Histone Core Phosphorylation Regulates DNA Accessibility
Open accessAbstract
Nucleosome unwrapping dynamics provide transient access to the complexes involved in DNA transcription, repair, and replication, whereas regulation of nucleosome unwrapping modulates occupancy of these complexes. Histone H3 is phosphorylated at tyrosine 41 (H3Y41ph) and threonine 45 (H3T45ph). H3Y41ph is implicated in regulating transcription, whereas H3T45ph is involved in DNA replication and apoptosis. These modifications are located in the DNA-histone interface near where the DNA exits the nucleosome, and are thus poised to disrupt DNA-histone interactions. However, the impact of histone phosphorylation on nucleosome unwrapping and accessibility is unknown. We find that the phosphorylation mimics H3Y41E and H3T45E, and the chemically correct modification, H3Y41ph, significantly increase nucleosome unwrapping. This enhances DNA accessibility to protein binding by 3-fold. H3K56 acetylation (H3K56ac) is also located in the same DNA-histone interface and increases DNA unwrapping. H3K56ac is implicated in transcription regulation, suggesting that H3Y41ph and H3K56ac could function together. We find that the combination of H3Y41ph with H3K56ac increases DNA accessibility by over an order of magnitude. These results suggest that phosphorylation within the nucleosome DNA entry-exit region increases access to DNA binding complexes and that the combination of phosphorylation with acetylation has the potential to significantly influence DNA accessibility to transcription regulatory complexes.
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Histone phosphorylation mainly occurs on serine and threonine residues, though some studies have found that tyrosine residues also can be phosphorylated.
“Histone phosphorylation mainly occurs on serine and threonine residues, though some studies have found that tyrosine residues also can be phosphorylated.184”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [184]
Cites
Crystal structure of the nucleosome core particle at 2.8 Å resolution
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., & Richmond, T. J. (1997) · Nature · doi:10.1038/38444 · Cited by 9,466 · see citing works
Self-citationThe language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679 · see citing works
Regulation of chromatin by histone modifications
Bannister, A. J., & Kouzarides, T. (2011) · Cell Research · doi:10.1038/cr.2011.22 · Cited by 6,012 · see citing works
Chen, X., Xiu, M., Xing, J., Yu, S., Min, D., & Guo, F. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479439 · Cited by 5,759 · see citing works
Small-Angle Scattering of X-Rays
Guinier, A., Fournet, G., Walker, C. B., & Vineyard, G. H. (1956) · Physics Today · doi:10.1063/1.3060069 · Cited by 4,311 · see citing works
Svergun, D. I. (1992) · Journal of Applied Crystallography · doi:10.1107/s0021889892001663 · Cited by 3,876 · see citing works
PRIMUS: a Windows PC-based system for small-angle scattering data analysis
Konarev, P. V., Волков, В. В., Sokolova, A. V., Koch, M. H. J., & Svergun, D. I. (2003) · Journal of Applied Crystallography · doi:10.1107/s0021889803012779 · Cited by 2,850 · see citing works
Svergun, D. I. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77443-6 · Cited by 2,229 · see citing works
<i>DAMMIF</i> , a program for rapid <i>ab-initio</i> shape determination in small-angle scattering
Franke, D., & Svergun, D. I. (2009) · Journal of Applied Crystallography · doi:10.1107/s0021889809000338 · Cited by 2,021 · see citing works
Uniqueness of ab initio shape determination in small-angle scattering
Волков, В. В., & Svergun, D. I. (2003) · Journal of Applied Crystallography · doi:10.1107/s0021889803000268 · Cited by 1,980 · see citing works
Lowary, P. T., & Widom, J. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1494 · Cited by 1,782 · see citing works
Automated matching of high- and low-resolution structural models
Kozin, M. B., & Svergun, D. I. (2001) · Journal of Applied Crystallography · doi:10.1107/s0021889800014126 · Cited by 1,302 · see citing works
Regulation of nucleosome dynamics by histone modifications
Zentner, G. E., & Henikoff, S. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2470 · Cited by 923 · cited 1× · see citing works
“Peptides H3(47-90)A47Thz with or without K56ac and H3(1-46) with or without pY41 were prepared on Fmoc-Dbz(Alloc)-derivitized resin as described in (42) and cleaved and purified as the C-terminal N-acylurea derivatives.”
