., Liu, X., Han, W., & Südhof, T. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511300103 · Cited by 79 · see citing works
Ch’ng, T. H., & Martin, K. C. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.011 · Cited by 73 · see citing works
Regional and subcellular distribution of HDAC4 in mouse brain
Darcy, M. J., Calvin, K., Cavnar, K., & Ouimet, C. C. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22241 · Cited by 69 · see citing works
Laminar organization of the early developing anterior hypothalamus
Caqueret, A., Boucher, F., & Michaud, J. L. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.06.019 · Cited by 56 · see citing works
Sugita, S., Ho, A., & Südhof, T. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00063-5 · Cited by 54 · see citing works
Diacylglycerol kinases in the regulation of dendritic spines
Kim, K., Yang, J., & Kim, E. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06499.x · Cited by 48 · see citing works
Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules
Huang, Z. J. (2006) · Nature Neuroscience · doi:10.1038/nn1638 · Cited by 41 · see citing works
The yin and yang of MeCP2 phosphorylation
Chao, H., & Zoghbi, H. Y. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901518106 · Cited by 37 · see citing works
Reeve, S. P., Lin, X., Şahin, H. B., Jiang, F., Yao, A., Liu, Z., Zhi, H., Broadie, K. S., Li, W., Giangrande, A., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5528-07.2008 · Cited by 29 · see citing works
SP1 regulates a human SNAP‐25 gene expression
Cai, F., Chen, B., Zhou, W., Zis, O., Liu, S., Holt, R. A., Honer, W. G., & Song, W. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05167.x · Cited by 24 · see citing works
The Kelch-like protein 1 modulates P/Q-type calcium current density
Aromolaran, K. A., Benzow, K. A., Koob, M. D., & Piedras-Renterı́a, E. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.12.046 · Cited by 22 · see citing works
Scrg1, a novel protein of the CNS is targeted to the large dense‐core vesicles in neuronal cells
Dandoy‐Dron, F., Griffond, B., Mishal, Z., Tovey, M. G., & Dron, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.03009.x · Cited by 18 · see citing works
Chen, H., CLARK, M. A., & Lambert, N. A. (2004) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(04)89012-8 · Cited by 11 · see citing works
Moesin helps to restrain synaptic growth at the Drosophila neuromuscular junction
Seabrooke, S., & Stewart, B. A. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20595 · Cited by 10 · see citing works
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From the genetic architecture to synaptic plasticity in autism spectrum disorder
Bourgeron, T. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3992 · Cited by 975 · see citing works
From neural development to cognition: unexpected roles for chromatin
Ronan, J. L., Wu, W., & Crabtree, G. R. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3413 · Cited by 544 · see citing works
Milazzo, G., Mercatelli, D., Muzio, G. D., Triboli, L., Rosa, P. D., Perini, G., & Giorgi, F. M. (2020) · Genes · doi:10.3390/genes11050556 · Cited by 431 · see citing works
Nuclear calcium signalling in the regulation of brain function
Bading, H. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3531 · Cited by 374 · see citing works
DNA 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
Brain changes in a maternal immune activation model of neurodevelopmental brain disorders
Bergdolt, L., & Dunaevsky, A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.002 · Cited by 266 · see citing works
Alzheimer’s Disease: From Firing Instability to Homeostasis Network Collapse
Frère, S. G. A., & Slutsky, I. (2018) · Neuron · doi:10.1016/j.neuron.2017.11.028 · Cited by 230 · see citing works
Yuan, M., Yang, B., Rothschild, G., Mann, J. J., Sanford, L. D., Tang, X., Huang, C., Wang, C., & Zhang, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01519-z · Cited by 246 · see citing works
“143,144 In contrast, the role of cytoplasmic HDACs is less understood.”
