Synergistic effects of H3 and H4 nucleosome tails on structure and dynamics of a lesion-containing DNA: Binding of a displaced lesion partner base to the H3 tail for GG-NER recognition

Cai, Yuqin; Fu, Iwen; Geacintov, Nicholas E.; Zhang, Yingkai; Broyde, Suse

doi:10.1016/j.dnarep.2018.02.009

Title: Synergistic effects of H3 and H4 nucleosome tails on structure and dynamics of a lesion-containing DNA: Binding of a displaced lesion partner base to the H3 tail for GG-NER recognition

Journal Article · Thu Mar 08 00:00:00 EST 2018 · DNA Repair

DOI:https://doi.org/10.1016/j.dnarep.2018.02.009· OSTI ID:1543539

Cai, Yuqin ^[1]; Fu, Iwen ^[1]; Geacintov, Nicholas E. ^[1]; Zhang, Yingkai ^[2]; Broyde, Suse ^[1]

New York Univ. (NYU), NY (United States)
New York Univ. (NYU), NY (United States); NYU-ECNU Center for Computational Chemistry, Shanghai (China)

How DNA lesions in nucleosomes are recognized for global genome nucleotide excision repair (GG-NER) remains poorly understood, and the roles that histone tails may play remains to be established. Histone H3 and H4 N-terminal tails are of particular interest as their acetylation states are important in regulating nucleosomal functions in transcription, replication and repair. In particular the H3 tail has been the focus of recent attention as a site for the interaction with XPC, the GG-NER lesion recognition factor. Here we have investigated how the structure and dynamics of the DNA lesion cis-B[a]P-dG, derived from the environmental carcinogen benzo[a]pyrene (B[a]P), is impacted by the presence of flanking H3 and H4 tails. This lesion is well-repaired by GG-NER, and adopts a base-displaced/intercalated conformation in which the lesion partner C is displaced into the major groove. We used molecular dynamics simulations to obtain structural and dynamic characterizations for this lesion positioned in nucleosomal DNA so that it is bracketed by the H3 and H4 tails. The H4 tail was studied in unacetylated and acetylated states, while the H3 tail was unacetylated, its state when it binds XPC (Kakumu, Nakanishi et al., 2017). Our results reveal that upon acetylation, the H4 tail is released from the DNA surface; the H3 tail then forms a pocket that induces flipping and capture of the displaced lesion partner base C. This reveals synergistic effects of the behavior of the two tails. We hypothesize that the dual capability of the H3 tail to sense the displaced lesion partner base and to bind XPC could foster recognition of this lesion by XPC for initiation of GG-NER in nucleosomes.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1543539

Journal Information:: DNA Repair, Vol. 65, Issue C; ISSN 1568-7864

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 9 works

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References (62)