MethodReconstitution of Nucleosome Core Particles from Recombinant Histones and DNA
Dyer, P. N., Edayathumangalam, R. S., White, C. L., Bao, Y., Chakravarthy, S., Muthurajan, U. M., & Luger, K. (2003) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(03)75002-2 · Cited by 867 · see citing works
Self-citation[18] Fluorescence resonance energy transfer and nucleic acids
Clegg, R. M. (1992) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(92)11020-j · Cited by 736 · see citing works
Interpreting the language of histone and DNA modifications
Rothbart, S. B., & Strahl, B. D. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.03.001 · Cited by 721 · see citing works
CBP/p300-mediated acetylation of histone H3 on lysine 56
Das, C., Lucia, M. S., Hansen, K. C., & Tyler, J. K. (2009) · Nature · doi:10.1038/nature07861 · Cited by 698 · see citing works
Mechanisms and Functions of ATP-Dependent Chromatin-Remodeling Enzymes
Narlikar, G. J., Sundaramoorthy, R., & Owen‐Hughes, T. (2013) · Cell · doi:10.1016/j.cell.2013.07.011 · Cited by 659 · see citing works
Polach, K. J., & Widom, J. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0606 · Cited by 657 · see citing works
JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin
Dawson, M. A., Bannister, A. J., Göttgens, B., Foster, S. D., Bartke, T., Green, A. R., & Kouzarides, T. (2009) · Nature · doi:10.1038/nature08448 · Cited by 624 · see citing works
Neumann, H., Hancock, S. M., Buning, R., Routh, A. L., Chapman, L., Somers, J., Owen‐Hughes, T., van Noort, J., Rhodes, D., & Chin, J. W. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.07.027 · Cited by 498 · see citing works
Post-Translational Modifications of Histones That Influence Nucleosome Dynamics
Bowman, G., & Poirier, M. (2014) · Chemical Reviews · doi:10.1021/cr500350x · Cited by 461 · see citing works
Self-citationAcetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly
Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A., & Zhang, Z. (2008) · Cell · doi:10.1016/j.cell.2008.06.018 · Cited by 447 · see citing works
Chen, C., Carson, J. J., Feser, J., Tamburini, B. A. J., Zabaronick, S., Linger, J. G., & Tyler, J. K. (2008) · Cell · doi:10.1016/j.cell.2008.06.035 · Cited by 426 · see citing works
Regulated nucleosome mobility and the histone code
Cosgrove, M. S., Boeke, J. D., & Wolberger, C. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb851 · Cited by 421 · see citing works
Crystal structure of the human centromeric nucleosome containing CENP-A
Tachiwana, H., Kagawa, W., Shiga, T., Osakabe, A., Miya, Y., Saito, K., Hayashi‐Takanaka, Y., Oda, T., Sato, M., Park, S. Y., et al. (2011) · Nature · doi:10.1038/nature10258 · Cited by 396 · see citing works
Acetylation in Histone H3 Globular Domain Regulates Gene Expression in Yeast
Xu, F., Zhang, K., & Grunstein, M. R. (2005) · Cell · doi:10.1016/j.cell.2005.03.011 · Cited by 394 · see citing works
High-resolution dynamic mapping of histone-DNA interactions in a nucleosome
Hall, M. A., Shundrovsky, A., Bai, L., Fulbright, R. M., Lis, J. T., & Wang, M. D. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1526 · Cited by 385 · see citing works
Nucleosomes facilitate their own invasion
Li, G., & Widom, J. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb801 · Cited by 375 · see citing works
Histone chaperones, a supporting role in the limelight
Loyola, A., & Almouzni, G. (2003) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/j.bbaexp.2003.09.012 · Cited by 331 · see citing works
Asymmetric Unwrapping of Nucleosomes under Tension Directed by DNA Local Flexibility
Ngo, T. T. M., Zhang, Q., Zhou, R., Yodh, J. G., & Ha, T. (2015) · Cell · doi:10.1016/j.cell.2015.02.001 · Cited by 324 · see citing works
STRUCTURE, DYNAMICS, AND FUNCTION OF CHROMATIN IN VITRO
Widom, J. (1998) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.27.1.285 · Cited by 292 · see citing works
Human SWI/SNF Interconverts a Nucleosome between Its Base State and a Stable Remodeled State
Schnitzler, G. R., Sif, S., & Kingston, R. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81217-9 · Cited by 282 · see citing works
Small-Angle Scattering of X-Rays.