BackgroundProgress toward treatments for synaptic defects in autism
Delorme, R., Ey, E., Toro, R., Leboyer, M., Gillberg, C., & Bourgeron, T. (2013) · Nature Medicine · doi:10.1038/nm.3193 · Cited by 218 · see citing works
Kumar, V., Kundu, S., Singh, A., & Singh, S. (2022) · Current Neuropharmacology · doi:10.2174/1570159x19666210609160017 · Cited by 210 · see citing works
Class II a HDAC s – new insights into their functions in physiology and pathology
Parra, M. (2014) · FEBS Journal · doi:10.1111/febs.13061 · Cited by 194 · see citing works
MicroRNA-29a Promotion of Nephrin Acetylation Ameliorates Hyperglycemia-Induced Podocyte Dysfunction
Lin, C., Lee, P., Hsu, Y., Lei, C., Ko, J., Chuang, P.-C., Huang, Y., Wang, S.-Y., Wu, S.-L., Chen, Y., et al. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013050527 · Cited by 193 · see citing works
The Mendelian disorders of the epigenetic machineryPreprint
Bjornsson, H. T. (2015) · Genome Research · doi:10.1101/gr.190629.115 · Cited by 192 · see citing works
CaMKII Isoforms in Learning and Memory: Localization and Function
Zalcman, G., Federman, N., & Romano, A. G. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00445 · Cited by 185 · see citing works
Chaudhuri, A. D., Dastgheyb, R. M., Yoo, S.-W., Trout, A., Talbot Jr, C. C., Hao, H., Witwer, K. W., & Haughey, N. J. (2018) · Cell Death & Disease · doi:10.1038/s41419-018-0369-4 · Cited by 184 · see citing works
Epigenetic mechanisms of major depression: Targeting neuronal plasticity
Uchida, S., Yamagata, H., Seki, T., & Watanabe, Y. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12621 · Cited by 181 · see citing works
How the epigenome integrates information and reshapes the synapse
Campbell, R. R., & Wood, M. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0121-9 · Cited by 175 · see citing works
HDAC inhibitors attenuate the development of hypersensitivity in models of neuropathic pain
Denk, F., Huang, W. L., Sidders, B. S., Bithell, A., Crow, M., Grist, J., Sharma, S., Ziemek, D., Rice, A. S. C., Buckley, N. J., et al. (2013) · Pain · doi:10.1016/j.pain.2013.05.021 · Cited by 172 · 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
LSD1n is an H4K20 demethylase regulating memory formation via transcriptional elongation control
Wang, J., Telese, F., Tan, Y., Li, W., Jin, C., He, X., Basnet, H., Ma, Q., Merkurjev, D., Zhu, X., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4069 · Cited by 169 · see citing works
Lang, C., Campbell, K. R., Ryan, B. J., Carling, P. J., Attar, M., Vowles, J., Perestenko, O. V., Bowden, R. J., Baig, F., Kasten, M., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.10.023 · Cited by 170 · see citing works
LRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation
Telese, F., Ma, Q., Perez, P. M., Notani, D., Oh, S., Li, W., Comoletti, D., Ohgi, K. A., Taylor, H., & Rosenfeld, M. G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.033 · Cited by 166 · see citing works
Ernst, C. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.03.001 · Cited by 145 · see citing works
Histone deacetylases (HDACs) and brain function
Volmar, C.-H., & Wahlestedt, C. (2015) · Neuroepigenetics · doi:10.1016/j.nepig.2014.10.002 · Cited by 151 · see citing works
Long‐term plasticity in the hippocampus: maintaining within and ‘tagging’ between synapses
Bin Ibrahim, M. Z., Benoy, A., & Sajikumar, S. (2022) · The FEBS Journal · doi:10.1111/febs.16065 · Cited by 137 · see citing works
HDAC3 Is a Negative Regulator of Cocaine-Context-Associated Memory Formation
Rogge, G. A., Singh, H., Dang, R., & Wood, M. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4472-12.2013 · Cited by 124 · see citing works
The promise and perils of HDAC inhibitors in neurodegeneration
