Capturing snapshots of APE1 processing DNA damage

Freudenthal, Bret D.; Beard, William A.; Cuneo, Matthew J.; Dyrkheeva, Nadezhda S.; Wilson, Samuel H.

doi:10.1038/nsmb.3105

Title: Capturing snapshots of APE1 processing DNA damage

Journal Article · Mon Oct 12 00:00:00 EDT 2015 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/nsmb.3105· OSTI ID:1261477

Freudenthal, Bret D. ^[1]; Beard, William A. ^[2]; Cuneo, Matthew J. ^[3]; Dyrkheeva, Nadezhda S. ^[1]; Wilson, Samuel H. ^[2]

National Inst. of Environmental Health Sciences (NIEHS), Triangle Park, NC (United States); Univ. of Kansas Medical Center, Kansas City, KS (United States)
National Inst. of Environmental Health Sciences (NIEHS), Triangle Park, NC (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

DNA apurinic-apyrimidinic (AP) sites are prevalent noncoding threats to genomic stability and are processed by AP endonuclease 1 (APE1). APE1 incises the AP-site phosphodiester backbone, generating a DNA-repair intermediate that is potentially cytotoxic. The molecular events of the incision reaction remain elusive, owing in part to limited structural information. Here we report multiple high-resolution human APE1-DNA structures that divulge new features of the APE1 reaction, including the metal-binding site, the nucleophile and the arginine clamps that mediate product release. We also report APE1-DNA structures with a T-G mismatch 5' to the AP site, representing a clustered lesion occurring in methylated CpG dinucleotides. Moreover, these structures reveal that APE1 molds the T-G mismatch into a unique Watson-Crick-like geometry that distorts the active site, thus reducing incision. Finally, these snapshots provide mechanistic clarity for APE1 while affording a rational framework to manipulate biological responses to DNA damage.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of Environmental Health Sciences

Grant/Contract Number:: AC05-00OR22725; Z01-ES050158; Z01-ES050161

OSTI ID:: 1261477

Journal Information:: Nature Structural & Molecular Biology, Vol. 22, Issue 11; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 106 works

Citation information provided by
Web of Science

References (63)