Beeman, W. W. (1956) · Journal of the American Chemical Society · doi:10.1021/ja01594a081 · Cited by 244 · see citing works
Histone Chaperones: Modulators of Chromatin Marks
Avvakumov, N., Nourani, A., & Côté, J. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.02.013 · Cited by 212 · see citing works
Regulating the Chromatin Landscape: Structural and Mechanistic Perspectives
Bartholomew, B. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-051810-093157 · Cited by 210 · see citing works
Histone fold modifications control nucleosome unwrapping and disassembly
Šimon, M., North, J. A., Shimko, J. C., Forties, R. A., Ferdinand, M. B., Manohar, M., Zhang, M., Fishel, R. A., Ottesen, J. J., & Poirier, M. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106264108 · Cited by 197 · see citing works
Self-citationXie, W., Song, C., Young, N. L., Sperling, A. S., Xu, F., Sridharan, R., Conway, A. E., Garcia, B. A., Plath, K., Clark, A. T., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.02.004 · Cited by 197 · see citing works
Wang, X., & Hayes, J. J. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01245-07 · Cited by 186 · see citing works
The histone shuffle: histone chaperones in an energetic dance
Das, C., Tyler, J. K., & Churchill, M. E. A. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.04.001 · Cited by 185 · see citing works
Luger, K. (2006) · Chromosome Research · doi:10.1007/s10577-005-1026-1 · Cited by 172 · see citing works
Self-citationProteomic characterization of novel histone post-translational modifications
Arnaudo, A. M., & Garcia, B. A. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-24 · Cited by 161 · see citing works
H3R42me2a is a histone modification with positive transcriptional effects
Casadio, F., Lu, X., Pollock, S. B., LeRoy, G., Garcia, B. A., Muir, T. W., Roeder, R. G., & Allis, C. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312925110 · Cited by 154 · see citing works
Shimko, J. C., North, J. A., Bruns, A. N., Poirier, M. G., & Ottesen, J. J. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.01.003 · Cited by 148 · see citing works
Self-citationSnf2-family proteins: chromatin remodellers for any occasion
Ryan, D., & Owen‐Hughes, T. (2011) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2011.07.022 · Cited by 140 · see citing works
Acetylation of Histone H3 at the Nucleosome Dyad Alters DNA-Histone Binding
Manohar, M., Mooney, A. M., North, J. A., Nakkula, R. J., Picking, J. W., Edon, A., Fishel, R. A., Poirier, M. G., & Ottesen, J. J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.003202 · Cited by 138 · see citing works
Self-citationGriffiths, D. S., Li, J., Dawson, M. A., Trotter, M. W. B., Cheng, Y., Smith, A. M., Mansfield, W. M., Liu, P., Kouzarides, T., Nichols, J., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2135 · Cited by 135 · see citing works
Regulation of the nucleosome unwrapping rate controls DNA accessibility
North, J. A., Shimko, J. C., Javaid, S., Mooney, A. M., Shoffner, M. A., Rose, S., Bundschuh, R. A., Fishel, R. A., Ottesen, J. J., & Poirier, M. G. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks747 · Cited by 117 · see citing works
Self-citationStructure and Scm3-mediated assembly of budding yeast centromeric nucleosomes
Dechassa, M. L., Wyns, K., Li, M., Hall, M. A., Wang, M. D., & Luger, K. (2011) · Nature Communications · doi:10.1038/ncomms1320 · Cited by 116 · see citing works
Self-citationPhosphorylation of Histone H3 Thr-45 Is Linked to Apoptosis
Hurd, P. J., Bannister, A. J., Halls, K., Dawson, M. A., Vermeulen, M., Olsen, J. V., Ismail, H. M., Somers, J., Mann, M., Owen‐Hughes, T., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.005421 · Cited by 113 · see citing works
Scratching the (lateral) surface of chromatin regulation by histone modifications
Tropberger, P., & Schneider, R. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2581 · Cited by 104 · see citing works
