Structural basis for recognition of H3K56-acetylated histone H3–H4 by the chaperone Rtt106
Open accessAbstract
Dynamic variations in the structure of chromatin influence virtually all DNA-related processes in eukaryotes and are controlled in part by post-translational modifications of histones. One such modification, the acetylation of lysine 56 (H3K56ac) in the amino-terminal α-helix (αN) of histone H3, has been implicated in the regulation of nucleosome assembly during DNA replication and repair, and nucleosome disassembly during gene transcription. In Saccharomyces cerevisiae, the histone chaperone Rtt106 contributes to the deposition of newly synthesized H3K56ac-carrying H3-H4 complex on replicating DNA, but it is unclear how Rtt106 binds H3-H4 and specifically recognizes H3K56ac as there is no apparent acetylated lysine reader domain in Rtt106. Here, we show that two domains of Rtt106 are involved in a combinatorial recognition of H3-H4. An N-terminal domain homodimerizes and interacts with H3-H4 independently of acetylation while a double pleckstrin-homology (PH) domain binds the K56-containing region of H3. Affinity is markedly enhanced upon acetylation of K56, an effect that is probably due to increased conformational entropy of the αN helix of H3. Our data support a mode of interaction where the N-terminal homodimeric domain of Rtt106 intercalates between the two H3-H4 components of the (H3-H4)(2) tetramer while two double PH domains in the Rtt106 dimer interact with each of the two H3K56ac sites in (H3-H4)(2). We show that the Rtt106-(H3-H4)(2) interaction is important for gene silencing and the DNA damage response.
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Rtt106, a fungal-specific histone chaperone, functions in histone deposition during DNA replication and transcription elongation in S. cerevisiae, and preferentially binds H3K56-acetylated histone H3-H4.
“Rtt106, a fungal-specific histone chaperone, functions in histone deposition during DNA replication and transcription elongation in S. cerevisiae, and preferentially binds H3K56-acetylated histone H3-H424–26.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [24]
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Cites
Sheldrick, G. M. (2007) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767307043930 · Cited by 87,861 · see citing works
[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475 · see citing works
<i>Coot</i> : model-building tools for molecular graphics
Emsley, P., & Cowtan, K. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444904019158 · Cited by 30,571 · see citing works
NMRPipe: A multidimensional spectral processing system based on UNIX pipes
Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., & Bax, A. (1995) · Journal of Biomolecular NMR · doi:10.1007/bf00197809 · Cited by 15,994 · see citing works
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse‐Kunstleve, R. W., Jiang, J., Kuszewski, J. J., Nilges, M., Pannu, N., et al. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998003254 · Cited by 15,720 · see citing works
Refinement of Macromolecular Structures by the Maximum-Likelihood Method
Murshudov, G. N., Vagin, A. A., & Dodson, E. J. (1997) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444996012255 · Cited by 14,671 · see citing works
Chromatin modifications and their function
Kouzarides, T. (2007) · Cell · doi:10.1016/j.cell.2007.02.005 · Cited by 10,883 · see citing works
MOLMOL: A program for display and analysis of macromolecular structures
Koradi, R., Billeter, M., & Kurt Wüthrich, A. (1996) · Journal of Molecular Graphics · doi:10.1016/0263-7855(96)00009-4 · Cited by 7,163 · see citing works
<i>PHENIX</i> : building new software for automated crystallographic structure determination
Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., & Terwilliger, T. C. (2002) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444902016657 · Cited by 4,361 · see citing works
Automated protein model building combined with iterative structure refinement.