Abasic Sites Stimulate Double-stranded DNA Cleavage Mediated by Topoisomerase II: DNA LESIONS AS ENDOGENOUS TOPOISOMERASE II POISONS Kingma, Paul S.; Corbett, Anita H.; Burcham, Philip C. Journal of Biological Chemistry, Vol. 270, Issue 37 https://doi.org/10.1074/jbc.270.37.21441	journal	September 1995
The abasic site as a challenge to DNA polymerase Cuniasse, Ph.; Fazakerley, G. V.; Guschlbauer, W. Journal of Molecular Biology, Vol. 213, Issue 2 https://doi.org/10.1016/S0022-2836(05)80192-5	journal	May 1990
Mutagenesis by Apurinic/Apyrimidinic Sites Loeb, L. A.; Preston, B. D. Annual Review of Genetics, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.ge.20.120186.001221	journal	December 1986
Endogenous DNA damage in humans: a review of quantitative data De Bont, R. Mutagenesis, Vol. 19, Issue 3 https://doi.org/10.1093/mutage/geh025	journal	May 2004
Reactions of oxyl radicals with DNA Breen, Anthony P.; Murphy, John A. Free Radical Biology and Medicine, Vol. 18, Issue 6 https://doi.org/10.1016/0891-5849(94)00209-3	journal	June 1995
Mammalian Base Excision Repair: the Forgotten Archangel Dianov, Grigory L.; Hübscher, Ulrich Nucleic Acids Research, Vol. 41, Issue 6 https://doi.org/10.1093/nar/gkt076	journal	February 2013
Overview of Base Excision Repair Biochemistry Kim, Yun-Jeong; M. Wilson III, David Current Molecular Pharmacology, Vol. 5, Issue 1 https://doi.org/10.2174/1874467211205010003	journal	January 2012
Recent advances in the structural mechanisms of DNA glycosylases Brooks, Sonja C.; Adhikary, Suraj; Rubinson, Emily H. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1834, Issue 1 https://doi.org/10.1016/j.bbapap.2012.10.005	journal	January 2013
Structure and Mechanism of DNA Polymerase β Beard, William A.; Wilson, Samuel H. Chemical Reviews, Vol. 106, Issue 2 https://doi.org/10.1021/cr0404904	journal	February 2006
DNA-bound structures and mutants reveal abasic DNA binding by APE1 DNA repair and coordination Mol, Clifford D.; Izumi, Tadahide; Mitra, Sankar Nature, Vol. 403, Issue 6768 https://doi.org/10.1038/35000249	journal	January 2000
Two divalent metal ions in the active site of a new crystal form of human apurinic/apyrimidinic endonuclease, ape1: implications for the catalytic mechanism 1 1Edited by I. A. Wilson Beernink, Peter T.; Segelke, Brent W.; Hadi, Masood Z. Journal of Molecular Biology, Vol. 307, Issue 4 https://doi.org/10.1006/jmbi.2001.4529	journal	April 2001
A “moving metal mechanism” for substrate cleavage by the DNA repair endonuclease APE-1 Oezguen, Numan; Schein, Catherine H.; Peddi, Srinivasa R. Proteins: Structure, Function, and Bioinformatics, Vol. 68, Issue 1 https://doi.org/10.1002/prot.21397	journal	April 2007
The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites Gorman, M. A. The EMBO Journal, Vol. 16, Issue 21 https://doi.org/10.1093/emboj/16.21.6548	journal	November 1997
Novel role of tyrosine in catalysis by human AP endonuclease 1 Mundle, Sophia T.; Fattal, Michael H.; Melo, Luisa F. DNA Repair, Vol. 3, Issue 11 https://doi.org/10.1016/j.dnarep.2004.06.009	journal	November 2004
Enzymatic Mechanism of Human Apurinic/Apyrimidinic Endonuclease against a THF AP Site Model Substrate ^† Mundle, Sophia T.; Delaney, James C.; Essigmann, John M. Biochemistry, Vol. 48, Issue 1 https://doi.org/10.1021/bi8016137	journal	January 2009
MD simulation and experimental evidence for Mg2+ binding at the b site in human AP endonuclease 1 Oezguen, Numan; Mantha, Anil K.; Izumi, Tadahide Bioinformation, Vol. 7, Issue 4 https://doi.org/10.6026/97320630007184	journal	October 2011
Conserved Structural Chemistry for Incision Activity in Structurally Non-homologous Apurinic/Apyrimidinic Endonuclease APE1 and Endonuclease IV DNA Repair Enzymes Tsutakawa, Susan E.; Shin, David S.; Mol, Clifford D. Journal of Biological Chemistry, Vol. 288, Issue 12 https://doi.org/10.1074/jbc.M112.422774	journal	January 2013