Baker, S. P., Phillips, J. V., Anderson, S., Qiu, Q., Shabanowitz, J., Smith, M. M., Yates, J. R., Hunt, D. F., & Grant, P. A. (2010) · Nature Cell Biology · doi:10.1038/ncb2030 · Cited by 89 · see citing works
Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency
Tan, Y., Xue, Y., Song, C., & Grunstein, M. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309914110 · Cited by 82 · see citing works
Phosphorylation of histone H3(T118) alters nucleosome dynamics and remodeling
North, J. A., Javaid, S., Ferdinand, M. B., Chatterjee, N., Picking, J. W., Shoffner, M. A., Nakkula, R. J., Bartholomew, B., Ottesen, J. J., Fishel, R. A., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr304 · Cited by 77 · see citing works
Self-citationMahto, S. K., Howard, C. J., Shimko, J. C., & Ottesen, J. J. (2011) · ChemBioChem · doi:10.1002/cbic.201100472 · Cited by 69 · see citing works
Self-citationRice, S. A. (1956) · Journal of Polymer Science · doi:10.1002/pol.1956.120199326 · Cited by 61 · see citing works
Three Distinct Patterns of Histone H3Y41 Phosphorylation Mark Active Genes
Dawson, M. A., Foster, S. D., Bannister, A. J., Robson, S. C., Hannah, R., Wang, X., Xhemalçe, B., Wood, A. D., Green, A. R., Göttgens, B., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.08.016 · Cited by 60 · see citing works
Yang, C., van der Woerd, M. J., Muthurajan, U. M., Hansen, J. C., & Luger, K. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr005 · Cited by 60 · see citing works
Self-citation[20] Cleavage of LexA repressor
Little, J. W., Kim, B., Roland, K. L., Smith, M. H., Lin, L.-L., & Slilaty, S. N. (1994) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(94)44022-0 · Cited by 58 · see citing works
Lo, K. A., Bauchmann, M., Baumann, A. P., Donahue, C. J., Thiede, M. A., Hayes, L. S., Etages, S. A. G. D., & Fraenkel, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019778 · Cited by 56 · see citing works
A quantitative model of nucleosome dynamics
Forties, R. A., North, J. A., Javaid, S., Tabbaa, O. P., Fishel, R. A., Poirier, M. G., & Bundschuh, R. A. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr422 · Cited by 52 · see citing works
Self-citationJang, S. M., Azébi, S., Soubigou, G., & Muchardt, C. (2014) · EMBO Reports · doi:10.15252/embr.201338356 · Cited by 49 · see citing works
Padinhateeri, R., Yan, J., & Marko, J. F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701459104 · Cited by 47 · see citing works
Histone H3 phosphorylation near the nucleosome dyad alters chromatin structure
North, J. A., Šimon, M., Ferdinand, M. B., Shoffner, M. A., Picking, J. W., Howard, C. J., Mooney, A. M., van Noort, J., Poirier, M. G., & Ottesen, J. J. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku150 · Cited by 46 · see citing works
Self-citationPreparing Semisynthetic and Fully Synthetic Histones H3 and H4 to Modify the Nucleosome Core
Shimko, J. C., Howard, C. J., Poirier, M. G., & Ottesen, J. J. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-305-3_14 · Cited by 21 · see citing works
Self-citation
Flagged first, then by citations
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Sorted by citations
Histone post-translational modifications - cause and consequence of genome function
Millán-Zambrano, G., Burton, A., Bannister, A. J., & Schneider, R. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00468-7 · Cited by 1,116 · see citing works
Nucleosome structure and dynamics are coming of age
Zhou, K., Gaullier, G., & Luger, K. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0166-x · Cited by 335 · see citing works
Self-citationYuan, 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
“Histone phosphorylation mainly occurs on serine and threonine residues, though some studies have found that tyrosine residues also can be phosphorylated.(184) Histone phosphorylation in the central nervous system is involved in stress response.”