Perrakis, A., Morris, R. J., & Lamzin, V. S. (1999) · Nature Structural Biology · doi:10.1038/8263 · Cited by 2,423 · see citing works
Minor, W., Cymborowski, M., Otwinowski, Z., & Chruszcz, M. (2006) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444906019949 · Cited by 2,118 · see citing works
The Tandem Affinity Purification (TAP) Method: A General Procedure of Protein Complex Purification
Puig, Ó., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado‐Nilsson, E., Wilm, M. S., & Séraphin, B. (2001) · Methods · doi:10.1006/meth.2001.1183 · Cited by 1,784 · see citing works
Structure and ligand of a histone acetyltransferase bromodomain
Dhalluin, C., Carlson, J. E., Zeng, L., He, C., Aggarwal, A. K., Zhou, M.-M., & Zhou, M.-M. (1999) · Nature · doi:10.1038/20974 · Cited by 1,732 · see citing works
Elevated recombination rates in transcriptionally active DNA
Thomas, B. J., & Rothstein, R. J. (1989) · Cell · doi:10.1016/0092-8674(89)90584-9 · Cited by 1,633 · see citing works
Likelihood-enhanced fast rotation functions
Storoni, L. C., McCoy, A. J., & Read, R. J. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444903028956 · Cited by 1,177 · see citing works
Hendrickson, W. A., Horton, J. R., & LeMaster, D. M. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb08287.x · Cited by 1,015 · see citing works
Preparation of nucleosome core particle from recombinant histones
Luger, K., Rechsteiner, T. J., & Richmond, T. J. (1999) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(99)04003-3 · Cited by 779 · 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
SOLVE and RESOLVE: Automated Structure Solution and Density Modification
Terwilliger, T. C. (2003) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(03)74002-6 · Cited by 466 · see citing works
Acetylation 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
Self-citationChen, 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
White, C. L., Suto, R. K., & Luger, K. (2001) · The EMBO Journal · doi:10.1093/emboj/20.18.5207 · Cited by 410 · see citing works
Screen for DNA‐damage‐responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells
Tjeertes, J. V., Miller, K. M., & Jackson, S. P. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.119 · Cited by 347 · see citing works
Histone H3-K56 acetylation is important for genomic stability in mammals
Yuan, J., Pu, M., Zhang, Z., & Lou, Z. (2009) · Cell Cycle · doi:10.4161/cc.8.11.8620 · Cited by 247 · see citing works
Self-citationNMR spectroscopy: a multifaceted approach to macromolecular structure
Ferentz, A. E., & Wagner, G. (2000) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583500003589 · Cited by 239 · see citing works
Williams, S. K., Truong, D. M., & Tyler, J. K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800057105 · Cited by 218 · see citing works
Xie, 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
Luger, K. (2006) · Chromosome Research · doi:10.1007/s10577-005-1026-1 · Cited by 172 · see citing works
The PH superfold: a structural scaffold for multiple functions
Blomberg, N., Baraldi, E., Nilges, M., & Saraste, M. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01472-3 · Cited by 166 · see citing works
Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information
Corpet, A., & Almouzni, G. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.10.002 · Cited by 152 · see citing works
VanDemark, A. P., Blanksma, M. C., Ferris, E., Heroux, A., Hill, C. P., & Formosa, T. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.03.025 · Cited by 144 · see citing works
Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing
Huang, S., Zhou, H., Katzmann, D., Hochstrasser, M., Atanasova, E., & Zhang, Z. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506176102 · Cited by 130 · see citing works
