Nuclear Calcium Signaling Regulates Nuclear Export of a Subset of Class IIa Histone Deacetylases following Synaptic Activity
Open accessAbstract
In neurons, dynamic changes in the subcellular localization of histone deacetylases (HDACs) are thought to contribute to signal-regulated gene expression. Here we show that in mouse hippocampal neurons, synaptic activity-dependent nucleo-cytoplasmic shuttling is a common feature of all members of class IIa HDACs, which distinguishes them from other classes of HDACs. Nuclear calcium, a key regulator in neuronal gene expression, is required for the nuclear export of a subset of class IIa HDACs. We found that inhibition of nuclear calcium signaling using CaMBP4 or increasing the nuclear calcium buffering capacity by means of expression of a nuclear targeted version of parvalbumin (PV.NLS-mC) led to a build-up of HDAC4 and HDAC5 in the cell nucleus, which in the case of PV.NLS-mC can be reversed by nuclear calcium transients triggered by bursts of action potential firing. A similar nuclear accumulation of HDAC4 and HDAC5 was observed in vivo in the mouse hippocampus following stereotaxic delivery of recombinant adeno-associated viruses expressing either CaMBP4 or PV.NLS-mC. The modulation of HDAC4 activity either by RNA interference-mediated reduction of HDAC4 protein levels or by expression of a constitutively nuclear localized mutant of HDAC4 leads to changes in the mRNA levels of several nuclear calcium-regulated genes with known functions in acquired neuroprotection (atf3, serpinb2), memory consolidation (homer1, arc), and the development of chronic pain (ptgs2, c1qc). These results identify nuclear calcium as a regulator of nuclear export of HDAC4 and HDAC5. The reduction of nuclear localized HDACs represents a novel transcription-promoting pathway stimulated by nuclear calcium.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cytoplasmic localization of HDAC4 is maintained by phosphorylation, suppressing MEF2 binding, whereas dephosphorylation by calcineurin allows nuclear translocation.
“Cytoplasmic localization of HDAC4 is maintained by HDAC phosphorylation, suppressing the binding of the transcription factor MEF2,141 whereas HDAC4 dephosphorylation by calcineurin allows nuclear translocation.142”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [141]
Citation 142 attaches to the clause about HDAC4 dephosphorylation and nuclear translocation. The Discussion (page unavailable) says cytoplasmic dephosphorylation unmasks HDAC4’s nuclear localization signal and initiates nuclear import, but names PP2A as a phosphatase that can catalyze it; it does not establish calcineurin’s role. (LLM, conf=0.86)
Experimental — accuracy not yet measuredPhosphorylation of HDAC4 by Ca2+/calmodulin-dependent protein kinases maintains cytoplasmic localization of HDAC4, leads to its nuclear export, and suppresses the transcription factor MEF2.
“Phosphorylation of HDAC4 by Ca 2+ /calmodulin-dependent protein kinases (CAMK) maintains cytoplasmic localization of HDAC4, leads to its nuclear export, 55,56 and suppresses the transcription factor MEF2.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [55]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Histone deacetylases (HDACs): characterization of the classical HDAC family
RUIJTER, A. J. M. D., GENNIP, A. H. V., CARON, H. N., KEMP, S., & KUILENBURG, A. B. P. V. (2003) · Biochemical Journal · doi:10.1042/bj20021321 · Cited by 3,114 · 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
Self-citationThe Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men
Yang, X., & Seto, E. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2346 · Cited by 1,239 · see citing works
Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.12.008 · Cited by 1,157 · 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
Arc/Arg3.1 Is Essential for the Consolidation of Synaptic Plasticity and Memories
Plath, N., Ohana, O., Dammermann, B., Errington, M. L., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.024 · Cited by 827 · see citing works
Three proteins define a class of human histone deacetylases related to yeast Hda1p
Grozinger, C. M., Hassig, C. A., & Schreiber, S. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.4868 · Cited by 770 · see citing works
Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression
Hardingham, G. E., Chawla, S., Johnson, C. M., & Bading, H. (1997) · Nature · doi:10.1038/385260a0 · Cited by 730 · see citing works
Self-citationERK phosphorylation potentiates Elk‐1‐mediated ternary complex formation and transactivation.