BackgroundChromatin accessibility: biological functions, molecular mechanisms and therapeutic application
Chen, Y., Liang, R., Li, Y., Jiang, L., Ma, D., Luo, Q., & Song, G. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02030-9 · Cited by 174 · see citing works
Biophysics of Chromatin Dynamics
Fierz, B., & Poirier, M. G. (2019) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-070317-032847 · Cited by 137 · see citing works
Self-citationNuclear metabolism and the regulation of the epigenome
Boon, R., da Silveira, G. G., & Mostoslavsky, R. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00285-4 · Cited by 125 · see citing works
The role of cigarette smoke-induced pulmonary vascular endothelial cell apoptosis in COPD
Song, Q., Chen, P., & Liu, X. (2021) · Respiratory Research · doi:10.1186/s12931-021-01630-1 · Cited by 122 · see citing works
Histone Modifications and their Role in Colorectal Cancer (Review)
Qin, J., Wen, B., Liang, Y., Yu, W., & Li, H. (2019) · Pathology & Oncology Research · doi:10.1007/s12253-019-00663-8 · Cited by 121 · see citing works
Distortion of histone octamer core promotes nucleosome mobilization by a chromatin remodeler
Sinha, K. K., Gross, J. D., & Narlikar, G. J. (2017) · Science · doi:10.1126/science.aaa3761 · Cited by 110 · see citing works
Collemare, J., & Seidl, M. F. (2019) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuz018 · Cited by 101 · see citing works
Fenley, A. T., Anandakrishnan, R., Kidane, Y. H., & Onufriev, A. V. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0181-5 · Cited by 93 · see citing works
Epigenome Regulation by Dynamic Nucleosome Unwrapping
Brahma, S., & Henikoff, S. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2019.09.003 · Cited by 88 · see citing works
Functional crosstalk between histone H2B ubiquitylation and H2A modifications and variants
Wojcik, F., Dann, G. P., Beh, L. Y., Debelouchina, G. T., Hofmann, R., & Muir, T. W. (2018) · Nature Communications · doi:10.1038/s41467-018-03895-5 · Cited by 84 · see citing works
DeepHistone: a deep learning approach to predicting histone modifications
Yin, Q., Wu, M., Liu, Q., Lv, H., & Jiang, R. (2018) · BMC Genomics · doi:10.1186/s12864-019-5489-4 · Cited by 81 · see citing works
Ferioli, M., Zauli, G., Maiorano, P., Milani, D., Mirandola, P., & Neri, L. M. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28304 · Cited by 78 · see citing works
The nucleosome: from structure to function through physics
Onufriev, A. V., & Schießel, H. (2019) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2018.11.003 · Cited by 71 · see citing works
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Gómez, J. L. (2019) · Current Allergy and Asthma Reports · doi:10.1007/s11882-019-0886-y · Cited by 66 · see citing works
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Wu, M.-S., Li, X., Liu, C., Xu, Q., Huang, J., Gu, S., & Chen, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210922150043 · Cited by 53 · see citing works
Muthurajan, U. M., Mattiroli, F., Bergeron, S., Zhou, K., Gu, Y., Chakravarthy, S., Dyer, P. N., Irving, T. C., & Luger, K. (2016) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2016.01.002 · Cited by 51 · see citing works
Self-citationInhibition of CRISPR-Cas12a DNA targeting by nucleosomes and chromatin
Strohkendl, I., Saifuddin, F. A., Gibson, B. A., Rosen, M. K., Russell, R., & Finkelstein, I. J. (2021) · Science Advances · doi:10.1126/sciadv.abd6030 · Cited by 48 · see citing works
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Krajewski, W. A., Li, J., & Dou, Y. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky526 · Cited by 40 · see citing works
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Bui, M., Pitman, M., Nuccio, A. G., Roque, S., Donlin-Asp, P., Nita‐Lazar, A., Papoian, G. A., & Dalal, Y. (2017) · Epigenetics & Chromatin · doi:10.1186/s13072-017-0124-6 · Cited by 38 · see citing works
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Budziszewski, G. R., Zhao, Y., Spangler, C. J., Kedziora, K. M., Williams, M. R., Azzam, D. N., Skrajna, A., Koyama, Y., Cesmat, A. P., Simmons, H. C., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac198 · Cited by 34 · see citing works
Kohler, R. S., Anugraham, M., López, M. N., Xiao, C. S., Schoetzau, A., Hettich, T., Schlotterbeck, G., Fedier, A., Jacob, F., & Heinzelmann-Schwarz, V. A. (2016) · Oncotarget · doi:10.18632/oncotarget.10543 · Cited by 32 · see citing works