New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Luger, Karolin; Dechassa, Mekonnen L.; Tremethick, David J. Nature Reviews Molecular Cell Biology, Vol. 13, Issue 7 https://doi.org/10.1038/nrm3382	journal	June 2012
Nucleosome Structure and Function McGinty, Robert K.; Tan, Song Chemical Reviews, Vol. 115, Issue 6 https://doi.org/10.1021/cr500373h	journal	October 2014
Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure Pepenella, Sharon; Murphy, Kevin J.; Hayes, Jeffrey J. Chromosoma, Vol. 123, Issue 1-2 https://doi.org/10.1007/s00412-013-0435-8	journal	August 2013
Post-Translational Modifications of Histones That Influence Nucleosome Dynamics Bowman, Gregory D.; Poirier, Michael G. Chemical Reviews, Vol. 115, Issue 6 https://doi.org/10.1021/cr500350x	journal	October 2014
Translating the Histone Code Jenuwein, T. Science, Vol. 293, Issue 5532 https://doi.org/10.1126/science.1063127	journal	August 2001
Emerging roles for histone modifications in DNA excision repair Mao, Peng; Wyrick, John J. FEMS Yeast Research, Vol. 16, Issue 7 https://doi.org/10.1093/femsyr/fow090	journal	October 2016
Genome-wide Map of Nucleosome Acetylation and Methylation in Yeast Pokholok, Dmitry K.; Harbison, Christopher T.; Levine, Stuart Cell, Vol. 122, Issue 4 https://doi.org/10.1016/j.cell.2005.06.026	journal	August 2005
The language of covalent histone modifications Strahl, Brian D.; Allis, C. David Nature, Vol. 403, Issue 6765 https://doi.org/10.1038/47412	journal	January 2000
The growing landscape of lysine acetylation links metabolism and cell signalling Choudhary, Chunaram; Weinert, Brian T.; Nishida, Yuya Nature Reviews Molecular Cell Biology, Vol. 15, Issue 8 https://doi.org/10.1038/nrm3841	journal	July 2014
Role of Histone Acetylation in Cell Cycle Regulation Koprinarova, Miglena; Schnekenburger, Michael; Diederich, Marc Current Topics in Medicinal Chemistry, Vol. 16, Issue 7 https://doi.org/10.2174/1568026615666150825140822	journal	November 2015
50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond Verdin, Eric; Ott, Melanie Nature Reviews Molecular Cell Biology, Vol. 16, Issue 4 https://doi.org/10.1038/nrm3931	journal	December 2014
Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. Smerdon, M. J.; Lan, S. Y.; Calza, R. E. Journal of Biological Chemistry, Vol. 257, Issue 22 https://doi.org/10.1016/S0021-9258(18)33468-9	journal	November 1982
Changes in nuclear protein acetylation in u.v.-damaged human cells Ramanathan, Brinda; Smerdon, Michael J. Carcinogenesis, Vol. 7, Issue 7 https://doi.org/10.1093/carcin/7.7.1087	journal	January 1986
Enhanced DNA Repair Synthesis in Hyperacetylated Nucleosomes Ramanathan, B.; Smerdon, M. J. Journal of Biological Chemistry, Vol. 264, Issue 19 https://doi.org/10.1016/S0021-9258(18)60422-3	journal	July 1989
Implication of Posttranslational Histone Modifications in Nucleotide Excision Repair Li, Shisheng International Journal of Molecular Sciences, Vol. 13, Issue 12 https://doi.org/10.3390/ijms131012461	journal	September 2012
Chromatin dynamics after DNA damage: The legacy of the access–repair–restore model Polo, Sophie E.; Almouzni, Geneviève DNA Repair, Vol. 36 https://doi.org/10.1016/j.dnarep.2015.09.014	journal	December 2015
DNA repair and the role of chromatin structure Smerdon, Michael J. Current Opinion in Cell Biology, Vol. 3, Issue 3 https://doi.org/10.1016/0955-0674(91)90069-B	journal	June 1991
Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. Smerdon, M. J.; Lieberman, M. W. Proceedings of the National Academy of Sciences, Vol. 75, Issue 9 https://doi.org/10.1073/pnas.75.9.4238	journal	September 1978
Acetylation Mimics Within a Single Nucleosome Alter Local DNA Accessibility In Compacted Nucleosome Arrays Mishra, Laxmi N.; Pepenella, Sharon; Rogge, Ryan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34808	journal	October 2016
Histone H4-K16 Acetylation Controls Chromatin Structure and Protein Interactions Shogren-Knaak, M. Science, Vol. 311, Issue 5762 https://doi.org/10.1126/science.1124000	journal	February 2006
30 nm Chromatin Fibre Decompaction Requires both H4-K16 Acetylation and Linker Histone Eviction Robinson, Philip J. J.; An, Woojin; Routh, Andrew Journal of Molecular Biology, Vol. 381, Issue 4 https://doi.org/10.1016/j.jmb.2008.04.050	journal	September 2008
Regulation of Nucleosome Stacking and Chromatin Compaction by the Histone H4 N-Terminal Tail–H2A Acidic Patch Interaction Chen, Qinming; Yang, Renliang; Korolev, Nikolay Journal of Molecular Biology, Vol. 429, Issue 13 https://doi.org/10.1016/j.jmb.2017.03.016	journal	June 2017
