Enhanced spontaneous DNA twisting/bending fluctuations unveiled by fluorescence lifetime distributions promote mismatch recognition by the Rad4 nucleotide excision repair complex

Chakraborty, Sagnik; Steinbach, Peter J.; Paul, Debamita; Mu, Hong; Broyde, Suse; Min, Jung-Hyun; Ansari, Anjum

doi:10.1093/nar/gkx1216

Title: Enhanced spontaneous DNA twisting/bending fluctuations unveiled by fluorescence lifetime distributions promote mismatch recognition by the Rad4 nucleotide excision repair complex

Journal Article · Mon Dec 18 00:00:00 EST 2017 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkx1216· OSTI ID:1543988

Chakraborty, Sagnik ^[1]; Steinbach, Peter J. ^[2]; Paul, Debamita ^[1]; Mu, Hong ^[3]; Broyde, Suse ^[3]; Min, Jung-Hyun ^[1]; Ansari, Anjum ^[1]

Univ. of Illinois, Chicago, IL (United States)
National Inst. of Health (NIH), Bethesda, MD (United States)
New York Univ. (NYU), NY (United States)

Rad4/XPC recognizes diverse DNA lesions including ultraviolet-photolesions and carcinogen-DNA adducts, initiating nucleotide excision repair. Studies have suggested that Rad4/XPC senses lesion-induced helix-destabilization to flip out nucleotides from damaged DNA sites. However, characterizing how DNA deformability and/or distortions impact recognition has been challenging. Here, using fluorescence lifetime measurements empowered by a maximum entropy algorithm, we mapped the conformational heterogeneities of artificially destabilized mismatched DNA substrates of varying Rad4-binding specificities. The conformational distributions, as probed by FRET between a cytosine-analog pair exquisitely sensitive to DNA twisting/bending, reveal a direct connection between intrinsic DNA deformability and Rad4 recognition. High-specificity CCC/CCC mismatch, free in solution, sampled a strikingly broad range of conformations from B-DNA-like to highly distorted conformations that resembled those observed with Rad4 bound; the extent of these distortions increased with bound Rad4 and with temperature. Conversely, the non-specific TAT/TAT mismatch had a homogeneous, B-DNA-like conformation. Molecular dynamics simulations also revealed a wide distribution of conformations for CCC/CCC, complementing experimental findings. We propose that intrinsic deformability promotes Rad4 damage recognition, perhaps by stalling a diffusing protein and/or facilitating ‘conformational capture’ of pre-distorted damaged sites. Surprisingly, even mismatched DNA specifically bound to Rad4 remains highly dynamic, a feature that may reflect the versatility of Rad4/XPC to recognize many structurally dissimilar lesions

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

Sponsoring Organization:: USDOE; National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: MCB060037

OSTI ID:: 1543988

Journal Information:: Nucleic Acids Research, Vol. 46, Issue 3; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (112)

Solution Structure of a Trans-Opened (10 S )-dA Adduct of (+)-(7 S ,8 R ,9 S ,10 R )-7,8-Dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[ a ]pyrene in a Fully Complementary DNA Duplex: Evidence for a Major Syn Conformation Pradhan, Padmanava; Tirumala, Sampath; Liu, Xiaohong Biochemistry, Vol. 40, Issue 20 https://doi.org/10.1021/bi002896q	journal	May 2001
Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Schuler, Benjamin; Lipman, Everett A.; Eaton, William A. Nature, Vol. 419, Issue 6908 https://doi.org/10.1038/nature01060	journal	October 2002
Studying Z-DNA and B- to Z-DNA transitions using a cytosine analogue FRET-pair Dumat, Blaise; Larsen, Anders Foller; Wilhelmsson, L. Marcus Nucleic Acids Research, Vol. 44, Issue 11 https://doi.org/10.1093/nar/gkw114	journal	February 2016