Didonna, A., & Opal, P. (2014) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.147 · Cited by 120 · see citing works
Synaptic Dysfunction in Alzheimer’s Disease: Aβ, Tau, and Epigenetic Alterations
Li, K., Wei, Q., Liu, F., Hu, F., Xie, A., Zhu, L., & Liu, D. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0533-3 · Cited by 119 · see citing works
Mielcarek, M., Zielonka, D., Carnemolla, A., Marcinkowski, T., & Guidez, F. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00042 · Cited by 111 · see citing works
Epigenetic modifications in the nervous system and their impact upon cognitive impairments
Rudenko, A., & Tsai, L. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.043 · Cited by 108 · 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
HDAC4: a key factor underlying brain developmental alterations in CDKL5 disorder
Trazzi, S., Fuchs, C., Viggiano, R., Franceschi, M. D., Valli, E., Jedynak, P., Hansen, F. K., Perini, G., Rimondini, R., Kurz, T., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw231 · Cited by 101 · see citing works
Estrogen-dependent association of HDAC4 with fear in female mice and women with PTSD
Maddox, S. A., Kilaru, V., Shin, J. H., Jovanović, T., Almli, L. M., Dias, B. G., Norrholm, S. D., Fani, N., Michopoulos, V., Ding, Z., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.250 · Cited by 104 · see citing works
Inducible control of gene expression with destabilized Cre
Sando, R. C., Baumgaertel, K., Pieraut, S., Torabi-Rander, N., Wandless, T. J., Mayford, M. R., & Maximov, A. (2013) · Nature Methods · doi:10.1038/nmeth.2640 · Cited by 102 · see citing works
Self-citationDouse, C. H., Bloor, S., Liu, Y., Shamin, M., Tchasovnikarova, I. A., Timms, R. T., Lehner, P. J., & Modis, Y. (2018) · Nature Communications · doi:10.1038/s41467-018-03045-x · Cited by 101 · see citing works
Valor, L. M. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8715-8 · Cited by 99 · see citing works
Histone Methylation by the Kleefstra Syndrome Protein EHMT1 Mediates Homeostatic Synaptic Scaling
Benevento, M., Iacono, G. L., 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
Thaler, F., & Mercurio, C. (2013) · ChemMedChem · doi:10.1002/cmdc.201300413 · Cited by 95 · see citing works
Neuner, S. M., Wilmott, L. A., Hoffmann, B. R., Mozhui, K., & Kaczorowski, C. C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.002 · Cited by 93 · see citing works
Kinase signalling in excitatory neurons regulates sleep quantity and depth
Kim, S. J., Hotta-Hirashima, N., Asano, F., Kitazono, T., Iwasaki, K., Nakata, S., Komiya, H., Asama, N., Matsuoka, T., Fujiyama, T., et al. (2022) · Nature · doi:10.1038/s41586-022-05450-1 · Cited by 96 · see citing works
Molecular and Synaptic Bases of CDKL5 Disorder
Zhu, Y., & Xiong, Z. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22639 · Cited by 94 · see citing works
The Genetics of Autism Spectrum Disorders
Huguet, G., Benabou, M., & Bourgeron, T. (2016) · Research and perspectives in endocrine interactions · doi:10.1007/978-3-319-27069-2_11 · Cited by 94 · see citing works
Eating disorder predisposition is associated with ESRRA and HDAC4 mutations
Cui, H., Moore, J., Ashimi, S. S., Mason, B. L., Drawbridge, J. N., Han, S., Hing, B. W. Q., Matthews, A. L., McAdams, C. J., Darbro, B. W., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci71400 · Cited by 85 · see citing works
Shimojo, M., Madara, J. C., Pankow, S., Liu, X., Yates, J., Südhof, T., & Maximov, A. (2019) · Genes & Development · doi:10.1101/gad.320077.118 · Cited by 59 · see citing works
Self-citationHippocampal HDAC4 Contributes to Postnatal Fluoxetine-Evoked Depression-Like Behavior
Sarkar, A., Chachra, P., Kennedy, P., Pena, C. J., Desouza, L. A., Nestler, E. J., & Vaidya, V. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.73 · Cited by 79 · see citing works