Self-citationHuang, R., Holbert, M. A., Tarrant, M. K., Curtet, S., Colquhoun, D. R., Rabbitts, B. M., Dancy, B. C. R., Hwang, Y., Tang, Y., Meeth, K. M., et al. (2010) · Journal of the American Chemical Society · doi:10.1021/ja103954u · Cited by 116 · see citing works
Bowman, A. J., Ward, R., Mkami, H. E., Owen‐Hughes, T., & Norman, D. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1003 · Cited by 105 · see citing works
Structural Basis of BACH1 Phosphopeptide Recognition by BRCA1 Tandem BRCT Domains
Botuyan, M. V., Nominé, Y., Yu, X., Juranić, N., Macura, S. I., Chen, J., & Mer, G. (2004) · Structure · doi:10.1016/j.str.2004.06.002 · Cited by 97 · see citing works
Self-citationA novel role for histone chaperones CAF‐1 and Rtt106p in heterochromatin silencing
Huang, S., Zhou, H., Tarara, J., & Zhang, Z. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601670 · Cited by 77 · see citing works
Self-citationZhou, H., Madden, B. J., Muddiman, D. C., & Zhang, Z. (2006) · Biochemistry · doi:10.1021/bi0521083 · Cited by 73 · see citing works
Self-citationStructural Analysis of Rtt106p Reveals a DNA Binding Role Required for Heterochromatin Silencing
Liu, Y., Huang, H., Zhou, B. O., Wang, S., Hu, Y., Li, X., Liu, J., Zang, J., Niu, L., Wu, J., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.055996 · Cited by 39 · see citing works
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Histone core modifications regulating nucleosome structure and dynamics
Tessarz, P., & Kouzarides, T. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3890 · Cited by 1,018 · see citing works
Histone exchange, chromatin structure and the regulation of transcription
Venkatesh, S., & Workman, J. L. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3941 · Cited by 940 · see citing works
Perceiving the epigenetic landscape through histone readers
Musselman, C. A., Lalonde, M., Côté, J., & Kutateladze, T. G. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2436 · Cited by 840 · see citing works
Histone chaperone networks shaping chromatin function
Hammond, C. M., Strømme, C. B., Huang, H., Patel, D. J., & Groth, A. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.159 · Cited by 528 · 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
AF9 YEATS Domain Links Histone Acetylation to DOT1L-Mediated H3K79 Methylation
Li, Y., Wen, H., Xi, Y., Tanaka, K. Y., Wang, H., Peng, D., Ren, Y.-F., Jin, Q., Dent, S., Li, W., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.049 · Cited by 383 · see citing works
Histone chaperones in nucleosome assembly and human disease
Burgess, R. J., & Zhang, Z. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2461 · Cited by 383 · see citing works
Self-citationDrug Discovery Targeting Bromodomain-Containing Protein 4
Liu, Z., Wang, P., Chen, H., Wold, E. A., Tian, B., Brasier, A. R., & Zhou, J. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b01761 · Cited by 325 · see citing works
Readout of Epigenetic Modifications
Patel, D. J., & Wang, Z. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-072711-165700 · Cited by 315 · see citing works
Emerging roles for chromatin as a signal integration and storage platform
Badeaux, A. I., & Shi, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3545 · Cited by 291 · see citing works
Protein acylation: mechanisms, biological functions and therapeutic targets
Shang, S., Liu, J., & Hua, F. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01245-y · Cited by 247 · see citing works
Beyond histone acetylation—writing and erasing histone acylations
Zhao, S., Zhang, X., & Li, H. (2018) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2018.10.001 · Cited by 207 · see citing works