Nucleotide excision repair of 2-acetylaminofluorene- and 2-aminofluorene-(C8)-guanine adducts: molecular dynamics simulations elucidate how lesion structure and base sequence context impact repair efficiencies Mu, Hong; Kropachev, Konstantin; Wang, Lihua Nucleic Acids Research, Vol. 40, Issue 19 https://doi.org/10.1093/nar/gks788	journal	August 2012
Integrating protein structural dynamics and evolutionary analysis with Bio3D Skjærven, Lars; Yao, Xin-Qiu; Scarabelli, Guido BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/s12859-014-0399-6	journal	December 2014
Sliding and jumping of single EcoRV restriction enzymes on non-cognate DNA Bonnet, Isabelle; Biebricher, Andreas; Porté, Pierre-Louis Nucleic Acids Research, Vol. 36, Issue 12 https://doi.org/10.1093/nar/gkn376	journal	June 2008
Distant Neighbor Base Sequence Context Effects in Human Nucleotide Excision Repair of a Benzo[a]pyrene-derived DNA Lesion Cai, Yuqin; Kropachev, Konstantin; Xu, Rong Journal of Molecular Biology, Vol. 399, Issue 3 https://doi.org/10.1016/j.jmb.2010.04.004	journal	June 2010
Structure and Dynamics of DNA and RNA Double Helices Obtained from the GGGGCC and CCCCGG Hexanucleotide Repeats That Are the Hallmark of C9FTD/ALS Diseases Zhang, Yuan; Roland, Christopher; Sagui, Celeste ACS Chemical Neuroscience, Vol. 8, Issue 3 https://doi.org/10.1021/acschemneuro.6b00348	journal	December 2016
Sequence Context- and Temperature-Dependent Nucleotide Excision Repair of a Benzo[ a ]pyrene Diol Epoxide-Guanine DNA Adduct Catalyzed by Thermophilic U vr ABC Proteins ^† Ruan, Qian; Liu, Tongming; Kolbanovskiy, Alexander Biochemistry, Vol. 46, Issue 23 https://doi.org/10.1021/bi700294k	journal	June 2007
Pre-Steady-State Binding of Damaged DNA by XPC−hHR23B Reveals a Kinetic Mechanism for Damage Discrimination ^† Trego, Kelly S.; Turchi, John J. Biochemistry, Vol. 45, Issue 6 https://doi.org/10.1021/bi051936t	journal	February 2006
Characterization and use of an unprecedentedly bright and structurally non-perturbing fluorescent DNA base analogue Sandin, Peter; Börjesson, Karl; Li, Hong Nucleic Acids Research, Vol. 36, Issue 1 https://doi.org/10.1093/nar/gkm1006	journal	November 2007
Thermodynamic and base-pairing studies of matched and mismatched DNA dodecamer duplexes containing cis-syn, (6-4) and Dewar photoproducts of TT Jing, Y.; Taylor, J. -S.; Kao, J. F. - L. Nucleic Acids Research, Vol. 26, Issue 16 https://doi.org/10.1093/nar/26.16.3845	journal	August 1998
Overproduction, Purification, and Characterization of the XPC Subunit of the Human DNA Repair Excision Nuclease Reardon, Joyce T.; Mu, David; Sancar, Aziz Journal of Biological Chemistry, Vol. 271, Issue 32 https://doi.org/10.1074/jbc.271.32.19451	journal	August 1996
A multistep damage recognition mechanism for global genomic nucleotide excision repair Sugasawa, K. Genes & Development, Vol. 15, Issue 5 https://doi.org/10.1101/gad.866301	journal	March 2001
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
Rapid search for specific sites on DNA through conformational switch of nonspecifically bound proteins Zhou, H. -X. Proceedings of the National Academy of Sciences, Vol. 108, Issue 21 https://doi.org/10.1073/pnas.1101555108	journal	May 2011
The role of dynamic conformational ensembles in biomolecular recognition Boehr, David D.; Nussinov, Ruth; Wright, Peter E. Nature Chemical Biology, Vol. 5, Issue 11 https://doi.org/10.1038/nchembio.232	journal	October 2009
Twist-open mechanism of DNA damage recognition by the Rad4/XPC nucleotide excision repair complex Velmurugu, Yogambigai; Chen, Xuejing; Slogoff Sevilla, Phillip Proceedings of the National Academy of Sciences, Vol. 113, Issue 16 https://doi.org/10.1073/pnas.1514666113	journal	March 2016