The Histone Deacetylase HDAC4 Regulates Long-Term Memory in Drosophila
Fitzsimons, H. L., Schwartz, S., Given, F. M., & Scott, M. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083903 · Cited by 77 · see citing works
Pharmacological intervention of histone deacetylase enzymes in the neurodegenerative disorders
Gupta, R. V., Ambasta, R. K., & Kumar, P. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117278 · Cited by 79 · 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
Schlumm, F., Mauceri, D., Freitag, H. E., & Bading, H. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.432773 · Cited by 76 · see citing works
A signalling pathway for transcriptional regulation of sleep amount in mice
Zhou, R., Wang, G., Li, Q., Meng, F., Liu, C., Gan, R., Ju, D., Liao, M., Xu, J., Sang, D., et al. (2022) · Nature · doi:10.1038/s41586-022-05510-6 · Cited by 76 · see citing works
Morris, M. J., & Monteggia, L. M. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.02.005 · Cited by 75 · see citing works
Anderson, K. W., Chen, J., Wang, M., Mast, N., Pikuleva, I. A., & Turko, I. V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126592 · Cited by 69 · see citing works
Chronic stress and antidepressant induced changes in Hdac5 and Sirt2 affect synaptic plasticity
Erburu, M. M., Muñoz-Cobo, I., Domínguez‐Andrés, J., Beltrán, E., Suzuki, T., Mai, A., Valente, S., Puerta, E., & Tordera, R. M. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.08.016 · Cited by 71 · see citing works
Epigenetics in Neurodevelopment: Emerging Role of Circular RNA
Meng, S., Zhou, H., Feng, Z., Xu, Z., Tang, Y., & Wu, M. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00327 · Cited by 70 · see citing works
Giorgio, E. D., Paluvai, H., Dalla, E., Ranzino, L., Renzini, A., Moresi, V., Minisini, M., Picco, R., & Brancolini, C. (2021) · Genome biology · doi:10.1186/s13059-021-02340-z · Cited by 67 · see citing works
Aging Triggers a Repressive Chromatin State at Bdnf Promoters in Hippocampal Neurons
Palomer, E., Martín‐Segura, A., Baliyan, S., Ahmed, T., Balschun, D., Venero, C., Martín, M. G., & Dotti, C. G. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.08.028 · Cited by 66 · see citing works
Li, P., Ensink, E., Lang, S., Marshall, L. L., Schilthuis, M., Lamp, J. A., Vega, I. E., & Labrie, V. (2020) · Genome biology · doi:10.1186/s13059-020-01960-1 · Cited by 65 · see citing works
Wu, Q., Yang, X., Zhang, L., Zhang, Y., & Feng, L. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0199-2 · Cited by 66 · see citing works
Epigenetic regulation of estrogen-dependent memory
Fortress, A. M., & Frick, K. M. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.05.001 · Cited by 62 · see citing works
Kwapis, J. L., Alaghband, Y., López, A. J., White, A. O., Campbell, R. R., Dang, R., Rhee, D., Tran, A. V., Carl, A. E., Matheos, D. P., et al. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.274 · Cited by 62 · see citing works
Role of Epigenetic Mechanisms in Chronic Pain
Mauceri, D. (2022) · Cells · doi:10.3390/cells11162613 · Cited by 61 · see citing works
Griffin, E. A., Melas, P. A., Zhou, R. W., Li, Y., Mercado, P., Kempadoo, K. A., Stephenson, S. I., Colnaghi, L., Taylor, K. M., Hu, M., et al. (2017) · Science Advances · doi:10.1126/sciadv.1701682 · Cited by 61 · see citing works
Larizza, L., & Finelli, P. (2018) · Clinical Genetics · doi:10.1111/cge.13365 · Cited by 57 · see citing works
Guo, Z., Zhang, Z., Wang, Q., Zhang, J., Wang, L., Zhang, Q., Li, H., & Wu, S. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2017.11.003 · Cited by 58 · see citing works
Epigenetic regulation in memory and cognitive disorders