Gille, H., Kortenjann, M., Thomae, O., Moomaw, C. R., Slaughter, C. A., Cobb, M. H., & Shaw, P. E. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07076.x · Cited by 665 · see citing works
Class II histone deacetylases: versatile regulators
Verdin, E., Dequiedt, F., & Kasler, H. G. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00073-8 · Cited by 664 · see citing works
Greer, P. L., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.002 · Cited by 661 · cited 2× · see citing works
“HDAC Nucleo-cytoplasmic Shuttling and Synaptic Activitydependent Transcription—Neurons respond and adapt to synaptic stimuli by initiating structural and functional changes, ranging from remodeling of fine anatomical structures to alterations in gene expression (1, 50), which at the behavioral level may ultimately lea…”
BackgroundGrozinger, C. M., & Schreiber, S. L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.140199597 · Cited by 587 · see citing works
Tse, C., Sera, T., Wolffe, A. P., & Hansen, J. C. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.8.4629 · Cited by 574 · see citing works
Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity
Hardingham, G. E., Arnold, F. J. L., & Bading, H. (2001) · Nature Neuroscience · doi:10.1038/85109 · Cited by 537 · see citing works
Self-citationNeuronal Activity-Regulated Gene Transcription in Synapse Development and Cognitive Function
West, A. E., & Greenberg, M. E. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005744 · Cited by 532 · see citing works
McKinsey, T. A., Zhang, C. L., & Olson, E. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.260501497 · Cited by 520 · see citing works
Lu, J., McKinsey, T. A., Nicol, R. L., & Olson, E. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.080064097 · Cited by 518 · see citing works
Rittinger, K., Budman, J., Xu, J., Volinia, S., Cantley, L. C., Smerdon, S. J., Gamblin, S. J., & Yaffe, M. B. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80363-9 · Cited by 506 · see citing works
Stimulation of Protein Tyrosine Phosphorylation by NMDA Receptor Activation
Bading, H., & Greenberg, M. E. (1991) · Science · doi:10.1126/science.1715095 · Cited by 463 · see citing works
Self-citationCalcium Regulation of Dendritic Growth via CaM Kinase IV and CREB-Mediated Transcription
Redmond, L., Kashani, A. H., & Ghosh, A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00737-7 · Cited by 462 · see citing works
Backs, J., Backs, T., Neef, S., Kreußer, M. M., Lehmann, L., Patrick, D. M., Grueter, C. E., Qi, X., Richardson, J. A., Hill, J. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813013106 · Cited by 431 · see citing works
CBP: A Signal-Regulated Transcriptional Coactivator Controlled by Nuclear Calcium and CaM Kinase IV
Chawla, S., Hardingham, G. E., Quinn, D. R., & Bading, H. (1998) · Science · doi:10.1126/science.281.5382.1505 · Cited by 427 · see citing works
Self-citationClass II Histone Deacetylases: from Sequence to Function, Regulation, and Clinical Implication
Yang, X., & Grégoire, S. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.8.2873-2884.2005 · Cited by 419 · see citing works
Ling, H., Zhang, T., Pereira, L., Means, C. K., Cheng, H., Gu, Y., Dalton, N. D., Peterson, K. L., Chen, J., Bers, D. M., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci38022 · Cited by 385 · see citing works
Physical and Functional HAT/HDAC Interplay Regulates Protein Acetylation Balance
Peserico, A., & Simone, C. (2010) · BioMed Research International · doi:10.1155/2011/371832 · Cited by 362 · see citing works
Distribution of histone deacetylases 1–11 in the rat brain
Broide, R. S., Redwine, J. M., Aftahi, N., Young, W. G., Bloom, F. E., & Winrow, C. J. (2007) · Journal of Molecular Neuroscience · doi:10.1007/bf02686117 · Cited by 347 · see citing works