Time-resolved fluorescence studies of nucleotide flipping by restriction enzymes Neely, Robert K.; Tamulaitis, Gintautas; Chen, Kai Nucleic Acids Research, Vol. 37, Issue 20 https://doi.org/10.1093/nar/gkp688	journal	September 2009
Structural, energetic and dynamic properties of guanine(C8)–thymine(N3) cross-links in DNA provide insights on susceptibility to nucleotide excision repair Ding, Shuang; Kropachev, Konstantin; Cai, Yuqin Nucleic Acids Research, Vol. 40, Issue 6 https://doi.org/10.1093/nar/gkr1087	journal	November 2011
Detection of Damaged DNA Bases by DNA Glycosylase Enzymes Friedman, Joshua I.; Stivers, James T. Biochemistry, Vol. 49, Issue 24 https://doi.org/10.1021/bi100593a	journal	June 2010
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
Dynamic Basis for One-Dimensional DNA Scanning by the Mismatch Repair Complex Msh2-Msh6 Gorman, Jason; Chowdhury, Arindam; Surtees, Jennifer A. Molecular Cell, Vol. 28, Issue 3 https://doi.org/10.1016/j.molcel.2007.09.008	journal	November 2007
Nucleic Acid Base Analog FRET-Pair Facilitating Detailed Structural Measurements in Nucleic Acid Containing Systems Börjesson, Karl; Preus, Søren; El-Sagheer, Afaf H. Journal of the American Chemical Society, Vol. 131, Issue 12 https://doi.org/10.1021/ja806944w	journal	April 2009
Oral Cell DNA Adducts as Potential Biomarkers for Lung Cancer Susceptibility in Cigarette Smokers Hecht, Stephen S. Chemical Research in Toxicology, Vol. 30, Issue 1 https://doi.org/10.1021/acs.chemrestox.6b00372	journal	December 2016
Nontarget DNA binding shapes the dynamic landscape for enzymatic recognition of DNA damage Friedman, Joshua I.; Majumdar, Ananya; Stivers, James T. Nucleic Acids Research, Vol. 37, Issue 11 https://doi.org/10.1093/nar/gkp161	journal	April 2009
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
Enzymatic capture of an extrahelical thymine in the search for uracil in DNA Parker, Jared B.; Bianchet, Mario A.; Krosky, Daniel J. Nature, Vol. 449, Issue 7161 https://doi.org/10.1038/nature06131	journal	August 2007
Two glycosylase families diffusively scan DNA using a wedge residue to probe for and identify oxidatively damaged bases Nelson, S. R.; Dunn, A. R.; Kathe, S. D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1400386111	journal	May 2014
Mammalian transcription factor A is a core component of the mitochondrial transcription machinery Shi, Y.; Dierckx, A.; Wanrooij, P. H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 41 https://doi.org/10.1073/pnas.1119738109	journal	September 2012
Structure and Flexibility Adaptation in Nonspecific and Specific Protein-DNA Complexes Kalodimos, C. G. Science, Vol. 305, Issue 5682 https://doi.org/10.1126/science.1097064	journal	July 2004
Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites 1 1Edited by M. Yaniv Batty, Dawn; Rapic’-Otrin, Vesna; Levine, Arthur S. Journal of Molecular Biology, Vol. 300, Issue 2 https://doi.org/10.1006/jmbi.2000.3857	journal	July 2000
Molecular Mechanisms of Mammalian Global Genome Nucleotide Excision Repair Gillet, Ludovic C. J.; Schärer, Orlando D. Chemical Reviews, Vol. 106, Issue 2 https://doi.org/10.1021/cr040483f	journal	February 2006
New Insights into the Transition Pathway from Nonspecific to Specific Complex of DNA with Escherichia Coli Integration Host Factor ^† Vivas, Paula; Kuznetsov, Serguei V.; Ansari, Anjum The Journal of Physical Chemistry B, Vol. 112, Issue 19 https://doi.org/10.1021/jp076042s	journal	May 2008
Conformational Analysis of DNA Repair Intermediates by Time-Resolved Fluorescence Spectroscopy Lin, Su; Horning, David P.; Szostak, Jack W. The Journal of Physical Chemistry A, Vol. 113, Issue 35 https://doi.org/10.1021/jp906746w	journal	September 2009
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