Rudenko, A., & Tsai, L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.034 · Cited by 56 · see citing works
Mechanisms of epigenetic memory and addiction
Tuesta, L. M., & Zhang, Y. (2014) · The EMBO Journal · doi:10.1002/embj.201488106 · Cited by 57 · see citing works
Fallah, M. S., Szarics, D., Robson, C. M., & Eubanks, J. H. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2020.613098 · Cited by 57 · see citing works
Zhu, Y., Huang, M., Bushong, E. A., Phan, S., Uytiepo, M., Beutter, E., Boemer, D., Tsui, K. C., Ellisman, M. H., & Maximov, A. (2019) · Nature Communications · doi:10.1038/s41467-019-11409-0 · Cited by 53 · see citing works
Self-citationNeuroendocrine pathways underlying risk and resilience to PTSD in women
Ravi, M., Stevens, J. S., & Michopoulos, V. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100790 · Cited by 55 · see citing works
Roberts, J. A., Varma, V. R., An, Y., Varma, S., Candia, J., Fantoni, G., Tiwari, V., Anerillas, C., Williamson, A., Saito, A., et al. (2021) · Science Advances · doi:10.1126/sciadv.abi8178 · Cited by 49 · see citing works
Immunotherapies targeting stimulatory pathways and beyond
Marin-Acevedo, J. A., Kimbrough, E. O., Manochakian, R., Zhao, Y., & Lou, Y. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01085-3 · Cited by 52 · see citing works
Wu, Y., Hou, F., Wang, X., Kong, Q., Han, X., & Bai, B. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00114 · Cited by 52 · see citing works
Sharma, N., Pollina, E. A., Nagy, M. A., Yap, E.-L., DiBiase, F. A., Hrvatin, S., Hu, L. S., Lin, C., & Greenberg, M. E. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.007 · Cited by 50 · see citing works
Kikuma, K., Li, X., Perry, S., Li, Q., Goel, P., Chen, C., Kim, D., Stavropoulos, N., & Dickman, D. K. (2019) · Nature Communications · doi:10.1038/s41467-019-10992-6 · Cited by 53 · see citing works
Wei, W., Zhao, Q., Wang, Z., Liau, W., Basic, D., Ren, H., Marshall, P. R., Zajaczkowski, E. L., Leighton, L. J., Madugalle, S. U., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110546 · Cited by 47 · see citing works
Epigenetic Targeting of Histone Deacetylases in Diagnostics and Treatment of Depression
Park, H., Kim, J., Ahn, S. H., & Ryu, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105398 · Cited by 50 · see citing works
An Evolutionary Genetic Perspective of Eating Disorders
Mayhew, A., Pigeyre, M., Couturier, J. L., & Meyre, D. (2017) · Neuroendocrinology · doi:10.1159/000484525 · Cited by 48 · see citing works
HDAC4 in ischemic stroke: mechanisms and therapeutic potential
Kong, Q., Hao, Y., Li, X., Wang, X., Ji, B., & Wu, Y. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0549-1 · Cited by 47 · see citing works
Le, T. N. H., Williams, S. R., Alaimo, J. T., & Elsea, S. H. (2019) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.61089 · Cited by 45 · see citing works
ATM-deficiency-induced microglial activation promotes neurodegeneration in ataxia-telangiectasia
Lai, J. F., Demirbas, D., Kim, J., Jeffries, A. M., Tolles, A. K., Park, J., Chittenden, T. W., Buckley, P. G., Yu, T. W., Lodato, M. A., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113622 · Cited by 42 · see citing works
Lin, T.-B., Hsieh, M., Lai, C., Cheng, J., Chau, Y., Ruan, T., Chen, G., & Peng, H. (2015) · Anesthesiology · doi:10.1097/aln.0000000000000663 · Cited by 44 · see citing works
Yeh, T., Luo, I.-W., Hsieh, Y., Tseng, T.-J., Chiang, H., & Hsieh, S. (2020) · Cells · doi:10.3390/cells9122725 · Cited by 43 · see citing works
Zobdeh, F., Еременко, И. И., Akan, M. A., Tarasov, V. V., Chubarev, V. N., Schiöth, H. B., & Mwinyi, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119127 · Cited by 42 · see citing works
Histone-acetylation: a link between Alzheimer's disease and post-traumatic stress disorder?
