The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.
Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4
Open accessAbstract
Stress induces long-lasting changes in neuronal gene expression and cholinergic neurotransmission, but the underlying mechanism(s) are incompletely understood. Here, we report that chromatin structure and histone modifications are causally involved in this transcriptional memory. Specifically, the AChE gene encoding the acetylcholine-hydrolyzing enzyme acetylcholinesterase is known to undergo long-lasting transcriptional and alternative splicing changes after stress. In mice subjected to stress, we identified two alternative 5′ exons that were down-regulated after stress in the hippocampus, accompanied by reduced acetylation and elevated trimethylation of H3K9 at the corresponding promoter. These effects were reversed completely by daily administration of the histone deacetylase (HDAC) inhibitor sodium butyrate for 1 wk after stress. H3K9 hypoacetylation was associated with a selective, sodium butyrate-reversible promoter accumulation of HDAC4. Hippocampal suppression of HDAC4 in vivo completely abolished the long-lasting AChE-related and behavioral stress effects. Our findings demonstrate long-lasting stress-inducible changes in AChE's promoter choices, identify the chromatin changes that support this long-term transcriptional memory, and reveal HDAC4 as a mediator of these effects in the hippocampus.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“These effects were reversed drastically by administration an HDAC inhibitor, and reduced hippocampal HDAC4 levels restored the long-lasting behavioral deficit.136”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [136]
The cited source says what the claim attributes to it.
In the citing paper
“The AChE gene, which encodes the acetylcholine-hydrolyzing enzyme acetylcholinesterase, was downregulated in the hippocampus after stress and accompanied by decreased acetylation and increased trimethylation of H3K9 at the corresponding promoter, as well as HDAC4 accumulation in hippocampal neurons.”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [136]
In the citing paper
“Another study reported increased hippocampal HDAC4 following chronic stress exposure, 84 whereas suppression of hippocampal HDAC4 abolished the long-lasting behavioral deficits induced by stress.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [84]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756
Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., & Monteggia, L. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00653-0 · Cited by 3,217
The use of the elevated plus maze as an assay of anxiety-related behavior in rodents
Walf, A. A., & Frye, C. A. (2007) · Nature Protocols · doi:10.1038/nprot.2007.44 · Cited by 3,035
Histone acetylation in chromatin structure and transcription
Grunstein, M. (1997) · Nature · doi:10.1038/38664 · Cited by 2,884
Histone deacetylases and cancer: causes and therapies
Marks, P. A., Rifkind, R. A., Richon, V. M., Breslow, R., Miller, T., & Kelly, W. K. (2001) · Nature reviews. Cancer · doi:10.1038/35106079 · Cited by 1,866
Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action
Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. (2006) · Nature Neuroscience · doi:10.1038/nn1659 · Cited by 1,780
Role of Histone H3 Lysine 9 Methylation in Epigenetic Control of Heterochromatin Assembly
Nakayama, J.-I., Rice, J. C., Strahl, B. D., Allis, C. D., & Grewal, S. I. S. (2001) · Science · doi:10.1126/science.1060118 · Cited by 1,739
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
Acetylcholine-Synthesizing T Cells Relay Neural Signals in a Vagus Nerve Circuit
Rosas-Ballina, M., Olofsson, P. S., Ochani, M., Valdés-Ferrer, S. I., Levine, Y. A., Reardon, C., Tusche, M. W., Pavlov, V. A., Andersson, U., Chavan, S., et al. (2011) · Science · doi:10.1126/science.1209985 · Cited by 1,551
Inhibition of Histone Deacetylase Activity by Butyrate
Davie, J. R. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.7.2485s · Cited by 1,515
Research works printed but not linked: 5
- 10.1126/science.1066752 · DOI
- 10.1038/nn1659 · DOI · Paper page
- 10.1111/j.1749-6632.2001.tb05830.x · DOI
- 10.1074/jbc.M402752200 · DOI
- 10.1016/S0924-9338(02)00654-5 · DOI · Paper page
Cited by
Sorted by citations
The Organic Anion Transporter (OAT) Family: A Systems Biology Perspective
Nigám, S. K., Bush, K. T., Martovetsky, G., Ahn, S.-Y., Liu, H. C., Richard, E., Bhatnagar, V., & Wu, W. (2014) · Physiological Reviews · doi:10.1152/physrev.00025.2013 · Cited by 526
Biological embedding of experience: a primer on epigenetics
Aristizabal, M. J., Anreiter, I., Halldorsdottir, T., Odgers, C. L., McDade, T. W., Goldenberg, A., Mostafavi, S., Kobor, M. S., Binder, E. B., Sokolowski, M. B., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820838116 · Cited by 268
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
“136 In addition, overexpression of HDAC4 in the hippocampus caused adult rats to be depressive but not anxious.”