Stability of DNA Duplexes Containing GG, CC, AA, and TT Mismatches Tikhomirova, Anna; Beletskaya, Irina V.; Chalikian, Tigran V. Biochemistry, Vol. 45, Issue 35 https://doi.org/10.1021/bi060304j	journal	September 2006
Single-Molecule FRET TACKLE Reveals Highly Dynamic Mismatched DNA−MutS Complexes Sass, Lauryn E.; Lanyi, Cherie; Weninger, Keith Biochemistry, Vol. 49, Issue 14 https://doi.org/10.1021/bi901871u	journal	April 2010
Synthesis and Characterization of Site-Specific and Stereoisomeric Fjord Dibenzo[ a,l ]pyrene Diol Epoxide− N ⁶ -Adenine Adducts: Unusual Thermal Stabilization of Modified DNA Duplexes Ruan, Qian; Kolbanovskiy, Alexander; Zhuang, Ping Chemical Research in Toxicology, Vol. 15, Issue 2 https://doi.org/10.1021/tx010157k	journal	February 2002
DNA damage recognition during nucleotide excision repair in mammalian cells Wood, Richard D. Biochimie, Vol. 81, Issue 1-2 https://doi.org/10.1016/S0300-9084(99)80036-4	journal	January 1999
Inferring Lifetime Distributions from Kinetics by Maximizing Entropy Using a Bootstrapped Model Steinbach, Peter J. Journal of Chemical Information and Computer Sciences, Vol. 42, Issue 6 https://doi.org/10.1021/ci025551i	journal	November 2002
How do site-specific DNA-binding proteins find their targets? Halford, S. E. Nucleic Acids Research, Vol. 32, Issue 10 https://doi.org/10.1093/nar/gkh624	journal	June 2004
1H NMR determination of base‐pair lifetimes in oligonucleotides containing single base mismatches Bhattacharya, Pratip K.; Cha, Julie; Barton, Jacqueline K. Nucleic Acids Research, Vol. 30, Issue 21 https://doi.org/10.1093/nar/gkf601	journal	November 2002
Mapping the Transition State for DNA Bending by IHF Vivas, Paula; Velmurugu, Yogambigai; Kuznetsov, Serguei V. Journal of Molecular Biology, Vol. 418, Issue 5 https://doi.org/10.1016/j.jmb.2012.02.028	journal	May 2012
Mutations induced by benzo[a]pyrene and dibenzo[a,l]pyrene in lacI transgenic B6C3F1 mouse lung result from stable DNA adducts Leavitt, S. A.; George, M. H.; Moore, T. Mutagenesis, Vol. 23, Issue 6 https://doi.org/10.1093/mutage/gen033	journal	August 2008
Stepwise binding and bending of DNA by Escherichia coli integration host factor Sugimura, S.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 49 https://doi.org/10.1073/pnas.0608337103	journal	November 2006
FRETmatrix: a general methodology for the simulation and analysis of FRET in nucleic acids Preus, Søren; Kilså, Kristine; Miannay, Francois-Alexandre Nucleic Acids Research, Vol. 41, Issue 1 https://doi.org/10.1093/nar/gks856	journal	September 2012
Single-molecule fluorescence spectroscopy maps the folding landscape of a large protein Pirchi, Menahem; Ziv, Guy; Riven, Inbal Nature Communications, Vol. 2, Issue 1 https://doi.org/10.1038/ncomms1504	journal	September 2011
The comings and goings of nucleotide excision repair factors on damaged DNA Riedl, T. The EMBO Journal, Vol. 22, Issue 19 https://doi.org/10.1093/emboj/cdg489	journal	October 2003
The XPC−HR23B Complex Displays High Affinity and Specificity for Damaged DNA in a True-Equilibrium Fluorescence Assay ^† Hey, Thomas; Lipps, Georg; Sugasawa, Kaoru Biochemistry, Vol. 41, Issue 21 https://doi.org/10.1021/bi012202t	journal	May 2002
Slow Conformational Changes in MutS and DNA Direct Ordered Transitions between Mismatch Search, Recognition and Signaling of DNA Repair Sharma, Anushi; Doucette, Christopher; Biro, F. Noah Journal of Molecular Biology, Vol. 425, Issue 22 https://doi.org/10.1016/j.jmb.2013.08.011	journal	November 2013
NMR structural studies of a 15-mer DNA duplex from a ras protooncogene modified with the carcinogen 2-aminofluorene: conformational heterogeneity Cho, Bongsup P.; Beland, Frederick A.; Marques, M. Matilde Biochemistry, Vol. 33, Issue 6 https://doi.org/10.1021/bi00172a013	journal	February 1994