Characterization of Mg ²⁺ Binding to the DNA Repair Protein Apurinic/Apyrimidic Endonuclease 1 via Solid-State ²⁵ Mg NMR Spectroscopy Lipton, A. S.; Heck, R. W.; Primak, S. Journal of the American Chemical Society, Vol. 130, Issue 29 https://doi.org/10.1021/ja0776881	journal	July 2008
Observing a DNA Polymerase Choose Right from Wrong Freudenthal, Bret D.; Beard, William A.; Shock, David D. Cell, Vol. 154, Issue 1 https://doi.org/10.1016/j.cell.2013.05.048	journal	July 2013
Watching DNA polymerase η make a phosphodiester bond Nakamura, Teruya; Zhao, Ye; Yamagata, Yuriko Nature, Vol. 487, Issue 7406 https://doi.org/10.1038/nature11181	journal	July 2012
Visualizing phosphodiester-bond hydrolysis by an endonuclease Molina, Rafael; Stella, Stefano; Redondo, Pilar Nature Structural & Molecular Biology, Vol. 22, Issue 1 https://doi.org/10.1038/nsmb.2932	journal	December 2014
Mapping the protein-DNA interface and the metal-binding site of the major human apurinic/apyrimidinic endonuclease Nguyen, Lam H.; Barsky, Daniel; Erzberger, Jan P. Journal of Molecular Biology, Vol. 298, Issue 3 https://doi.org/10.1006/jmbi.2000.3653	journal	May 2000
The role of Mg2+ and specific amino acid residues in the catalytic reaction of the major human abasic endonuclease: new insights from EDTA-resistant incision of acyclic abasic site analogs and site-directed mutagenesis Erzberger, Jan P.; Wilson, David M. Journal of Molecular Biology, Vol. 290, Issue 2 https://doi.org/10.1006/jmbi.1999.2888	journal	July 1999
Pre-steady-state Kinetic Characterization of the AP Endonuclease Activity of Human AP Endonuclease 1 Maher, Robyn L.; Bloom, Linda B. Journal of Biological Chemistry, Vol. 282, Issue 42 https://doi.org/10.1074/jbc.M704341200	journal	August 2007
High-Resolution Crystal Structures Reveal Plasticity in the Metal Binding Site of Apurinic/Apyrimidinic Endonuclease I He, Hongzhen; Chen, Qiujia; Georgiadis, Millie M. Biochemistry, Vol. 53, Issue 41 https://doi.org/10.1021/bi500676p	journal	October 2014
Effects of Backbone Contacts 3‘ to the Abasic Site on the Cleavage and the Product Binding by Human Apurinic/Apyrimidinic Endonuclease (APE1) ^† Izumi, Tadahide; Schein, Catherine H.; Oezguen, Numan Biochemistry, Vol. 43, Issue 3 https://doi.org/10.1021/bi0346190	journal	January 2004
The human apurinic/apyrimidinic endonuclease-1 suppresses activation of poly(adp-ribose) polymerase-1 induced by DNA single strand breaks Peddi, Srinivasa R.; Chattopadhyay, Ranajoy; Naidu, C. V. Toxicology, Vol. 224, Issue 1-2 https://doi.org/10.1016/j.tox.2006.04.025	journal	July 2006
Incision Activity of Human Apurinic Endonuclease (Ape) at Abasic Site Analogs in DNA Wilson, David M.; Takeshita, Masaru; Grollman, Arthur P. Journal of Biological Chemistry, Vol. 270, Issue 27 https://doi.org/10.1074/jbc.270.27.16002	journal	July 1995
Transient-State Kinetics of Apurinic/Apyrimidinic (AP) Endonuclease 1 Acting on an Authentic AP Site and Commonly Used Substrate Analogs: The Effect of Diverse Metal Ions and Base Mismatches Schermerhorn, Kelly M.; Delaney, Sarah Biochemistry, Vol. 52, Issue 43 https://doi.org/10.1021/bi401218r	journal	October 2013
Rare Bases in Animal DNA Vanyushin, B. F.; Tkacheva, S. G.; Belozersky, A. N. Nature, Vol. 225, Issue 5236 https://doi.org/10.1038/225948a0	journal	March 1970
Number of CpG islands and genes in human and mouse. Antequera, F.; Bird, A. Proceedings of the National Academy of Sciences, Vol. 90, Issue 24 https://doi.org/10.1073/pnas.90.24.11995	journal	December 1993
The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA Shen, Jiang-Cheng; Rideout, William M.; Jones, Peter A. Nucleic Acids Research, Vol. 22, Issue 6 https://doi.org/10.1093/nar/22.6.972	journal	January 1994