Shaping chromatin for repair Gospodinov, Anastas; Herceg, Zdenko Mutation Research/Reviews in Mutation Research, Vol. 752, Issue 1 https://doi.org/10.1016/j.mrrev.2012.10.001	journal	January 2013
The amino-terminal tails of histones H2A and H3 coordinate efficient base excision repair, DNA damage signaling and postreplication repair in Saccharomyces cerevisiae Meas, Rithy; Smerdon, Michael J.; Wyrick, John J. Nucleic Acids Research, Vol. 43, Issue 10 https://doi.org/10.1093/nar/gkv372	journal	April 2015
Histones H3 and H4 require their relevant amino-tails for efficient nuclear import and replication-coupled chromatin assembly in vivo Ejlassi, Aïda; Menil-Philippot, Vanessa; Galvani, Angélique Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03218-6	journal	June 2017
Opposing roles of H3- and H4-acetylation in the regulation of nucleosome structure—a FRET study Gansen, Alexander; Tóth, Katalin; Schwarz, Nathalie Nucleic Acids Research, Vol. 43, Issue 3 https://doi.org/10.1093/nar/gku1354	journal	January 2015
Xeroderma pigmentosum group C protein interacts with histones: regulation by acetylated states of histone H3 Kakumu, Erina; Nakanishi, Seiya; Shiratori, Hiromi M. Genes to Cells, Vol. 22, Issue 3 https://doi.org/10.1111/gtc.12479	journal	February 2017
Nucleotide Excision Repair in Eukaryotes Scharer, O. D. Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 10 https://doi.org/10.1101/cshperspect.a012609	journal	October 2013
Fifty years of benzo(a)pyrene Phillips, David H. Nature, Vol. 303, Issue 5917 https://doi.org/10.1038/303468a0	journal	June 1983
NMR Solution Structures of Stereoisomeric Covalent Polycyclic Aromatic Carcinogen−DNA Adducts: Principles, Patterns, and Diversity Geacintov, Nicholas E.; Cosman, Monique; Hingerty, Brian E. Chemical Research in Toxicology, Vol. 10, Issue 2 https://doi.org/10.1021/tx9601418	journal	February 1997
DNA Adduct Formation by Polycyclic Aromatic Hydrocarbon Dihydrodiol Epoxides Szeliga, Jan; Dipple, Anthony Chemical Research in Toxicology, Vol. 11, Issue 1 https://doi.org/10.1021/tx970142f	journal	January 1998
Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes Hess, M. T.; Gunz, D.; Luneva, N. Molecular and Cellular Biology, Vol. 17, Issue 12 https://doi.org/10.1128/MCB.17.12.7069	journal	December 1997
Resistance of bulky DNA lesions to nucleotide excision repair can result from extensive aromatic lesion–base stacking interactions Reeves, Dara A.; Mu, Hong; Kropachev, Konstantin Nucleic Acids Research, Vol. 39, Issue 20 https://doi.org/10.1093/nar/gkr537	journal	July 2011
The human DNA repair factor XPC-HR23B distinguishes stereoisomeric benzo[a]pyrenyl-DNA lesions Mocquet, Vincent; Kropachev, Konstantin; Kolbanovskiy, Marina The EMBO Journal, Vol. 26, Issue 12 https://doi.org/10.1038/sj.emboj.7601730	journal	May 2007
Solution conformation of the (+)-cis-anti-[BP]dG adduct in a DNA duplex: Intercalation of the covalently attached benzo[a]pyrenyl ring into the helix and displacement of the modified deoxyguanosine Cosman, Monique; de los Santos, Carlos; Fiala, Radovan Biochemistry, Vol. 32, Issue 16 https://doi.org/10.1021/bi00067a001	journal	April 1993
Nucleotide Excision Repair Lesion-Recognition Protein Rad4 Captures a Pre-Flipped Partner Base in a Benzo[ a ]pyrene-Derived DNA Lesion: How Structure Impacts the Binding Pathway Mu, Hong; Geacintov, Nicholas E.; Min, Jung-Hyun Chemical Research in Toxicology, Vol. 30, Issue 6 https://doi.org/10.1021/acs.chemrestox.7b00074	journal	May 2017
Recognition of DNA damage by the Rad4 nucleotide excision repair protein Min, Jung-Hyun; Pavletich, Nikola P. Nature, Vol. 449, Issue 7162 https://doi.org/10.1038/nature06155	journal	September 2007
DNA Stretching and Extreme Kinking in the Nucleosome Core Ong, Michelle S.; Richmond, Timothy J.; Davey, Curt A. Journal of Molecular Biology, Vol. 368, Issue 4 https://doi.org/10.1016/j.jmb.2007.02.062	journal	May 2007
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Differences in the Access of Lesions to the Nucleotide Excision Repair Machinery in Nucleosomes Cai, Yuqin; Kropachev, Konstantin; Terzidis, Michael A. Biochemistry, Vol. 54, Issue 27 https://doi.org/10.1021/acs.biochem.5b00564	journal	June 2015
Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Cosman, M.; de los Santos, C.; Fiala, R. Proceedings of the National Academy of Sciences, Vol. 89, Issue 5 https://doi.org/10.1073/pnas.89.5.1914	journal	March 1992
Entrapment of a Histone Tail by a DNA Lesion in a Nucleosome Suggests the Lesion Impacts Epigenetic Marking: A Molecular Dynamics Study Fu, Iwen; Cai, Yuqin; Zhang, Yingkai Biochemistry, Vol. 55, Issue 2 https://doi.org/10.1021/acs.biochem.5b01166	journal	January 2016