An unprecedented nucleic acid capture mechanism for excision of DNA damage Rubinson, Emily H.; Gowda, A. S. Prakasha; Spratt, Thomas E. Nature, Vol. 468, Issue 7322 https://doi.org/10.1038/nature09428	journal	October 2010
DNA-tension dependence of restriction enzyme activity reveals mechanochemical properties of the reaction pathway van den Broek, B. Nucleic Acids Research, Vol. 33, Issue 8 https://doi.org/10.1093/nar/gki565	journal	April 2005
Characterization of Nucleobase Analogue FRET Acceptor tC _nitro Preus, Søren; Börjesson, Karl; Kilså, Kristine The Journal of Physical Chemistry B, Vol. 114, Issue 2 https://doi.org/10.1021/jp909471b	journal	January 2010
Differential Nucleotide Excision Repair Susceptibility of Bulky DNA Adducts in Different Sequence Contexts: Hierarchies of Recognition Signals Cai, Yuqin; Patel, Dinshaw J.; Geacintov, Nicholas E. Journal of Molecular Biology, Vol. 385, Issue 1 https://doi.org/10.1016/j.jmb.2008.09.087	journal	January 2009
Structural Differences in the NOE-derived Structure of G–T Mismatched DNA Relative to Normal DNA are Correlated with Differences in 13C Relaxation-based Internal Dynamics Isaacs, Richard J.; Rayens, William S.; Spielmann, H. Peter Journal of Molecular Biology, Vol. 319, Issue 1 https://doi.org/10.1016/S0022-2836(02)00265-6	journal	May 2002
Solution Structure of the Minor Conformer of a DNA Duplex Containing a dG Mismatch Opposite a Benzo[ a ]pyrene Diol Epoxide/dA Adduct: Glycosidic Rotation from Syn to Anti at the Modified Deoxyadenosine ^† Schwartz, J. L.; Rice, J. S.; Luxon, B. A. Biochemistry, Vol. 36, Issue 37 https://doi.org/10.1021/bi971306u	journal	September 1997
The Catalytic Power of Uracil DNA Glycosylase in the Opening of Thymine Base Pairs Cao, Chunyang; Jiang, Yu Lin; Krosky, Daniel J. Journal of the American Chemical Society, Vol. 128, Issue 40 https://doi.org/10.1021/ja062978n	journal	October 2006
Time-resolved fluorescence resonance energy transfer: A versatile tool for the analysis of nucleic acids Klostermeier, Dagmar; Millar, David P. Biopolymers, Vol. 61, Issue 3 https://doi.org/10.1002/bip.10146	journal	January 2002
Alteration in the cavity size adjacent to the active site of RB69 DNA polymerase changes its conformational dynamics Xia, Shuangluo; Wood, Marcus; Bradley, Michael J. Nucleic Acids Research, Vol. 41, Issue 19 https://doi.org/10.1093/nar/gkt674	journal	August 2013
Kinetic Mechanism of Damage Site Recognition and Uracil Flipping by Escherichia coli Uracil DNA Glycosylase ^† Stivers, James T.; Pankiewicz, Krzysztof W.; Watanabe, Kyoichi A. Biochemistry, Vol. 38, Issue 3 https://doi.org/10.1021/bi9818669	journal	January 1999
The amino terminal extension of mammalian mitochondrial RNA polymerase ensures promoter specific transcription initiation Posse, Viktor; Hoberg, Emily; Dierckx, Anke Nucleic Acids Research, Vol. 42, Issue 6 https://doi.org/10.1093/nar/gkt1397	journal	January 2014
How nucleotide excision repair protects against cancer Friedberg, Errol C. Nature Reviews Cancer, Vol. 1, Issue 1 https://doi.org/10.1038/35094000	journal	October 2001
Mammary carcinogenicity in female CD rats of fjord region diol epoxides of benzo[c]phenanthrene, benzo[g]chrysene and dibenzo[ a,l ]pyrene Amin, Shantu; Krzeminski, Jacek; Rivenson, Abraham Carcinogenesis, Vol. 16, Issue 8 https://doi.org/10.1093/carcin/16.8.1971	journal	January 1995
NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA Iwahara, J.; Zweckstetter, M.; Clore, G. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 41 https://doi.org/10.1073/pnas.0605868103	journal	September 2006