The Role of Epigenetics in the Chronic Sinusitis with Nasal Polyp
Liu, T., Sun, Y., & Bai, W. (2020) · Current Allergy and Asthma Reports · doi:10.1007/s11882-020-00976-8 · Cited by 31 · see citing works
Etier, A., Dumetz, F., Chéreau, S., & Ponts, N. (2022) · Toxins · doi:10.3390/toxins14050317 · Cited by 27 · see citing works
Gibson, M. D., Gatchalian, J., Slater, A., Kutateladze, T. G., & Poirier, M. G. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1320 · Cited by 26 · see citing works
Self-citationMolecular dynamics simulations of nucleosomes are coming of age
Fedulova, A. S., Armeev, G. A., Romanova, T. A., Singh‐Palchevskaia, L., Kosarim, N. A., Motorin, N. A., Komarova, G. A., & Shaytan, A. К. (2024) · Wiley Interdisciplinary Reviews Computational Molecular Science · doi:10.1002/wcms.1728 · Cited by 25 · see citing works
Donovan, B. T., Luo, Y., Meng, Z., & Poirier, M. G. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkac1267 · Cited by 25 · see citing works
Self-citationDynamics of histone H3 acetylation in the nucleosome core during mouse pre-implantation development
Ziegler-Birling, C., Daujat, S., Schneider, R., & Torres‐Padilla, M. (2015) · Epigenetics · doi:10.1080/15592294.2015.1103424 · Cited by 24 · see citing works
Advances and Opportunities in Epigenetic Chemical Biology
Beyer, J. N., Raniszewski, N. R., & Burslem, G. M. (2020) · ChemBioChem · doi:10.1002/cbic.202000459 · Cited by 23 · see citing works
Cai, Y., Liu, X., Shen, L., Wang, N., He, Y., Zhang, H., Wang, P., & Zhang, Z. (2022) · Molecular Plant Pathology · doi:10.1111/mpp.13225 · Cited by 21 · see citing works
Addressing the Possibility of a Histone-Like Code in Bacteria
Carabetta, V. J. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00442 · Cited by 19 · see citing works
Structural dynamics of nucleosome mediated by acetylations at H3K56 and H3K115,122
Rajagopalan, M., Balasubramanian, S., Ioshikhes, I. P., & Ramaswamy, A. (2016) · European Biophysics Journal · doi:10.1007/s00249-016-1191-5 · Cited by 18 · see citing works
Signaling‐to‐chromatin pathways in the immune system
de Paz, A. M., & Josefowicz, S. Z. (2021) · Immunological Reviews · doi:10.1111/imr.12955 · Cited by 18 · see citing works
Jing, Y., Li, X., Liu, Z., & Li, X. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.899013 · Cited by 19 · see citing works
Chemistry‐Driven Epigenetic Investigation of Histone and DNA Modifications
Sueoka, T., Koyama, K., Hayashi, G., & Okamoto, A. (2018) · The Chemical Record · doi:10.1002/tcr.201800040 · Cited by 17 · see citing works
Han, Z., Zhang, Z., Guan, Y., Chen, B., Yu, M., Zhang, L., Fang, J., Gao, Y., & Guo, Z. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.01.120 · Cited by 17 · see citing works
Regulation of Methyllysine Readers through Phosphorylation
Andrews, F. H., Gatchalian, J., Krajewski, K., Strahl, B. D., & Kutateladze, T. G. (2016) · ACS Chemical Biology · doi:10.1021/acschembio.5b00802 · Cited by 17 · see citing works
One-Pot Quantitative Top- and Middle-Down Analysis of GluC-Digested Histone H4
Holt, M. V., Wang, T., & Young, N. L. (2019) · Journal of the American Society for Mass Spectrometry · doi:10.1007/s13361-019-02219-1 · Cited by 16 · see citing works
Self-citationMechanisms of Histone Modifications
Vanzan, L., Sklias, A., Bošković, M., Herceg, Z., Murr, R., & Suter, D. M. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91909-8.00019-0 · Cited by 15 · see citing works
Histone modifications—models and mechanisms
Blakey, C. A., & Litt, M. D. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-799958-6.00002-0 · Cited by 14 · see citing works
DNA sequence influences hexasome orientation to regulate DNA accessibility
Brehove, M. S., Shatoff, E., Donovan, B. T., Jipa, C., Bundschuh, R. A., & Poirier, M. G. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz283 · Cited by 15 · see citing works
Self-citationNakatsu, K., Yanase, M., Hayashi, G., & Okamoto, A. (2020) · Organic Letters · doi:10.1021/acs.orglett.0c01450 · Cited by 14 · see citing works
Single-Molecule Techniques to Study Chromatin
Chanou, A., & Hamperl, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.699771 · Cited by 14 · see citing works