Zhang, S., Zou, M., Lü, L., Lau, D., Ditzel, D. A. W., Delucinge-Vivier, C., Aso, Y., Descombes, P., & Bading, H. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000604 · Cited by 311 · see citing works
Self-citationZhang, S.-J., Steijaert, M. N., Lau, D., Schütz, G., Delucinge-Vivier, C., Descombes, P., & Bading, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.025 · Cited by 304 · see citing works
Self-citationNeuronal 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
Self-citationHardingham, G. E., Arnold, F. J. L., & Bading, H. (2001) · Nature Neuroscience · doi:10.1038/88380 · Cited by 290 · see citing works
Self-citationRescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities
Oliveira, A. M. M., Hemstedt, T. J., & Bading, H. (2012) · Nature Neuroscience · doi:10.1038/nn.3151 · Cited by 289 · see citing works
Self-citationIdentification 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
HDAC4 Governs a Transcriptional Program Essential for Synaptic Plasticity and Memory
Sando, R., Gounko, N., Pieraut, S., Liao, L., Yates, J., & Maximov, A. (2012) · Cell · doi:10.1016/j.cell.2012.09.037 · Cited by 274 · see citing works
Hardingham, G. E., Chawla, S., Cruzalegui, F. H., & Bading, H. (1999) · Neuron · doi:10.1016/s0896-6273(00)80737-0 · Cited by 273 · see citing works
Self-citationPapadia, S., Stevenson, P., Hardingham, N. R., Bading, H., & Hardingham, G. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5019-04.2005 · Cited by 262 · see citing works
Self-citationClass IIa histone deacetylases: regulating the regulators
Martin, M., Kettmann, R., & Dequiedt, F. (2007) · Oncogene · doi:10.1038/sj.onc.1210613 · Cited by 243 · see citing works
An Essential Role for Histone Deacetylase 4 in Synaptic Plasticity and Memory Formation
Kim, M.-S., Akhtar, M. W., Adachi, M., Mahgoub, M., Bassel-Duby, R., Kavalali, E. T., Olson, E. N., & Monteggia, L. M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2089-12.2012 · Cited by 235 · see citing works
Mechanism for Nucleocytoplasmic Shuttling of Histone Deacetylase 7
Kao, H., Verdel, A., Tsai, C., Simon, C. M., Juguilon, H., & Khochbin, S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107631200 · Cited by 223 · see citing works
Regulation of CBP-Mediated Transcription by Neuronal Calcium Signaling
Hu, S., Chrivia, J. C., & Ghosh, A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80738-2 · Cited by 222 · see citing works
A Dynamic Role for HDAC7 in MEF2-mediated Muscle Differentiation
Dressel, U., Bailey, P. J., Wang, S.-C., Downes, M., Evans, R. M., & Muscat, G. E. O. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101508200 · Cited by 212 · 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
The Histone Deacetylase HDAC4 Connects Neural Activity to Muscle Transcriptional Reprogramming
Cohen, T. J., Waddell, D. S., Barrientos, T., Lu, Z., Feng, G., Cox, G. A., Bodine, S. C., & Yao, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706268200 · Cited by 190 · see citing works
Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways
Riccio, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2671 · Cited by 185 · see citing works
Histone Deacetylase 4 Possesses Intrinsic Nuclear Import and Export Signals
Wang, A. H., & Yang, X. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.17.5992-6005.2001 · Cited by 180 · see citing works
Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated
Hardingham, G. E., & Bading, H. (2002) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/s1570-9639(02)00455-7 · Cited by 168 · see citing works
Self-citationLee, B., Butcher, G. Q., Hoyt, K. R., Impey, S., & Obrietan, K. H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4288-04.2005 · Cited by 165 · see citing works
Phosphorylation of c-Fos at the C-terminus enhances its transforming activity.