Kinetics and energetics of base-pair opening in 5'-d(CGCGAATTCGCG)-3' and a substituted dodecamer containing G.cntdot.T mismatches Moe, James G.; Russu, Irina M. Biochemistry, Vol. 31, Issue 36 https://doi.org/10.1021/bi00151a005	journal	September 1992
Mutational signature of aristolochic acid: Clue to the recognition of a global disease Rosenquist, Thomas A.; Grollman, Arthur P. DNA Repair, Vol. 44 https://doi.org/10.1016/j.dnarep.2016.05.027	journal	August 2016
A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA Blainey, P. C.; van Oijen, A. M.; Banerjee, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15 https://doi.org/10.1073/pnas.0509723103	journal	April 2006
Cancer Risk Assessment, Indicators, and Guidelines for Polycyclic Aromatic Hydrocarbons in the Ambient Air Boström, Carl-Elis; Gerde, Per; Hanberg, Annika Environmental Health Perspectives, Vol. 110, Issue s3 https://doi.org/10.1289/ehp.02110s3451	journal	February 2002
Xeroderma pigmentosum group C sensor: unprecedented recognition strategy and tight spatiotemporal regulation Puumalainen, Marjo-Riitta; Rüthemann, Peter; Min, Jun-Hyun Cellular and Molecular Life Sciences, Vol. 73, Issue 3 https://doi.org/10.1007/s00018-015-2075-z	journal	October 2015
Filtering artifacts from lifetime distributions when maximizing entropy using a bootstrapped model Steinbach, Peter J. Analytical Biochemistry, Vol. 427, Issue 1 https://doi.org/10.1016/j.ab.2012.04.008	journal	August 2012
Tumor Suppressor p53 Slides on DNA with Low Friction and High Stability Tafvizi, Anahita; Huang, Fang; Leith, Jason S. Biophysical Journal, Vol. 95, Issue 1 https://doi.org/10.1529/biophysj.108.134122	journal	July 2008
Applying 6-Methylisoxanthopterin-Enhanced Fluorescence To Examine Protein–DNA Interactions in the Picomolar Range Moreno, Andrew; Knee, Joseph; Mukerji, Ishita Biochemistry, Vol. 51, Issue 34 https://doi.org/10.1021/bi300466d	journal	August 2012
Timing facilitated site transfer of an enzyme on DNA Schonhoft, Joseph D.; Stivers, James T. Nature Chemical Biology, Vol. 8, Issue 2 https://doi.org/10.1038/nchembio.764	journal	January 2012
The Sequence Dependence of Human Nucleotide Excision Repair Efficiencies of Benzo[a]pyrene-derived DNA Lesions: Insights into the Structural Factors that Favor Dual Incisions Kropachev, Konstantin; Kolbanovskii, Marina; Cai, Yuqin Journal of Molecular Biology, Vol. 386, Issue 5 https://doi.org/10.1016/j.jmb.2008.12.082	journal	March 2009
Lack of recognition by global-genome nucleotide excision repair accounts for the high mutagenicity and persistence of aristolactam-DNA adducts Sidorenko, Victoria S.; Yeo, Jung-Eun; Bonala, Radha R. Nucleic Acids Research, Vol. 40, Issue 6 https://doi.org/10.1093/nar/gkr1095	journal	November 2011
A model for initial DNA lesion recognition by NER and MMR based on local conformational flexibility Isaacs, Richard J.; Spielmann, H. Peter DNA Repair, Vol. 3, Issue 5 https://doi.org/10.1016/j.dnarep.2004.01.004	journal	May 2004
Nearest-Neighbor Thermodynamics and NMR of DNA Sequences with Internal A·A, C·C, G·G, and T·T Mismatches ^† Peyret, Nicolas; Seneviratne, P. Ananda; Allawi, Hatim T. Biochemistry, Vol. 38, Issue 12 https://doi.org/10.1021/bi9825091	journal	March 1999
The Xeroderma Pigmentosum Group C Protein Complex XPC-HR23B Plays an Important Role in the Recruitment of Transcription Factor IIH to Damaged DNA Yokoi, Masayuki; Masutani, Chikahide; Maekawa, Takafumi Journal of Biological Chemistry, Vol. 275, Issue 13 https://doi.org/10.1074/jbc.275.13.9870	journal	March 2000
Exocyclic amino groups of flanking guanines govern sequence-dependent adduct conformations and local structural distortions for minor groove-aligned benzo[a]pyrenyl-guanine lesions in a GG mutation hotspot context Rodríguez, Fabián A.; Cai, Yuqin; Lin, Chin Nucleic Acids Research, Vol. 35, Issue 5 https://doi.org/10.1093/nar/gkm022	journal	February 2007