BackgroundKratsman, N., Getselter, D., & Elliott, E. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.11.003 · Cited by 239
HDAC4: Mechanism of Regulation and Biological Functions
Wang, Z., Qin, G., & Zhao, T. C. (2014) · Epigenomics · doi:10.2217/epi.13.73 · Cited by 239
Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus
Chetty, S., Friedman, A. R., Taravosh‐Lahn, K., Kirby, E. D., Mirescu, C., Guo, F., Krupik, D., Nicholas, A. C., Geraghty, A. C., Krishnamurthy, A., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.190 · Cited by 237
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
Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis
Feng, X., Li, J. R., Qi, S., Lin, Q. F., Jin, J. B., & Hua, X. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610670114 · Cited by 178
Hippocampal MicroRNA-124 Enhances Chronic Stress Resilience in Mice
Higuchi, F., Uchida, S., Yamagata, H., Abe-Higuchi, N., Hobara, T., Hara, K., Kobayashi, A., Shintaku, T., Itoh, Y., Suzuki, T., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0319-16.2016 · Cited by 158
Checks and balances on cholinergic signaling in brain and body function
Soreq, H. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.05.007 · Cited by 121
Self-citationKim, J., Seung, H., Kwon, K. J., Ko, M. J., Lee, E. J., Oh, H. A., Choi, C. S., Kim, K. C., Gonzales, E. L., You, J. S., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104927 · Cited by 121
Heat Acclimation, Epigenetics, and Cytoprotection Memory
Horowitz, M. (2014) · Comprehensive physiology · doi:10.1002/cphy.c130025 · Cited by 134
Mielcarek, M., Zielonka, D., Carnemolla, A., Marcinkowski, T., & Guidez, F. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00042 · Cited by 111
Cardiomyocyte‐secreted acetylcholine is required for maintenance of homeostasis in the heart
Roy, A., Fields, W. C., Resende, C. R., Resende, R. R., Guatimosim, S., Prado, V. F., Gros, R., & Prado, M. A. M. (2013) · The FASEB Journal · doi:10.1096/fj.13-238279 · Cited by 111
Interplay between pro-inflammatory cytokines and growth factors in depressive illnesses
Audet, M., & Anisman, H. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00068 · Cited by 107
Epigenetics and cytoprotection with heat acclimation
Horowitz, M. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00552.2015 · Cited by 100
de Abreu, M. S., Demin, K. A., Giacomini, A. C. V. V., Amstislavskaya, T. G., Strekalova, T. V., Maslov, G. O., Kositsin, Y., Petersen, E. V., & Kalueff, A. V. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100405 · Cited by 94
Raviv, S., Bharti, K., Rencus‐Lazar, S., Cohen‐Tayar, Y., Schyr, R. B., Evantal, N., Meshorer, E., Zilberberg, A., Idelson, M., Reubinoff, B. E., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004360 · Cited by 88
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
Sharma, S., Taliyan, R., & Ramagiri, S. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0461-x · Cited by 74
Cholinesterases as Biomarkers for Parasympathetic Dysfunction and Inflammation-Related Disease
Shenhar‐Tsarfaty, S., Berliner, S., Bornstein, N. M., & Soreq, H. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0176-4 · Cited by 73
Self-citationMolecular mechanisms of psychiatric diseases
Blokhin, I. O., Khorkova, O., Saveanu, R. V., & Wahlestedt, C. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105136 · Cited by 64
Zimmermann, M. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12359 · Cited by 60
The Role of the Glucocorticoids in Developing Resilience to Stress and Addiction
Srinivasan, S., Shariff, M. R., & Bartlett, S. E. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00068 · Cited by 62
The Effects of Stress and Meditation on the Immune System, Human Microbiota, and Epigenetics.