Chen, R. H., Juo, P., Curran, T., & Blenis, J. (1996) · PubMed · Cited by 160 · see citing works
Zhao, X., Ito, A., Kane, C. D., Liao, T.-S., Bolger, T. A., Lemrow, S. M., Means, A. R., & Yao, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105086200 · Cited by 151 · see citing works
Wiegert, J. S., & Bading, H. (2010) · Cell Calcium · doi:10.1016/j.ceca.2010.11.009 · Cited by 151 · see citing works
Self-citationLiu, Y., Randall, W. R., & Schneider, M. F. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200408128 · Cited by 150 · see citing works
Arnold, F. J. L., Hofmann, F., Bengtson, C. P., Wittmann, M., Vanhoutte, P., & Bading, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.077446 · Cited by 148 · see citing works
Self-citationRegulatory signal transduction pathways for class IIa histone deacetylases
Parra, M., & Verdin, E. M. (2010) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2010.04.004 · Cited by 147 · see citing works
Calcium Signaling in Synapse-to-Nucleus CommunicationPreprint
Hagenston, A. M., & Bading, H. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004564 · Cited by 140 · see citing works
Self-citationZhang, S., Buchthal, B., Lau, D., Hayer, S. N., Dick, O., Schwaninger, M., Veltkamp, R. C., Zou, M., Weiss, U. K., & Bading, H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2672-10.2011 · Cited by 137 · see citing works
Self-citationDavis, F. J., Gupta, M., Camoretti-Mercado, B., Schwartz, R. J., & Gupta, M. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209998200 · Cited by 132 · see citing works
Nucleoplasmic Calcium Is Required for Cell Proliferation
Rodrigues, M. Â., Gomes, D. A., Leite, M. F., Grant, W. M., Zhang, L., Lam, W., Cheng, Y., Bennett, A. M., & Nathanson, M. H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700490200 · Cited by 131 · see citing works
PP2A Regulates HDAC4 Nuclear Import
Paroni, G., Cernotta, N., Dello Russo, C., Gallinari, P., Pallaoro, M., Foti, C., Talamo, F., Orsatti, L., Steinkühler, C., & Brancolini, C. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-06-0623 · Cited by 126 · see citing works
Zhou, X., Richon, V. M., Rifkind, R. A., & Marks, P. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1056 · Cited by 120 · see citing works
Pusl, T., Wu, J. J., Zimmerman, T. L., Zhang, L., Ehrlich, B. E., Berchtold, M. W., Hoek, J. B., Karpen, S. J., Nathanson, M. H., & Bennett, A. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203002200 · Cited by 119 · see citing works
Nuclear Calcium/Calmodulin Regulates Memory Consolidation
Limbäck-Stokin, K., Korzus, E., Nagaoka-Yasuda, R., & Mayford, M. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1022-04.2004 · Cited by 114 · see citing works
Illi, B., Russo, C. D., Colussi, C., Rosati, J. D., Pallaoro, M., Spallotta, F., Rotili, D., Valente, S., Ragone, G., Martelli, F., et al. (2007) · Circulation Research · doi:10.1161/circresaha.107.157305 · Cited by 113 · see citing works
Simonetti, M., Hagenston, A. M., Vardeh, D., Freitag, H. E., Mauceri, D., Lu, J., Satagopam, V., Schneider, R., Costigan, M., Bading, H., et al. (2013) · Neuron · doi:10.1016/j.neuron.2012.10.037 · Cited by 112 · see citing works
Self-citationMauceri, D., Freitag, H. E., Oliveira, A. M. M., Bengtson, C. P., & Bading, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.022 · Cited by 98 · see citing works
Self-citationBookmarking the Genome: Maintenance of Epigenetic Information
Zaidi, S. K., Young, D. W., Montecino, M. A., van Wijnen, A. J., Stein, J. L., Lian, J. B., & Stein, G. S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.r110.197061 · Cited by 89 · see citing works
Wang, J., Campos, B., Jamieson, G. A., et al. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.51.30245 · Cited by 88 · see citing works
Histone Deacetylase 7 Promotes PML Sumoylation and Is Essential for PML Nuclear Body Formation
Gao, C., Ho, C.-C., Reineke, E. L., Lam, M. C., Cheng, X., Stanya, K. J., Liu, Y., Chakraborty, S., Shih, H.-M., & Kao, H. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00874-08 · Cited by 87 · see citing works
Cohen, T. J., Barrientos, T., Hartman, Z. C., Garvey, S. M., Cox, G. A., & Yao, T. (2008) · The FASEB Journal · doi:10.1096/fj.08-115931 · Cited by 86 · see citing works
Baltan, S., Bachleda, A., Morrison, R. S., & Murphy, S. P. (2011) · Translational Stroke Research · doi:10.1007/s12975-011-0087-z · Cited by 85 · see citing works