Nucleosome Histone Tail Conformation and Dynamics: Impacts of Lysine Acetylation and a Nearby Minor Groove Benzo[ a ]pyrene-Derived Lesion Fu, Iwen; Cai, Yuqin; Geacintov, Nicholas E. Biochemistry, Vol. 56, Issue 14 https://doi.org/10.1021/acs.biochem.6b01208	journal	March 2017
Histone H4 acetylation in human cells Frequency of acetylation at different sites defined by immunolabeling with site-specific antibodies Turner, Bryan M.; O'Neill, Laura P.; Allan, Irene M. FEBS Letters, Vol. 253, Issue 1-2 https://doi.org/10.1016/0014-5793(89)80947-0	journal	August 1989
Patterns of histone acetylation Thorne, Alan W.; Kmiciek, Daniel; Mitchelson, Keith European Journal of Biochemistry, Vol. 193, Issue 3 https://doi.org/10.1111/j.1432-1033.1990.tb19390.x	journal	November 1990
Histone H4 acetylation in Drosophila Frequency of acetylation at different sites defined by immunolabelling with site-specific antibodies Munks, Rebecca J. L.; Moore, Jayne; O'Neill, Laura P. FEBS Letters, Vol. 284, Issue 2 https://doi.org/10.1016/0014-5793(91)80695-Y	journal	June 1991
Selective use of H4 acetylation sites in the yeast Saccharomyces cerevisiae Clarke, D. J.; O'Neill, L. P.; Turner, B. M. Biochemical Journal, Vol. 294, Issue 2 https://doi.org/10.1042/bj2940557	journal	September 1993
Non-random acetylation of histone H4 by a cytoplasmic histone acetyltransferase as determined by novel methodology Sobel, R. E.; Cook, R. G.; Allis, C. D. Journal of Biological Chemistry, Vol. 269, Issue 28 https://doi.org/10.1016/S0021-9258(17)32348-7	journal	July 1994
Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines Kuo, Min-Hao; Brownell, James E.; Sobel, Richard E. Nature, Vol. 383, Issue 6597 https://doi.org/10.1038/383269a0	journal	September 1996
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00255	journal	July 2015
PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data Roe, Daniel R.; Cheatham, Thomas E. Journal of Chemical Theory and Computation, Vol. 9, Issue 7 https://doi.org/10.1021/ct400341p	journal	June 2013
Clustering Molecular Dynamics Trajectories: 1. Characterizing the Performance of Different Clustering Algorithms Shao, Jianyin; Tanner, Stephen W.; Thompson, Nephi Journal of Chemical Theory and Computation, Vol. 3, Issue 6 https://doi.org/10.1021/ct700119m	journal	October 2007
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Aromatic–Proline Interactions: Electronically Tunable CH/π Interactions Zondlo, Neal J. Accounts of Chemical Research, Vol. 46, Issue 4 https://doi.org/10.1021/ar300087y	journal	June 2012
ASH1L histone methyltransferase regulates the handoff between damage recognition factors in global-genome nucleotide excision repair Balbo Pogliano, Chiara; Gatti, Marco; Rüthemann, Peter Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01080-8	journal	November 2017
DNA Quality Control by Conformational Readout on the Undamaged Strand of the Double Helix Buterin, Tonko; Meyer, Christoph; Giese, Bernd Chemistry & Biology, Vol. 12, Issue 8 https://doi.org/10.1016/j.chembiol.2005.06.011	journal	August 2005
Base-Displaced Intercalated Structure of the Food Mutagen 2-Amino-3-methylimidazo[4,5- f ]quinoline in the Recognition Sequence of the Nar I Restriction Enzyme, a Hotspot for −2 bp Deletions Wang, Feng; DeMuro, Nicholas E.; Elmquist, C. Eric Journal of the American Chemical Society, Vol. 128, Issue 31 https://doi.org/10.1021/ja062004v	journal	August 2006
Repair-Resistant DNA Lesions Geacintov, Nicholas E.; Broyde, Suse Chemical Research in Toxicology, Vol. 30, Issue 8 https://doi.org/10.1021/acs.chemrestox.7b00128	journal	July 2017
Single-Molecule Imaging Reveals that Rad4 Employs a Dynamic DNA Damage Recognition Process Kong, Muwen; Liu, Lili; Chen, Xuejing Molecular Cell, Vol. 64, Issue 2 https://doi.org/10.1016/j.molcel.2016.09.005	journal	October 2016
Real-Time Tracking of Parental Histones Reveals Their Contribution to Chromatin Integrity Following DNA Damage Adam, Salomé; Dabin, Juliette; Chevallier, Odile Molecular Cell, Vol. 64, Issue 1 https://doi.org/10.1016/j.molcel.2016.08.019	journal	October 2016
Roll: a new algorithm for the detection of protein pockets and cavities with a rolling probe sphere Yu, Jian; Zhou, Yong; Tanaka, Isao Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp599	journal	October 2009
CASTp: Computed Atlas of Surface Topography of proteins Binkowski, T. A. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg512	journal	July 2003

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Title: Synergistic effects of H3 and H4 nucleosome tails on structure and dynamics of a lesion-containing DNA: Binding of a displaced lesion partner base to the H3 tail for GG-NER recognition

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