Transcription-associated histone modifications and cryptic transcription
Smolle, M. M., & Workman, J. L. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.08.008 · Cited by 203 · see citing works
Disrupting Acetyl-Lysine Recognition: Progress in the Development of Bromodomain Inhibitors
Romero, F. A., Taylor, A. M., Crawford, T. D., Tsui, V., Côté, A., & Magnuson, S. R. (2015) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.5b01514 · Cited by 194 · see citing works
Lu, C. T., Huang, K.-Y., Su, M.-G., Lee, T.-Y., Bretaña, N. A., Chang, W., Chen, Y., Chen, Y., & Huang, H.-D. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1229 · Cited by 193 · see citing works
m5C modification of mRNA serves a DNA damage code to promote homologous recombination
Chen, H., Yang, H., Zhu, X., Yadav, T., Ouyang, J., Truesdell, S. S., Tan, J. J., Wang, Y., Duan, M.-H., Wei, L., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16722-7 · Cited by 181 · see citing works
Structural basis of histone H2A–H2B recognition by the essential chaperone FACT
Hondele, M., Stuwe, T., Hassler, M., Halbach, F., Bowman, A. J., Zhang, E., Nijmeijer, B., Kotthoff, C., Rybin, V., Amlacher, S., et al. (2013) · Nature · doi:10.1038/nature12242 · Cited by 181 · see citing works
Pleckstrin homology (PH) like domains – versatile modules in protein–protein interaction platforms
Scheffzek, K., & Welti, S. (2012) · FEBS Letters · doi:10.1016/j.febslet.2012.06.006 · Cited by 141 · see citing works
Mechanisms of BRCA1–BARD1 nucleosome recognition and ubiquitylation
Hu, Q., Botuyan, M. V., Zhao, D., Cui, G., Mer, E., & Mer, G. (2021) · Nature · doi:10.1038/s41586-021-03716-8 · Cited by 137 · see citing works
Self-citationA Cul4 E3 Ubiquitin Ligase Regulates Histone Hand-Off during Nucleosome Assembly
Han, J., Zhang, H., Zhang, H., Wang, Z., Zhou, H., & Zhang, Z. (2013) · Cell · doi:10.1016/j.cell.2013.10.014 · Cited by 130 · see citing works
Self-citationAcetylation Reader Proteins: Linking Acetylation Signaling to Genome Maintenance and Cancer
Gong, F., Chiu, L.-Y., & Miller, K. M. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006272 · Cited by 132 · see citing works
Replication-Coupled Nucleosome Assembly in the Passage of Epigenetic Information and Cell Identity
Serra‐Cardona, A., & Zhang, Z. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.12.003 · Cited by 128 · see citing works
Self-citationThe Histone Chaperone FACT Contributes to DNA Replication-Coupled Nucleosome Assembly
Yang, J., Zhang, X., Feng, J., Leng, H., Li, S., Xiao, J., Liu, S., Xu, Z., Xu, J., Li, D., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.096 · Cited by 114 · see citing works
Self-citationExpression homeostasis during DNA replication
Voichek, Y., Bar‐Ziv, R., & Barkai, N. (2016) · Science · doi:10.1126/science.aad1162 · Cited by 105 · see citing works
Sauer, P. V., Gu, Y., Liu, W. H., Mattiroli, F., Panne, D., Luger, K., & Churchill, M. E. A. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky823 · Cited by 91 · see citing works
Liu, W. H., Roemer, S. C., Port, A. M., & Churchill, M. E. A. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks906 · Cited by 91 · see citing works
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Winkler, D. D., Zhou, H., Dar, M. A., Zhang, Z., & Luger, K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks812 · Cited by 82 · see citing works
Self-citationRetractedNovel strategies targeting bromodomain-containing protein 4 (BRD4) for cancer drug discovery
Liang, D., Yu, Y., & Ma, Z. (2020) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2020.112426 · Cited by 72 · see citing works
Liu, W. H., Roemer, S. C., Zhou, Y., Shen, Z.-J., Dennehey, B. K., Balsbaugh, J. L., Liddle, J. C., Nemkov, T. G., Ahn, N. G., Hansen, K. C., et al. (2016) · eLife · doi:10.7554/elife.18023 · Cited by 71 · see citing works