Bahari‐Javan, S., Sananbenesi, F., & Fischer, A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00160 · Cited by 41 · see citing works
Histone deacetylases 1 and 2 are required for brain development
Jaworska, J., Ziemka‐Nałęcz, M., & Zalewska, T. (2015) · The International Journal of Developmental Biology · doi:10.1387/ijdb.150071tz · Cited by 41 · see citing works
Fitzsimons, H. L. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.006 · Cited by 41 · see citing works
The role of nuclear Ca2+ in maintaining neuronal homeostasis and brain health
Mozolewski, P., Jeziorek, M., Schuster, C., Bading, H., Frost, B. E., & Dobrowolski, R. (2021) · Journal of Cell Science · doi:10.1242/jcs.254904 · Cited by 39 · see citing works
Puma, D. D. L., Colussi, C., Bandiera, B., Puliatti, G., Rinaudo, M., Cocco, S., Paciello, F., Re, A., Ripoli, C., Chiara, G. D., et al. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04817-5 · Cited by 39 · see citing works
Zhong, T., Ren, F., Huang, C., Zou, W., Yu, Y., Pan, Y., Sun, B., Wang, E., & Guo, Q. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.12.049 · Cited by 38 · see citing works
Chen, Y., Wang, Y., Modrusan, Z. D., Sheng, M., & Kaminker, J. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0569-14.2014 · Cited by 38 · see citing works
HDAC4 is required for inflammation-associated thermal hypersensitivity
Crow, M., Khovanov, N., Kelleher, J. H., Sharma, S., Grant, A. D., Bogdanov, Y. D., Wood, J. N., McMahon, S. B., & Denk, F. (2015) · The FASEB Journal · doi:10.1096/fj.14-264440 · Cited by 37 · see citing works
Schwartz, S., Truglio, M., Scott, M. J., & Fitzsimons, H. L. (2016) · Genetics · doi:10.1534/genetics.115.183194 · Cited by 36 · see citing works
Liu, Y., Zhang, L., Wu, Q., & Feng, L. (2021) · Acta Pharmacologica Sinica · doi:10.1038/s41401-021-00671-y · Cited by 37 · see citing works
Wu, K. L. H., Wu, C., Tain, Y., Huang, L., Chao, Y., Hung, C., Wu, J., Chen, S.-R., Tsai, P.-C., & Chan, J. Y. H. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.02.004 · Cited by 36 · see citing works
MiR-206-3p alleviates chronic constriction injury-induced neuropathic pain through targeting HDAC4
Wen, J., He, T., Qi, F., & Chen, H. (2018) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.18-0091 · Cited by 36 · see citing works
Pusalkar, M., Suri, D., Kelkar, A., Bhattacharya, A., Galande, S., & Vaidya, V. A. (2015) · Developmental Psychobiology · doi:10.1002/dev.21365 · Cited by 35 · see citing works
Haploinsufficiency of HDAC4 does not cause intellectual disability in all affected individuals
Wheeler, P. G., Huang, D., & Zunyan Dai, Y. (2014) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.36542 · Cited by 35 · see citing works
Activity-Dependent Gene Expression in Neurons
Lee, P. R., & Fields, R. D. (2020) · The Neuroscientist · doi:10.1177/1073858420943515 · Cited by 35 · see citing works
Chen, Y., Lu, C.-H., Ke, C., Chiu, S.-J., Chang, C., Yang, B., Gelovani, J. G., & Liu, R.-S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168633 · Cited by 32 · see citing works
Macabuag, N., Esmieu, W., Breccia, P., Jarvis, R. E., Blackaby, W., Lazari, O., Urbonas, L., Eznarriaga, M., Williams, R., Strijbosch, A., et al. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c01149 · Cited by 34 · see citing works
- Authors
- Sando, R., Gounko, N., Pieraut, S., Liao, L., Yates, J., & Maximov, A.
- Affiliations
- Scripps Research Institute (US)
- Corresponding author
- Maximov, Anton
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-11
- Volume
- 151
- Issue
- 4
- Pages
- 821-834
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3496186
- OpenAlex
- W2031926951
- Cited by
- 274
- References
- 118
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 23 · 2023: 18 · 2022: 19 · 2021: 22 · 2020: 20 · 2019: 24 · 2018: 21 · 2017: 17 · 2016: 23 · 2015: 22 · 2014: 25 · 2013: 14
- FWCI
- 7.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Lirias (submittedVersion)
- Funders
- National Institute of Mental Health (MH085776, R01MH085776, R01MH067880, MH067880-09)
- National Institute of Neurological Disorders and Stroke (P30NS057096, NS057096)
- National Center for Research Resources (P41RR011823, RR011823)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- HDAC4, histone deacetylase, synaptic plasticity, memory, NMDA receptor, nuclear import, chromatin, transcriptional repression, central synapses, intellectual disability, neurotransmission, spatial learning, experience-dependent plasticity
- MeSH terms
- Animals, Brain, Histone Deacetylases, Memory, Neuronal Plasticity, Neurons, Synapses, Transcription Factors, Transcription, Genetic, Receptors, N-Methyl-D-Aspartate, Prosencephalon, Active Transport, Cell Nucleus, Mice
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