Househam, A. M., Peterson, C. T., Mills, P. J., & Chopra, D. (2017) · PubMed · Cited by 57
Elevation of Il6 is associated with disturbed let-7 biogenesis in a genetic model of depression
Wei, Y. B., Liu, J. J., Villaescusa, J. C., Åberg, E., Brené, S., Wegener, G., Mathé, A. A., & Lavebratt, C. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.136 · Cited by 57
Transcription Factors Bind Negatively Selected Sites within Human mtDNA Genes
Blumberg, A., Sailaja, B. S., Kundaje, A. B., Levin, L., Dadon, S., Shmorak, S., Shaulian, E., Meshorer, E., & Mishmar, D. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu210 · Cited by 55
Self-citationDecline in Serum Cholinesterase Activities Predicts 2-Year Major Adverse Cardiac Events
Arbel, Y., Shenhar‐Tsarfaty, S., Waiskopf, N., Finkelstein, A., Halkin, A., Revivo, M., Berliner, S. A., Herz, I., Shapira, I., Keren, G., et al. (2013) · Molecular Medicine · doi:10.2119/molmed.2013.00139 · Cited by 53
Self-citationVihervaara, A., Mahat, D. B., Himanen, S. V., Blom, M. A. H., Lis, J. T., & Sistonen, L. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.03.007 · Cited by 52
Liu, W., Pan, Y., Yang, L., Xie, Y. Z., Chen, X., Chang, J., Hao, W., Zhu, L., & Wan, B. (2022) · Journal of Environmental Sciences · doi:10.1016/j.jes.2022.04.022 · Cited by 52
Fetal microglial phenotype in vitro carries memory of prior in vivo exposure to inflammation
Cao, M., Cortes, M., Moore, C. S., Leong, S. Y., Durosier, L. D., Burns, P., Fecteau, G., Desrochers, A., Auer, R. N., Barreiro, L. B., et al. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00294 · Cited by 52
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
Sailaja, B. S., Aita, R., Maledatu, S., Ribnicky, D., Verzi, M. P., & Raskin, I. (2021) · PLoS ONE · doi:10.1371/journal.pone.0248691 · Cited by 60
Self-citationAzad, G. K., Ito, K., Sailaja, B. S., Biran, A., Nissim‐Rafinia, M., Yamada, Y., Brown, D. T., Takizawa, T., & Meshorer, E. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201703141 · Cited by 45
Self-citationYang, L., Wang, J., Wang, D., Hu, G., Liu, Z., Yan, D., Serikuly, N., Alpyshov, E. T., Demin, K. A., Strekalova, T. V., et al. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112644 · Cited by 46
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
Nätt, D., Johansson, I., Faresjö, T., Ludvigsson, J., & Thorsell, A. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0123-z · Cited by 43
Frasch, M. G., Lobmaier, S. M., Stampalija, T., Desplats, P., Pallarés, M. E., Pastor, V. E., Brocco, M. A., Wu, H., Schulkin, J. A., Herry, C. L., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.026 · Cited by 47
Histone methyltransferase Ash1L mediates activity-dependent repression of neurexin-1α
Zhu, Τ., Liang, C., Li, D., Tian, M., Liu, S., Gao, G., & Guan, J. (2016) · Scientific Reports · doi:10.1038/srep26597 · Cited by 43
Fear and C-reactive protein cosynergize annual pulse increases in healthy adults
Shenhar‐Tsarfaty, S., Yayon, N., Waiskopf, N., Shapira, I., Toker, S., Zaltser, D., Berliner, S. A., Ritov, Y., & Soreq, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1418264112 · Cited by 42
Self-citationFitzsimons, H. L. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.006 · Cited by 41
Central and peripheral anti-inflammatory effects of acetylcholinesterase inhibitors
Vaknine, S., & Soreq, H. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108020 · Cited by 41
Self-citationGezen‐Ak, D., Alaylıoğlu, M., Yurttaş, Z., Çamoğlu, T., Şengül, B., İşler, C., Kina, U. Y., Keskin, E., Atasoy, İ. L., Kafadar, A. M., et al. (2023) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2023.109322 · Cited by 37
Myrzakhanova, M., Gambardella, C., Falugi, C., Gatti, A., Tagliafierro, G., Ramoino, P., Bianchini, P., & Diaspro, A. (2013) · BioMed Research International · doi:10.1155/2013/205183 · Cited by 37