Kinetics of Protein-DNA Interaction: Facilitated Target Location in Sequence-Dependent Potential Slutsky, Michael; Mirny, Leonid A. Biophysical Journal, Vol. 87, Issue 6 https://doi.org/10.1529/biophysj.104.050765	journal	December 2004
Kinetic gating mechanism of DNA damage recognition by Rad4/XPC Chen, Xuejing; Velmurugu, Yogambigai; Zheng, Guanqun Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6849	journal	January 2015
Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice Gorman, Jason; Plys, Aaron J.; Visnapuu, Mari-Liis Nature Structural & Molecular Biology, Vol. 17, Issue 8 https://doi.org/10.1038/nsmb.1858	journal	July 2010
Nucleotide Excision Repair Efficiencies of Bulky Carcinogen–DNA Adducts Are Governed by a Balance between Stabilizing and Destabilizing Interactions Cai, Yuqin; Geacintov, Nicholas E.; Broyde, Suse Biochemistry, Vol. 51, Issue 7 https://doi.org/10.1021/bi201794x	journal	February 2012
SSB protein diffusion on single-stranded DNA stimulates RecA filament formation Roy, Rahul; Kozlov, Alexander G.; Lohman, Timothy M. Nature, Vol. 461, Issue 7267 https://doi.org/10.1038/nature08442	journal	October 2009
Adenine–DNA Adducts Derived from the Highly Tumorigenic Dibenzo[ a , l ]pyrene Are Resistant to Nucleotide Excision Repair while Guanine Adducts Are Not Kropachev, Konstantin; Kolbanovskiy, Marina; Liu, Zhi Chemical Research in Toxicology, Vol. 26, Issue 5 https://doi.org/10.1021/tx400080k	journal	April 2013
Altered Dynamics of DNA Bases Adjacent to a Mismatch: A Cue for Mismatch Recognition by MutS Nag, Nabanita; Rao, B. J.; Krishnamoorthy, G. Journal of Molecular Biology, Vol. 374, Issue 1 https://doi.org/10.1016/j.jmb.2007.08.065	journal	November 2007
Microsecond Dynamics of Protein–DNA Interactions: Direct Observation of the Wrapping/Unwrapping Kinetics of Single-stranded DNA around the E.coli SSB Tetramer Kuznetsov, Serguei V.; Kozlov, Alexander G.; Lohman, Timothy M. Journal of Molecular Biology, Vol. 359, Issue 1 https://doi.org/10.1016/j.jmb.2006.02.070	journal	May 2006
Dynamics of a Benzo[a]pyrene-derived Guanine DNA Lesion in TGT and CGC Sequence Contexts: Enhanced Mobility in TGT Explains Conformational Heterogeneity, Flexible Bending, and Greater Susceptibility to Nucleotide Excision Repair Cai, Yuqin; Patel, Dinshaw J.; Geacintov, Nicholas E. Journal of Molecular Biology, Vol. 374, Issue 2 https://doi.org/10.1016/j.jmb.2007.09.034	journal	November 2007
Genetic toxicity of 2-acetylaminofluorene, 2-aminofluorene and some of their metabolites and model metabolites Heflich, Robert H.; Neft, Robin E. Mutation Research/Reviews in Genetic Toxicology, Vol. 318, Issue 2 https://doi.org/10.1016/0165-1110(94)90025-6	journal	October 1994
Base Flipping Free Energy Profiles for Damaged and Undamaged DNA Zheng, Han; Cai, Yuqin; Ding, Shuang Chemical Research in Toxicology, Vol. 23, Issue 12 https://doi.org/10.1021/tx1003613	journal	December 2010
Differential Removal of DNA Adducts Derived from anti -Diol Epoxides of Dibenzo[ a,l ]pyrene and Benzo[ a ]pyrene in Human Cells ^† Dreij, Kristian; Seidel, Albrecht; Jernström, Bengt Chemical Research in Toxicology, Vol. 18, Issue 4 https://doi.org/10.1021/tx0497090	journal	April 2005
Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils Porecha, R. H.; Stivers, J. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 31 https://doi.org/10.1073/pnas.0801612105	journal	July 2008
Ultrafast Fluorescence Dynamics of Tryptophan in the Proteins Monellin and IIA ^Glc Xu, Jianhua; Toptygin, Dmitri; Graver, Karen J. Journal of the American Chemical Society, Vol. 128, Issue 4 https://doi.org/10.1021/ja055746h	journal	February 2006