Bhan, A., Deb, P., & Mandal, S. S. (2017) · doi:10.1002/9783527697274.ch2 · Cited by 14 · see citing works
Nucleosomes and their complexes in the cryoEM era: Trends and limitations
Armeev, G. A., Gribkova, A. K., & Shaytan, A. К. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1070489 · Cited by 13 · see citing works
Li, Y., Quan, L., Zhou, Y., Jiang, Y., Li, K., Wu, T., & Lyu, Q. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac489 · Cited by 13 · see citing works
Noncanonical IFN Signaling: Mechanistic Linkage of Genetic and Epigenetic Events
Johnson, H. M., & Ahmed, C. M. I. (2016) · Mediators of Inflammation · doi:10.1155/2016/9564814 · Cited by 13 · see citing works
Noncanonical IFN Signaling, Steroids, and STATs: A Probable Role of V-ATPase
Johnson, H. M., Noon-Song, E. N., & Ahmed, C. M. I. (2019) · Mediators of Inflammation · doi:10.1155/2019/4143604 · Cited by 13 · see citing works
Dynamic Chromatin Regulation from a Single Molecule Perspective
Fierz, B. (2015) · ACS Chemical Biology · doi:10.1021/acschembio.5b00832 · Cited by 12 · see citing works
Ren, B., Tan, H. L., Nguyen, T. T. T., Sayed, A. M. M., Li, Y., Mok, Y., Yang, H. H., & Chen, E. S. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1010 · Cited by 12 · see citing works
Moritz, L., Schon, S. B., Rabbani, M., Sheng, Y., Pendlebury, D. F., Agrawal, R., Sultan, C., Jorgensen, K. C., Zheng, X., Diehl, A. G., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.16.460631 · Cited by 12 · see citing works
Mackler, R. M., Jones, N. D., Gardner, A. M., Lopez, M. A., Howard, C. J., Fishel, R. A., & Yoder, K. E. (2019) · PLoS ONE · doi:10.1371/journal.pone.0212764 · Cited by 10 · see citing works
Hi-CO: 3D genome structure analysis with nucleosome resolution
Ohno, M., Ando, T., Priest, D. G., & Taniguchi, Y. (2021) · Nature Protocols · doi:10.1038/s41596-021-00543-z · Cited by 11 · see citing works
Asim, M. N., Ibrahim, M. A., Malik, M. I., Razzak, I., Dengel, A. R., & Ahmed, S. (2022) · Complex & Intelligent Systems · doi:10.1007/s40747-022-00802-w · Cited by 11 · see citing works
Catching Nucleosome by Its Decorated Tails Determines Its Functional States
Sehrawat, P., Shobhawat, R., & Kumar, A. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.903923 · Cited by 9 · see citing works
Methods for Investigating DNA Accessibility with Single Nucleosomes
Gibson, M. D., Brehove, M. S., Luo, Y., North, J. A., & Poirier, M. G. (2016) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2016.08.014 · Cited by 9 · see citing works
Self-citationOnufriev, A. V. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1067787 · Cited by 8 · see citing works
Effects of DNA Superhelical Stress on the Stability of H2B-Ubiquitylated Nucleosomes.
Krajewski, W. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.09.014 · Cited by 8 · see citing works
Chikhirzhina, E. V., Starkova, T. Y., & Polyanichko, A. M. (2020) · BIOPHYSICS · doi:10.1134/s0006350920020049 · Cited by 8 · see citing works
Milestones in transcription and chromatin published in the Journal of Biological Chemistry
Gottesfeld, J. M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.tm118.004162 · Cited by 7 · see citing works
Alsaker, C., Breidt, F. J., & van der Woerd, M. J. (2018) · Journal of the American Statistical Association · doi:10.1080/01621459.2017.1408467 · Cited by 6 · see citing works
Kotlar, R. M., Jones, N. D., Senavirathne, G., Gardner, A. M., Messer, R. K., Tan, Y. Y., Rabe, A. J., Fishel, R. A., & Yoder, K. E. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100550 · Cited by 6 · see citing works
Gocek, N., Żabka, A., Wróblewski, M., & Polit, J. T. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010208 · Cited by 5 · see citing works
Yekta, R. F., Farahani, M., Koushki, M., & Dashatan, N. A. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1481426 · Cited by 5 · see citing works
Gao, Z., He, T., Zhang, P., Hu, X., Ge, M., Xu, Y.-Q., Wang, P., & Pan, H. (2024) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2024.2375372 · Cited by 5 · see citing works
Hong, Z. Z., Yu, R. R., Zhang, X., Webb, A. M., Burge, N. L., Poirier, M. G., & Ottesen, J. J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/661744 · Cited by 5 · see citing works
Self-citationHistone tetrasome dynamics affects chromatin transcription