Epigenetic regulation of cardiac fibrosis
Stratton, M. S., & McKinsey, T. A. (2016) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2016.02.011 · Cited by 66 · see citing works
Targeted protein posttranslational modifications by chemically induced proximity for cancer therapy
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Yadav, T., & Whitehouse, I. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.059 · Cited by 62 · see citing works
Bromodomains in Protozoan Parasites: Evolution, Function, and Opportunities for Drug Development
Jeffers, V., Yang, C., Huang, S., & Sullivan, W. J. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00047-16 · Cited by 62 · see citing works
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Self-citationRegulating Chromatin by Histone Acetylation
Steunou, A., Rossetto, D., & Côté, J. (2013) · Springer eBooks · doi:10.1007/978-1-4614-8624-4_4 · Cited by 54 · see citing works
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Fazly, A., Li, Q., Hu, Q., Mer, G., Horazdovsky, B. F., & Zhang, Z. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.347450 · Cited by 56 · see citing works
Self-citationSelective binding of the PHD6 finger of MLL4 to histone H4K16ac links MLL4 and MOF
Zhang, Y., Jang, Y., Lee, J., Ahn, J., Xu, L., Holden, M. R., Cornett, E. M., Krajewski, K., Klein, B. J., Wang, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10324-8 · Cited by 52 · see citing works
The replisome guides nucleosome assembly during DNA replication
Zhang, W., Feng, J., & Li, Q. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00398-z · Cited by 50 · see citing works
Self-citationMultisite Substrate Recognition in Asf1-Dependent Acetylation of Histone H3 K56 by Rtt109
Zhang, L., Serra‐Cardona, A., Zhou, H., Wang, M., Yang, N., Zhang, Z., & Xu, R.-M. (2018) · Cell · doi:10.1016/j.cell.2018.07.005 · Cited by 48 · see citing works
Self-citationWriters, Readers, and Erasers of Epigenetic Marks
Nicholson, T. B., Veland, N., & Chen, T. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800206-3.00003-3 · Cited by 45 · see citing works
Dahlin, J. L., Chen, X., Walters, M. A., & Zhang, Z. (2014) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2014.978975 · Cited by 44 · see citing works
Self-citationRepair of replication-dependent double-strand breaks differs between the leading and lagging strands
Kimble, M. T., Sane, A., Reid, R. J. D., Johnson, M. J., Rothstein, R. J., & Symington, L. S. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.10.032 · Cited by 41 · see citing works
Rtt105 functions as a chaperone for replication protein A to preserve genome stability
Li, S., Xu, Z., Xu, J., Zuo, L., Yu, C., Zheng, P., Gan, H., Wang, X., Li, L., Sharma, S., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201899154 · Cited by 39 · see citing works
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Andrews, F. H., Shanle, E. K., Strahl, B. D., & Kutateladze, T. G. (2016) · Transcription · doi:10.1080/21541264.2015.1125987 · Cited by 38 · see citing works
Hu, J., Wang, Y.-Q., Li, Y., Xu, L., Cao, D., Song, S., Damaneh, M. S., Wang, X., Meng, T., Chen, Y.-L., et al. (2017) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2017.05.049 · Cited by 37 · see citing works
Mei, Q., Xu, C., Gogol, M., Tang, J., Chen, W., Yu, X., Workman, J. L., & Li, S. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz101 · Cited by 35 · see citing works
DeNizio, J. E., Elsässer, S. J., & Black, B. E. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku090 · Cited by 34 · see citing works