Sugo, N., Oshiro, H., Takemura, M., Kobayashi, T., Kohno, Y., Uesaka, N., Song, W., & Yamamoto, N. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07218.x · Cited by 85 · see citing works
Acetylation/Deacetylation Modulates the Stability of DNA Replication Licensing Factor Cdt1
Glozak, M. A., & Seto, E. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809394200 · Cited by 84 · see citing works
Nuclear Ca2+ regulates cardiomyocyte function
Guatimosim, S., Amaya, M. J., Guerra, M. T., Aguiar, C. J., Goes, A. M., Gómez-Viquez, N. L., Rodrigues, M. Â., Gomes, D. A., Martins-Cruz, J., Lederer, W. J., et al. (2008) · Cell Calcium · doi:10.1016/j.ceca.2007.11.016 · Cited by 81 · see citing works
Ma, C., & D’Mello, S. R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.146860 · Cited by 80 · see citing works
Chan, J. K. L., Sun, L., Yang, X., Zhu, G., & Wu, Z. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301922200 · Cited by 79 · see citing works
Complex, multimodal behavioral profile of the Homer1 knockout mouse
Jaubert, P. J., Golub, M. S., Lo, Y. Y., Germann, S. L., Dehoff, M. H., Worley, P. F., Kang, S. H., Schwarz, M. K., SEEBURG, P. H., & Berman, R. F. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00240.x · Cited by 75 · see citing works
Wiegert, J. S., Bengtson, C. P., & Bading, H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701448200 · Cited by 70 · see citing works
Self-citationTian, F., Hu, X., Wu, X., Jiang, H., Pan, H., Marini, A. M., & Lipsky, R. H. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06058.x · Cited by 70 · 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 · cited 1× · see citing works
“These observations are in agreement with previous studies on the subcellular localization of HDACs in the brain (39, 47).”
ResultBengtson, C. P., Freitag, H. E., Weislogel, J.-M., & Bading, H. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.10.044 · Cited by 65 · see citing works
Self-citationBuchthal, B., Lau, D., Weiss, U. K., Weislogel, J.-M., & Bading, H. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.382507 · Cited by 60 · see citing works
Self-citationAjamian, F., Suuronen, T., Salminen, A., & Reeben, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00545-7 · Cited by 38 · see citing works
Effects of histone acetylation and CpG methylation on the structure of nucleosomes
Lee, J. Y., & Lee, T.-H. (2012) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2012.05.006 · Cited by 37 · see citing works
Guan, Y. A., Chen, Q., Yang, X., Haines, P., Pei, M., Terek, R. M., Wei, X., Zhao, T., & Wei, L. (2012) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00348.2011 · Cited by 37 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
“140 Cytoplasmic localization of HDAC4 is maintained by HDAC phosphorylation, suppressing the binding of the transcription factor MEF2, 141 whereas HDAC4 dephosphorylation by calcineurin allows nuclear translocation.”
BackgroundEpigenetic 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
- Authors
- Schlumm, F., Mauceri, D., Freitag, H. E., & Bading, H.
- Affiliations
- Heidelberg University (DE)
- Corresponding author
- Bading, Hilmar
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2013-03
- Volume
- 288
- Issue
- 12
- Pages
- 8074-8084
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3605626
- OpenAlex
- W2040289150
- Cited by
- 76
- References
- 83
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 10 · 2023: 2 · 2022: 13 · 2021: 9 · 2020: 4 · 2019: 5 · 2018: 2 · 2017: 7 · 2016: 1 · 2015: 8 · 2014: 5 · 2013: 3
- FWCI
- 2.54
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Keywords
- nuclear calcium signaling, histone deacetylase, class IIa HDACs, HDAC4, HDAC5, nucleocytoplasmic shuttling, nuclear export, synaptic activity, hippocampal neurons, parvalbumin, action potential firing, calcium buffering, transcriptional regulation, memory consolidation, chronic pain, neuroprotection
- MeSH terms
- Animals, Cell Nucleus, Cells, Cultured, Cytoplasm, Gene Expression Regulation, Hippocampus, Histone Deacetylases, Humans, Mice, Inbred C57BL, Neurons, Parvalbumins, Repressor Proteins, Gene Expression, Amino Acid Substitution, Calcium Signaling, Active Transport, Cell Nucleus, Mice, Rats
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