Natural Nuclear Factor Kappa Beta Inhibitors
Tambuwala, M. M. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000655 · Cited by 36
Mallei, A., Ieraci, A., & Popoli, M. (2018) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2018.1500029 · Cited by 36
Pusalkar, M., Suri, D., Kelkar, A., Bhattacharya, A., Galande, S., & Vaidya, V. A. (2015) · Developmental Psychobiology · doi:10.1002/dev.21365 · Cited by 36
Sagarkar, S., Balasubramanian, N., Mishra, S., Choudhary, A. G., Kokare, D. M., & Sakharkar, A. J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.01.022 · Cited by 36
Karen, C., & Rajan, K. E. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-019-00655-x · Cited by 37
Valproic acid potentiates curcumin-mediated neuroprotection in lipopolysaccharide induced rats
Zaky, A., Mahmoud, M., Awad, D., Sabaa, B. M. E., Kandeel, K., & Bassiouny, A. R. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00337 · Cited by 35
Cortes, M., Cao, M., Liu, H. L., Moore, C. S., Durosier, L. D., Burns, P., Fecteau, G., Desrochers, A., Barreiro, L. B., Antel, J. P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-09439-z · Cited by 32
Telencephalon transcriptome analysis of chronically stressed adult zebrafish
Huang, V., Butler, A. A., & Lubin, F. D. (2019) · Scientific Reports · doi:10.1038/s41598-018-37761-7 · Cited by 33
Synaptically Localized Transcriptional Regulators in Memory Formation
Uchida, S., & Shumyatsky, G. P. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.023 · Cited by 33
Muñoz-Llanos, M., García-Pérez, M. A., Xu, X., Tejos‐Bravo, M., Vidal, E. A., Moyano, T. C., Gutiérrez, R. A., Aguayo, F. I., Pacheco, A., García‐Rojo, G., et al. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00251 · Cited by 32
The stage-dependent roles of Ldb1 and functional redundancy with Ldb2 in mammalian retinogenesis
Gueta, K., David, A., Cohen, T., Menuchin-Lasowski, Y., Nobel, H., Narkis, G., Li, L., Love, P. E., de Melo, J., Blackshaw, S., et al. (2016) · Development · doi:10.1242/dev.129734 · Cited by 31
HDAC4 Does Not Act as a Protein Deacetylase in the Postnatal Murine Brain In Vivo
Mielcarek, M., Seredenina, T. S., Stokes, M. P., Osborne, G. F., Landles, C., Inuabasi, L., Franklin, S., Silva, J. C., Luthi‐Carter, R., Beaumont, V., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080849 · Cited by 30
Hayase, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158950 · Cited by 25
Moyano, P. M., Flores, A., García, J., García, J. M., Anadón, M. J., Frejo, M. T., Solà, E., Pelayo, A., & del Pino, J. (2021) · Food and Chemical Toxicology · doi:10.1016/j.fct.2021.112614 · Cited by 24
Peng, L., Zhu, M., Yang, Y., Weng, Y., Zou, W., Zhu, X., Guo, Q., & Zhong, T. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.001 · Cited by 24
Livyatan, I., & Meshorer, E. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.33 · Cited by 22
Self-citationAutism Spectrum Disorder: A Neuro-Immunometabolic Hypothesis of the Developmental Origins
Frasch, M. G., Yoon, B.-J., Helbing, D. L., Snir, G., Antonelli, M. C., & Bauer, R. (2023) · Biology · doi:10.3390/biology12070914 · Cited by 21
Wolugbom, J. A., Areloegbe, S. E. J., & Olaniyi, K. S. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03074-0 · Cited by 25
New perspectives for multi-level regulations of neuronal acetylcholinesterase by dioxins
Xie, H. Q., Xu, T., Chen, Y., Li, Y., Xia, Y., Xu, S. L., Wang, L., Tsim, K. W. K., & Zhao, B. (2016) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2016.06.030 · Cited by 21
Cao, M., MacDonald, J. W., Liu, H. L., Weaver, M., Cortes, M., Durosier, L. D., Burns, P., Fecteau, G., Desrochers, A., Schulkin, J. A., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01063 · Cited by 20
Apocynin Prevents Abnormal Megakaryopoiesis and Platelet Activation Induced by Chronic Stress