Shi, X., Fedulova, A. S., Kotova, E., Maluchenko, N. V., Armeev, G. A., Chen, Q., Prasanna, C., Sivkina, A. L., Feofanov, A. V., Kirpichnikov, M. P., et al. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf356 · Cited by 3 · see citing works
Chromatin and epigenetic regulation in malignant tumors: A comprehensive review
Zhang, X., Liu, D., Chen, X., Li, T., & Wu, G. (2025) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.70005 · Cited by 3 · see citing works
Histone modifications across cancers: mechanisms, therapy and clinical translation
Lu, P., Chan, Y.-T., Kwok, C.-F., Li, Q., Jiang, Z., Xu, L., Feng, Z., Yuan, H., Zou, J., Xun, Y., et al. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02707-5 · Cited by 3 · see citing works
Induced Pluripotent Stem Cells
Mobley, A. S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-811014-0.00004-4 · Cited by 2 · see citing works
(2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29434 · Cited by 2 · see citing works
RetractedCrosstalk of Histone Modifications in the Healthy Human Immune SystemPreprint
Đermadi, D., Kalesinskas, L., Ganesan, A., Kuo, A. J., Cheung, P., Cheng, S., Dvorak, M., Scriba, T. J., Habtezion, A., Donato, M., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.21.477300 · Cited by 1 · see citing works
Epigenetic regulation via histone modifications in ovarian cancer
Li, J., & Huang, H. (2025) · International review of cytology · doi:10.1016/bs.ircmb.2025.08.003 · Cited by 1 · see citing works
Potential of Micronuclear Epigenetic Signatures in Analyses of Toxicity and Genomic Instability
Paul, S., Das, A., Bandyopadhyay, A. K., & Giri, A. K. (2026) · Cell Biology International · doi:10.1002/cbin.70142 · Cited by 1 · see citing works
Histone Surface Exposure Drives Nucleosome Stacking Diversity Through DNA Engagement in Trans
Mu, Z., & Huang, J. (2026) · Journal of Molecular Biology · doi:10.1016/j.jmb.2026.169774 · Cited by 1 · see citing works
Zhang, Z., Fan, X., Zhong, J., Jia, L., Han, Y., Yang, C., He, Z., Li, X., Yau, S., Wu, R., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-70070-6 · Cited by 1 · see citing works
La Nutrición como modulador epigenético y su papel en la prevención de enfermedades
Vasquez, E. D., Ramírez‐Moreno, E., Zafra‐Rojas, Q. Y., Cruz‐Cansino, N. D. S., & Delgado‐Olivares, L. (2021) · Educación y Salud Boletín Científico Instituto de Ciencias de la Salud Universidad Autónoma del Estado de Hidalgo · doi:10.29057/icsa.v9i18.6593 · Cited by 1 · see citing works
DNA Methylation in Polycystic Kidney Disease and Bio-distribution of the C3-G12 peptide
Bates, M. (2016) · Otago University Research Archive (University of Otago)
HDACi-induced DNA damage: identifying potential endpoints for safety assessment
Wang, W. (2016) · ORCA Online Research @Cardiff (Cardiff University)
Ahmed, C. M. I., & Johnson, H. M. (2017) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0000931.pub3
Histone kinases and phosphatases
Azizyan, M., Watson, N. A., & Higgins, J. M. G. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-19001-8.00006-4
- Authors
- Brehove, M., Wang, T., North, J., Luo, Y., Dreher, S. J., Shimko, J. C., Ottesen, J. J., Luger, K., & Poirier, M. G.
- Affiliations
- The Ohio State University (US)
- Colorado State University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Poirier, Michael G.
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2015-09
- Volume
- 290
- Issue
- 37
- Pages
- 22612-22621
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC4566235
- OpenAlex
- W1567904427
- Cited by
- 93
- References
- 65
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 4 · 2023: 3 · 2022: 11 · 2021: 12 · 2020: 7 · 2019: 14 · 2018: 12 · 2017: 5 · 2016: 12 · 2015: 3
- FWCI
- 4.63
- 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
- Howard Hughes Medical Institute
- National Institutes of Health (5p01gm088409-05)
- National Institute of General Medical Sciences (GM 088409, R01GM083055, GM083055, P01- GM088409, R01GM105404, R01GM096192)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- histone H3 phosphorylation, H3K56 acetylation, nucleosome unwrapping, DNA accessibility, histone modifications, transcriptional regulation, DNA replication, apoptosis
- MeSH terms
- Acetylation, DNA, Histones, Humans, Nucleosomes, Phosphorylation, Transcription, Genetic
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