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Zhang, W., Zeng, F., Liu, Y., Shao, C., Li, S., Lv, H., Shi, Y., Niu, L., Teng, M., & Li, X. (2015) · Scientific Reports · doi:10.1038/srep18688 · Cited by 34 · see citing works
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Qi, Y., He, Q., Ai, H., Guo, J., & Li, J. (2017) · Chemical Communications · doi:10.1039/c7cc01721a · Cited by 32 · see citing works
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Hondele, M., & Ladurner, A. G. (2013) · Nucleus · doi:10.4161/nucl.27235 · Cited by 31 · see citing works
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T herapeutic targeting of chromatin: status and opportunities
Siklos, M. I., & Kubicek, S. (2021) · FEBS Journal · doi:10.1111/febs.15966 · Cited by 28 · see citing works
Mechanisms of RNF168 nucleosome recognition and ubiquitylation
Hu, Q., Zhao, D., Cui, G., Bhandari, J., Thompson, J. R., Botuyan, M. V., & Mer, G. (2024) · Molecular Cell · doi:10.1016/j.molcel.2023.12.036 · Cited by 28 · see citing works
Self-citationSimoneau, A., Delgoshaie, N., Celic, I., Dai, J., Abshiru, N. A., Costantino, S., Thibault, P., Boeke, J. D., Verreault, A., & Würtele, H. (2015) · Genetics · doi:10.1534/genetics.115.175919 · Cited by 26 · see citing works
The HIRA histone chaperone complex subunit UBN1 harbors H3/H4- and DNA-binding activity
Ricketts, M. D., Dasgupta, N., Fan, J., Han, J., Gerace, M., Tang, Y., Black, B. E., Adams, P. D., & Marmorstein, R. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007480 · Cited by 24 · see citing works
Dynamic association of PfEMP1 and KAHRP in knobs mediates cytoadherence during Plasmodium invasion
Ganguly, A. K., Ranjan, P., Kumar, A., & Bhavesh, N. S. (2015) · Scientific Reports · doi:10.1038/srep08617 · Cited by 23 · see citing works
Mechanistic and structural insights into histone H2A–H2B chaperone in chromatin regulation
Huang, Y., Dai, Y., & Zhou, Z. (2020) · Biochemical Journal · doi:10.1042/bcj20190852 · Cited by 23 · see citing works
Zunder, R. M., & Rine, J. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00871-12 · Cited by 22 · see citing works
Crystal structure of DPF3b in complex with an acetylated histone peptide
Li, W., Zhao, A., Tempel, W., Loppnau, P., & Liu, Y. (2016) · Journal of Structural Biology · doi:10.1016/j.jsb.2016.07.001 · Cited by 22 · 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
Identification of Elg1 interaction partners and effects on post-replication chromatin re-formation
Gali, V. K., Dickerson, D. R., Katou, Y., Fujiki, K., Shirahige, K., Owen‐Hughes, T., Kubota, T., & Donaldson, A. D. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007783 · Cited by 21 · see citing works
Structural characterization of the Asf1–Rtt109 interaction and its role in histone acetylation
Lercher, L., Danilenko, N., Kirkpatrick, J., & Carlomagno, T. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1283 · Cited by 21 · see citing works
Manipulation of the host protein acetylation network by human immunodeficiency virus type 1.
Jeng, M. Y., Ali, I., & Ott, M. (2015) · PubMed · doi:10.3109/10409238.2015.1061973 · Cited by 19 · see citing works
Xu, L., Cheng, A., Huang, M., Zhang, J., Jiang, Y., Wang, C., Li, F., Bao, H., Gao, J., Wang, N., et al. (2017) · FEBS Journal · doi:10.1111/febs.14198 · Cited by 19 · see citing works
Structure and function of histone chaperone FACT
Bondarenko, M. T., Maluchenko, N. V., Valieva, M. E., Gerasimova, N. S., Kulaeva, O. I., Georgiev, P. G., & Studitsky, V. M. (2015) · Molecular Biology · doi:10.1134/s0026893315060023 · Cited by 18 · see citing works
Ramos, I., Fernández‐Rivero, N., Arranz, R., Aloria, K., Finn, R. M., Arizmendi, J. M., Ausió, J., Valpuesta, J., Muga, A., & Prado, A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt899 · Cited by 17 · see citing works