Sandrini, L., Ieraci, A., Amadio, P., Popoli, M., Tremoli, E., & Barbieri, S. S. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/9258937 · Cited by 21
Behavioral stress reduces RIP140 expression in astrocyte and increases brain lipid accumulation
Feng, X., Lin, Y., & Wei, L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.008 · Cited by 20
Xi, Q., Gao, N., Zhang, X., Zhang, B., Ye, W., Wu, J., & Zhang, X. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.09.012 · Cited by 20
Xu, H., Xie, H. Q., Tao, W., Zhou, Z., Li, S.-Z., & Zhao, B. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0167-5 · Cited by 20
Duggan, S. P., Behan, F. M., Kirca, M., Zaheer, A., McGarrigle, S. A., Reynolds, J. V., Vaz, G. M. F., Senge, M. O., & Kelleher, D. P. (2016) · Scientific Reports · doi:10.1038/srep32638 · Cited by 20
The Stress-Responding miR-132-3p Shows Evolutionarily Conserved Pathway Interactions
Haviv, R., Oz, E., & Soreq, H. (2017) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0515-z · Cited by 21
Self-citationDifferentiation of human glioblastoma U87 cells into cholinergic neuron
Liu, H., Xia, J., Wang, T., Li, W., Song, Y., & Tan, G. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.03.049 · Cited by 19
Gut feeling: MicroRNA discriminators of the intestinal TLR9–cholinergic links
Nadorp, B., & Soreq, H. (2015) · International Immunopharmacology · doi:10.1016/j.intimp.2015.04.058 · Cited by 19
Self-citationCoimbra, B., Soares‐Cunha, C., Borges, S., de Vasconcelos, N. A. P., Sousa, N., & Rodrigues, A. J. (2017) · eLife · doi:10.7554/elife.25843 · Cited by 19
Histone deacetylase 4 (HDAC4): a new player in anorexia nervosa?
Sild, M., & Booij, L. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0366-8 · Cited by 19
Holtkamp, C., Koos, B., Unterberg, M., Rahmel, T., Bergmann, L., Bazzi, Z., Bazzi, M., Bukhari, H., Adamzik, M., & Rump, K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217269 · Cited by 17
Wu, K. L. H., Liu, W., Wu, C., Fu, M., Huang, H., Tain, Y., Liang, C., Hung, C., Chen, I., Hung, P., et al. (2024) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2024.109571 · Cited by 17
Barbieri, S. S., Sandrini, L., Musazzi, L., Popoli, M., & Ieraci, A. (2021) · Biomolecules · doi:10.3390/biom11060885 · Cited by 17
Grafting improves drought stress memory by increasing the P5CS1 gene expression in Brassica rapa
Luo, L., Zheng, Y., Gao, Z., Chen, Q., Kong, X., & Yang, Y. (2020) · Plant and Soil · doi:10.1007/s11104-020-04547-8 · Cited by 16
K V, A., Madhana, R. M., Bais, A. K., Singh, V. B., Malik, A., Sinha, S., Lahkar, M., Kumar, P., & Samudrala, P. K. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00315 · Cited by 15
Waiskopf, N., & Soreq, H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800159-2.00052-x · Cited by 15
Self-citationZhang, T., Linglin, Z., Zeng, S., Bai, L., Chen, J., Zhang, Z., Wang, Y., & Duan, C. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2805 · Cited by 14
Ekronarongchai, S., Palaga, T., Saonanon, P., Pruksakorn, V., Hirankarn, N., van Hagen, P. M., Dik, W. A., & Virakul, S. (2021) · Thyroid · doi:10.1089/thy.2020.0948 · Cited by 14
Zhang, L., Chen, C., & Qi, J. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147051 · Cited by 13
HP1BP3 expression determines maternal behavior and offspring survival
Garfinkel, B. P., Arad, S., Neuner, S. M., Netser, S., Wagner, S., Kaczorowski, C. C., Rosen, C. J., Gal, M., Soreq, H., & Orly, J. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12312 · Cited by 13
Self-citationHod, K., Sperber, A. D., Maharshak, N., Ron, Y., Shapira, I., Zeltser, D., Rogowski, O., Berliner, S. A., Shenhar‐Tsarfaty, S., & Dekel, R. (2018) · Neurogastroenterology & Motility · doi:10.1111/nmo.13464 · Cited by 13
How Epigenetics Can Enhance Pig Welfare?