Biochemical and Structural Domain Analysis of Xeroderma Pigmentosum Complementation Group C Protein ^† Bunick, Christopher G.; Miller, Michael R.; Fuller, Brian E. Biochemistry, Vol. 45, Issue 50 https://doi.org/10.1021/bi061370o	journal	December 2006
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
Recognition of Damaged DNA for Nucleotide Excision Repair: A Correlated Motion Mechanism with a Mismatched cis-syn Thymine Dimer Lesion Mu, Hong; Geacintov, Nicholas E.; Zhang, Yingkai Biochemistry, Vol. 54, Issue 34 https://doi.org/10.1021/acs.biochem.5b00840	journal	August 2015
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
Poor base stacking at DNA lesions may initiate recognition by many repair proteins Yang, Wei DNA Repair, Vol. 5, Issue 6 https://doi.org/10.1016/j.dnarep.2006.02.004	journal	June 2006
Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery Geacintov, Nicholas E.; Broyde, Suse; Buterin, Tonko Biopolymers, Vol. 65, Issue 3 https://doi.org/10.1002/bip.10239	journal	September 2002
Structural Differences in the NOE-derived Structure of G-T Mismatched DNA relative to Normal DNA are Correlated with Differences in (13)C Relaxation-based Internal Dynamics Isaacs, R. J.; Rayens, W. S.; Spielmann, H. P. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr5253	dataset	January 2002
Structural Differences in the NOE-derived Structure of G-T Mismatched DNA relative to Normal DNA are Correlated with Differences in (13)C Relaxation-based Internal Dynamics Isaacs, R. J.; Rayens, W. S.; Spielmann, H. P. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr5252	dataset	January 2002
Relationship between mutagenicity and DNA adduct formation in mammalian cells for fjord- and bay-region diol-epoxides of polycyclic aromatic hydrocarbons Phillips, David H.; Hewer, Alan; Seidel, Albrecht Chemico-Biological Interactions, Vol. 80, Issue 2 https://doi.org/10.1016/0009-2797(91)90023-z	journal	January 1991
Indirect Detection of DNA Damage Maher, L. James Chemistry & Biology, Vol. 12, Issue 8 https://doi.org/10.1016/j.chembiol.2005.08.002	journal	August 2005
Analysis of Kinetics Using a Hybrid Maximum-Entropy/Nonlinear-Least-Squares Method: Application to Protein Folding Steinbach, Peter J.; Ionescu, Roxana; Matthews, C. Robert Biophysical Journal, Vol. 82, Issue 4 https://doi.org/10.1016/s0006-3495(02)75570-7	journal	April 2002
Analyzing the Distribution of Decay Constants in Pulse-Fluorimetry Using the Maximum Entropy Method Livesey, A. K.; Brochon, J. C. Biophysical Journal, Vol. 52, Issue 5 https://doi.org/10.1016/s0006-3495(87)83264-2	journal	November 1987
Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro Kusumoto, Rika; Masutani, Chikahide; Sugasawa, Kaoru Mutation Research/DNA Repair, Vol. 485, Issue 3 https://doi.org/10.1016/s0921-8777(00)00082-3	journal	April 2001
Xeroderma Pigmentosum Group C Protein Complex Is the Initiator of Global Genome Nucleotide Excision Repair Sugasawa, Kaoru; Ng, Jessica M. Y.; Masutani, Chikahide Molecular Cell, Vol. 2, Issue 2 https://doi.org/10.1016/s1097-2765(00)80132-x	journal	August 1998
The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH Uchida, Akio; Sugasawa, Kaoru; Masutani, Chikahide DNA Repair, Vol. 1, Issue 6 https://doi.org/10.1016/s1568-7864(02)00031-9	journal	June 2002
Single Molecule Measurements of Repressor Protein 1D Diffusion on DNA Wang, Y. M.; Austin, Robert H.; Cox, Edward C. Physical Review Letters, Vol. 97, Issue 4 https://doi.org/10.1103/physrevlett.97.048302	journal	July 2006
Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery E., Geacintov, N.; S., Broyde,; T., Buterin, Wiley-Blackwell https://doi.org/10.5167/uzh-14585	text	January 2002

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