Zhang, H., Lu, P., Tang, H.-L., Yan, H.-J., Jiang, W., Shi, H., Chen, S.-Y., Gao, M.-M., Zeng, X.-D., & Long, Y.-S. (2020) · Cellular and molecular neurobiology · doi:10.1007/s10571-020-00895-2 · Cited by 17 · see citing works
Gazy, I., Liefshitz, B., Bronstein, A. M., Parnas, O., Atias, N., Sharan, R., & Kupiec, M. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.113.005561 · Cited by 17 · see citing works
Структура и функции шаперона гистонов FACT
Bondarenko, M. T., Малюченко, Н. В., Valieva, M. E., Gerasimova, N. S., Kulaeva, O. I., Georgiev, P. G., & Студитский, В. М. (2015) · Molecular Biology · doi:10.7868/s0026898415060026 · Cited by 17 · see citing works
Nikolov, V. N., Malavia, D., & Kubota, T. (2022) · Nature Communications · doi:10.1038/s41467-022-29591-z · Cited by 16 · see citing works
Structure-specific recognition protein-1 (SSRP1) is an elongated homodimer that binds histones
Marcianò, G., Vela, S. D., Tria, G., Svergun, D. I., Byron, O., & Huang, D. T. C. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000994 · Cited by 16 · see citing works
McCullough, L. L., Pham, T. H., Parnell, T. J., Connell, Z., Chandrasekharan, M. B., Stillman, D. J., & Formosa, T. (2019) · Genetics · doi:10.1534/genetics.118.301853 · Cited by 15 · see citing works
Chromatin balances cell redox and energy homeostasis
Suganuma, T., & Workman, J. L. (2023) · Epigenetics & Chromatin · doi:10.1186/s13072-023-00520-8 · Cited by 14 · see citing works
Gershon, L., & Kupiec, M. (2021) · Genes · doi:10.3390/genes12030342 · Cited by 12 · see citing works
Peil, K., Jürgens, H., Luige, J., Kristjuhan, K., & Kristjuhan, A. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00347-7 · Cited by 12 · see citing works
H3K56 acetylation regulates chromatin maturation following DNA replication
Duan, S., Nodelman, I. M., Zhou, H., Tsukiyama, T., Bowman, G. D., & Zhang, Z. (2025) · Nature Communications · doi:10.1038/s41467-024-55144-7 · Cited by 11 · see citing works
Self-citationImpacts on Sirtuin Function and Bioavailability of the Dietary Bioactive Compound Dihydrocoumarin
Jacobi, J. L., Yang, B. H., Li, X., Menze, A. K., Laurentz, S., Janle, E. M., Ferruzzi, M. G., McCabe, G. P., Chapple, C. C. S., & Kirchmaier, A. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149207 · Cited by 11 · see citing works
A role for Rtt109 in buffering gene-dosage imbalance during DNA replication
Voichek, Y., Bar‐Ziv, R., & Barkai, N. (2016) · Nucleus · doi:10.1080/19491034.2016.1216743 · Cited by 8 · see citing works
Cac1 WHD and PIP domains have distinct roles in replisome progression and genomic stability
Tsirkas, I., Dovrat, D., Yang, L., Kalyva, A., Lotysh, D., Li, Q., & Aharoni, A. (2020) · Current Genetics · doi:10.1007/s00294-020-01113-8 · Cited by 9 · see citing works
Self-citationChromatin dynamics and DNA replication roadblocks
Hammond-Martel, I., Verreault, A., & Würtele, H. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103140 · Cited by 8 · see citing works
Histone exchange: sculpting the epigenome
Terweij, M., & van Leeuwen, F. (2013) · Frontiers in Life Science · doi:10.1080/21553769.2013.838193 · Cited by 7 · see citing works
Histone Chaperones in the Assembly and Disassembly of Chromatin
Dennehey, B. K., & Tyler, J. K. (2013) · Springer eBooks · doi:10.1007/978-1-4614-8624-4_2 · Cited by 6 · see citing works
Valero, M. L., Sendra, R., & Pamblanco, M. (2016) · Journal of Proteomics · doi:10.1016/j.jprot.2016.01.004 · Cited by 7 · see citing works
Replication-coupled inheritance of chromatin states
Song, A., Wang, Y., Liu, C., Yu, J., Zhang, Z., Lan, L., Lin, H., Zhao, J., & Li, G. (2024) · Cell Insight · doi:10.1016/j.cellin.2024.100195 · Cited by 6 · see citing works
Self-citationStructure and function of histone chaperones in replication-coupled chromatin assembly