da Silva, A. N., Araújo, M. S., Pértille, F., & Zanella, A. J. (2021) · Animals · doi:10.3390/ani12010032 · Cited by 19
Mohammadi-Farani, A., Limoee, M., & Shirooie, S. (2021) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000633 · Cited by 11
Histone deacetylase inhibition abolishes stress-induced spatial memory impairment
Vargas-López, V., Lamprea, M. R., & Múnera, A. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.009 · Cited by 12
Kotova, M. M., Amikishiev, S. V., Apukhtin, K. V., Galstyan, D. S., de Abreu, M. S., Stewart, A., Yang, L., & Kalueff, A. V. (2025) · Journal of Comparative Physiology B · doi:10.1007/s00360-025-01613-4 · Cited by 10
Mohammadi-Farani, A., Farhangian, S., & Shirooie, S. (2022) · Research in Pharmaceutical Sciences · doi:10.4103/1735-5362.359435 · Cited by 9
Brain region-specific effects of immobilization stress on cholinesterases in mice
Valuskova, P., Farár, V., Janisova, K., Ondičová, K., Mravec, B., Květňanský, R., & Mysliveček, J. (2016) · Stress · doi:10.1080/10253890.2016.1263836 · Cited by 9
The effect of sodium channels on neurological/neuronal disorders: A systematic review
Bagheri, S., Haddadi, R., Saki, S., Kourosh‐Arami, M., & Komaki, A. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10153 · Cited by 8
Omer, D., Cohen-Zontag, O., Gnatek, Y., Harari‐Steinberg, O., Pleniceanu, O., Namestnikov, M., Cohen, A.-H., Nissim‐Rafinia, M., Tam, G., Tomer Kalisky, C., et al. (2023) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2023.04.005 · Cited by 6
Self-citationHistone Deacetylation in Alzheimer’s Diseases (AD); Hope or Hype
Ateya, N. H., Al-Taie, S. F., Jasim, S. A., Uthirapathy, S., Chaudhary, K., Rani, P., Kundlas, M., Naidu, K. S., Amer, N. A., & Ahmed, J. K. (2025) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-025-01670-0 · Cited by 7
The Current and Future Role of Drugs and Probiotics in the Management of Inflammatory Bowel Disease
de Souza, M. D. S. S., Barbalho, S. M., Goulart, R. D. Á., & de Carvalho, A. D. C. A. (2015) · Journal of Biosciences and Medicines · doi:10.4236/jbm.2015.38008 · Cited by 7
A non‐adaptationist hypothesis of play behaviour
Lewis, A. (2023) · The Journal of Physiology · doi:10.1113/jp284413 · Cited by 7
Pesticide tolerance induced by a generalized stress response in wood frogs (Rana sylvatica)
Billet, L. S., & Hoverman, J. T. (2020) · Ecotoxicology · doi:10.1007/s10646-020-02277-2 · Cited by 7
Role of histone deacetylases in neuroplasticity impairments and inflammation in major depression
Garayo, A., Azqueta, A., & Tordera, R. M. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104081 · Cited by 7
Kniffin, A. R., Bangasser, D. A., & Parikh, V. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15999 · Cited by 7
Lau, K. M., Gong, A. G. W., Xu, M. L., Lam, C. T. W., Zhang, L. M. L., Bi, C. W. C., Cui, D., Cheng, A. W. M., Dong, T. T.-X., Tsim, K. W. K., et al. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.013 · Cited by 5
Metadata
- Authors
- Sailaja, B. S., Cohen-Carmon, D., Zimmerman, G., Soreq, H., & Meshorer, E.
- Affiliations
- Hebrew University of Jerusalem (IL)
- Departments of aGenetics and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-12-10
- Volume
- 109
- Issue
- 52
- Pages
- E3687-95
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3535662
- OpenAlex
- W2102812580
- Cited by
- 121
- References
- 47
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 10 · 2023: 7 · 2022: 5 · 2021: 10 · 2020: 7 · 2019: 10 · 2018: 5 · 2017: 10 · 2016: 14 · 2015: 14 · 2014: 15 · 2013: 10
- FWCI
- 5.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Israel Science Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
- Keywords
- acetylcholinesterase, HDAC4, histone deacetylase, stress, transcriptional memory, alternative splicing, H3K9 acetylation, H3K9 trimethylation, histone modifications, chromatin structure, sodium butyrate, hippocampus, cholinergic neurotransmission, long-term stress effects
- MeSH terms
- Acetylcholinesterase, Animals, Chromatin, Exons, Hippocampus, Histone Deacetylases, Male, Neurons, Promoter Regions, Genetic, Stress, Physiological, Swimming, Transcription, Genetic, DNA Methylation, Gene Silencing, Epigenesis, Genetic, Mice, Histone Deacetylase Inhibitors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review