Liu, C.-P., & Xu, R.-M. (2025) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2025.103059 · Cited by 6 · see citing works
Young, T. J., Cui, Y., Pfeffer, C. M., Hobbs, E., Liu, W., Irudayaraj, J., & Kirchmaier, A. L. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1009226 · Cited by 6 · see citing works
Burgess, R. J., Han, J., & Zhang, Z. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.552463 · Cited by 5 · see citing works
Self-citationLiu, H., Wang, P., Liu, L., Min, Z., Luo, K., & Wan, Y. (2015) · Scientific Reports · doi:10.1038/srep15583 · Cited by 5 · see citing works
The Role of the MCM2-7 Helicase Subunit MCM2 in Epigenetic Inheritance
Jia, J., & Yu, C. (2024) · Biology · doi:10.3390/biology13080572 · Cited by 4 · see citing works
Epigenetic regulation of Epstein–Barr virus: From bench to bedside
Gao, X. Y., Yang, H.-X., Cheng, S., Cai, H., Xiong, J., & Zhao, W. (2024) · Clinical and Translational Discovery · doi:10.1002/ctd2.357 · Cited by 4 · see citing works
Bragantini, B., Charron, C., Bourguet, M., Paul, A., Tiotiu, D., Rothé, B., Marty, H., Terral, G., Hessmann, S., Decourty, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22077-4 · Cited by 4 · see citing works
Structural insights into multifunctionality of human FACT complex subunit hSSRP1
Li, X., Li, H., Jing, Q., Wang, M., Hu, T., Li, L., Zhang, Q., Liu, M., Fu, Y. V., Han, J., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101360 · Cited by 3 · see citing works
Self-citationEpigenetic Reprogramming of the Glucose Metabolic Pathways by the Chromatin Effectors During Cancer
Mondal, P., Tiwary, N., Sengupta, A., Dhang, S., Roy, S., & Das, C. (2022) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-07634-3_9 · Cited by 3 · see citing works
Histone Recognition by Tandem Modules and Modulation by Multiple PTMs
Li, H., Zhao, S., & Patel, D. J. (2015) · Springer eBooks · doi:10.1007/978-3-319-18102-8_7 · Cited by 3 · see citing works
The Journey of Histones: Molecular Mechanisms of the Histone Chaperoning Cascade
Cho, C., & Song, J. (2026) · Biochemistry · doi:10.1021/acs.biochem.6c00070 · Cited by 1 · see citing works
- Authors
- Su, D., Hu, Q., Li, Q., Thompson, J. R., Cui, G., Fazly, A., Davies, B. A., Botuyan, M. V., Zhang, Z., & Mer, G.
- Affiliations
- Mayo Clinic (US)
- Corresponding author
- Zhang, Zhiguo
- Mer, Georges
- ORCID
- Venue
- Nature
- Published
- 2012-02-05
- Volume
- 483
- Issue
- 7387
- Pages
- 104-107
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3439842
- OpenAlex
- W2046725709
- Cited by
- 128
- References
- 38
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 8 · 2023: 3 · 2022: 4 · 2021: 10 · 2020: 10 · 2019: 6 · 2018: 9 · 2017: 10 · 2016: 13 · 2015: 12 · 2014: 8 · 2013: 15 · 2012: 11
- FWCI
- 5.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Cancer Institute (P50CA108961, R01CA132878)
- National Institute of General Medical Sciences (R01GM072719)
- 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 › DNA Repair Mechanisms
- Keywords
- H3K56 acetylation, histone chaperone, nucleosome assembly, DNA replication, pleckstrin homology domain, histone acetylation, chromatin structure, Saccharomyces cerevisiae, histone deposition, conformational entropy
- MeSH terms
- Acetylation, Animals, Binding Sites, DNA Damage, Histones, Lysine, Models, Molecular, Mutation, Magnetic Resonance Spectroscopy, Protein Binding, Saccharomyces cerevisiae, Structure-Activity Relationship, Substrate Specificity, Xenopus laevis, Protein Structure, Tertiary, Crystallography, X-Ray, Pliability, Molecular Chaperones, Gene Silencing, Saccharomyces cerevisiae Proteins, Genomic Instability, Protein Multimerization
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