Human Apurinic/Apyrimidinic Endonuclease 1 (APE1) Has 3′ RNA Phosphatase and 3′ Exoribonuclease Activities Chohan, Manbir; Mackedenski, Sebastian; Li, Wai-Ming Journal of Molecular Biology, Vol. 427, Issue 2 https://doi.org/10.1016/j.jmb.2014.12.001	journal	January 2015
Identification of Apurinic/apyrimidinic endonuclease 1 (APE1) as the endoribonuclease that cleaves c-myc mRNA Barnes, T.; Kim, W. -C.; Mantha, A. K. Nucleic Acids Research, Vol. 37, Issue 12 https://doi.org/10.1093/nar/gkp275	journal	April 2009
Two distinct human DNA diesterases that hydrolyze 3′-blocking deoxyribose fragments from oxidized DNA Chen, Davis S.; Herman, Tory; Demple, Bruce Nucleic Acids Research, Vol. 19, Issue 21 https://doi.org/10.1093/nar/19.21.5907	journal	January 1991
The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway Gros, L. Nucleic Acids Research, Vol. 32, Issue 1 https://doi.org/10.1093/nar/gkh165	journal	January 2004
APE1/Ref-1 as an emerging therapeutic target for various human diseases: phytochemical modulation of its functions Thakur, Shweta; Sarkar, Bibekananda; Cholia, Ravi P. Experimental & Molecular Medicine, Vol. 46, Issue 7 https://doi.org/10.1038/emm.2014.42	journal	July 2014
Recognition and repair of chemically heterogeneous structures at DNA ends: Detection and Repair of Abnormal DNA Termini Andres, Sara N.; Schellenberg, Matthew J.; Wallace, Bret D. Environmental and Molecular Mutagenesis, Vol. 56, Issue 1 https://doi.org/10.1002/em.21892	journal	August 2014
The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Xanthoudakis, S.; Smeyne, R. J.; Wallace, J. D. Proceedings of the National Academy of Sciences, Vol. 93, Issue 17 https://doi.org/10.1073/pnas.93.17.8919	journal	August 1996
Functional Assessment of Population and Tumor-Associated APE1 Protein Variants Illuzzi, Jennifer L.; Harris, Nicole A.; Manvilla, Brittney A. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0065922	journal	June 2013
Human AP endonuclease 1 (APE1): From mechanistic insights to druggable target in cancer Abbotts, Rachel; Madhusudan, Srinivasan Cancer Treatment Reviews, Vol. 36, Issue 5 https://doi.org/10.1016/j.ctrv.2009.12.006	journal	August 2010
The role of Asn-212 in the catalytic mechanism of human endonuclease APE1: Stopped-flow kinetic study of incision activity on a natural AP site and a tetrahydrofuran analogue Kanazhevskaya, Lyubov Yu.; Koval, Vladimir V.; Lomzov, Alexander A. DNA Repair, Vol. 21 https://doi.org/10.1016/j.dnarep.2014.06.008	journal	September 2014
Mechanism of repair of 5′-topoisomerase II–DNA adducts by mammalian tyrosyl-DNA phosphodiesterase 2 Schellenberg, Matthew J.; Appel, C. Denise; Adhikari, Sanjay Nature Structural & Molecular Biology, Vol. 19, Issue 12 https://doi.org/10.1038/nsmb.2418	journal	October 2012
Structural basis for the recognition and cleavage of abasic DNA in Neisseria meningitidis Lu, D.; Silhan, J.; MacDonald, J. T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 42 https://doi.org/10.1073/pnas.1206563109	journal	October 2012
Initiation of DNA replication at CpG islands in mammalian chromosomes Delgado, S. The EMBO Journal, Vol. 17, Issue 8 https://doi.org/10.1093/emboj/17.8.2426	journal	April 1998
Mutagenesis of 8-Oxoguanine Adjacent to an Abasic Site in Simian Kidney Cells: Tandem Mutations and Enhancement of G→T Transversions Kalam, M. Abul; Basu, Ashis K. Chemical Research in Toxicology, Vol. 18, Issue 8 https://doi.org/10.1021/tx050119r	journal	August 2005
Visualizing transient Watson–Crick-like mispairs in DNA and RNA duplexes Kimsey, Isaac J.; Petzold, Katja; Sathyamoorthy, Bharathwaj Nature, Vol. 519, Issue 7543 https://doi.org/10.1038/nature14227	journal	March 2015
Replication infidelity via a mismatch with Watson–Crick geometry Bebenek, Katarzyna; Pedersen, Lars C.; Kunkel, Thomas A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 5 https://doi.org/10.1073/pnas.1012825108	journal	January 2011
Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis Wang, W.; Hellinga, H. W.; Beese, L. S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 43 https://doi.org/10.1073/pnas.1114496108	journal	October 2011
Functional sites of interaction between release factor RF1 and the ribosome Wilson, Kevin S.; Nakamura, Yoshikazu; Ito, Koichi Nature Structural Biology, Vol. 7, Issue 10, p. 866-870 https://doi.org/10.1038/82818	journal	October 2000
An Electron Localization Function Study of the Lone Pair Chesnut, D. B. The Journal of Physical Chemistry A, Vol. 104, Issue 49 https://doi.org/10.1021/jp002957u	journal	December 2000
The DNA-Binding Domain of Human PARP-1 Interacts with DNA Single-Strand Breaks as a Monomer through Its Second Zinc Finger Eustermann, Sebastian; Videler, Hortense; Yang, Ji-Chun Journal of Molecular Biology, Vol. 407, Issue 1 https://doi.org/10.1016/j.jmb.2011.01.034	journal	March 2011
Substrate Binding by Human Apurinic/Apyrimidinic Endonuclease Indicates a Briggs-Haldane Mechanism Strauss, Phyllis R.; Beard, William A.; Patterson, Thomas A. Journal of Biological Chemistry, Vol. 272, Issue 2 https://doi.org/10.1074/jbc.272.2.1302	journal	January 1997
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Analytical expressions for the homotropic binding of ligand to protein dimers and trimers Lefurgy, Scott T.; Leyh, Thomas S. Analytical Biochemistry, Vol. 421, Issue 2 https://doi.org/10.1016/j.ab.2011.12.016	journal	February 2012
Structure and Mechanism of DNA Polymerase β Beard, William A.; Wilson, Samuel H. ChemInform, Vol. 37, Issue 21 https://doi.org/10.1002/chin.200621260	journal	May 2006
DNA Sequence Context Effects on the Glycosylase Activity of Human 8-Oxoguanine DNA Glycosylase Sassa, Akira; Beard, William A.; Prasad, Rajendra Journal of Biological Chemistry, Vol. 287, Issue 44 https://doi.org/10.1074/jbc.m112.397786	journal	September 2012
Base Excision Repair of Tandem Modifications in a Methylated CpG Dinucleotide Sassa, Akira; Çağlayan, Melike; Dyrkheeva, Nadezhda S. Journal of Biological Chemistry, Vol. 289, Issue 20 https://doi.org/10.1074/jbc.m114.557769	journal	April 2014
Coordination of Steps in Single-nucleotide Base Excision Repair Mediated by Apurinic/Apyrimidinic Endonuclease 1 and DNA Polymerase β Liu, Yuan; Prasad, Rajendra; Beard, William A. Journal of Biological Chemistry, Vol. 282, Issue 18 https://doi.org/10.1074/jbc.m611295200	journal	March 2007
Structure of human apurinic/apyrimidinic endonuclease 1 with the essential Mg ²⁺ cofactor Manvilla, Brittney A.; Pozharski, Edwin; Toth, Eric A. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12 https://doi.org/10.1107/s0907444913027042	journal	November 2013
A Dominant-Negative Form of the Major Human Abasic Endonuclease Enhances Cellular Sensitivity to Laboratory and Clinical DNA-Damaging Agents McNeill, D. R.; Wilson, D. M. Molecular Cancer Research, Vol. 5, Issue 1 https://doi.org/10.1158/1541-7786.mcr-06-0329	journal	January 2007
Watching a DNA polymerase in action Freudenthal, Bret D.; Beard, William A.; Wilson, Samuel H. Cell Cycle, Vol. 13, Issue 5 https://doi.org/10.4161/cc.27789	journal	January 2014

Cited By (26)

Role of AP-endonuclease (Ape1) active site residues in stabilization of the reactant enzyme-DNA complex Batebi, Hossein; Dragelj, Jovan; Imhof, Petra Proteins: Structure, Function, and Bioinformatics, Vol. 86, Issue 4 https://doi.org/10.1002/prot.25460	journal	February 2018
Damage sensor role of UV-DDB during base excision repair Jang, Sunbok; Kumar, Namrata; Beckwitt, Emily C. Nature Structural & Molecular Biology, Vol. 26, Issue 8 https://doi.org/10.1038/s41594-019-0261-7	journal	July 2019
Crystal Structure of Human Nocturnin Catalytic Domain Estrella, Michael A.; Du, Jin; Korennykh, Alexei Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34615-0	journal	November 2018
Effects of mono- and divalent metal ions on DNA binding and catalysis of human apurinic/apyrimidinic endonuclease 1 Miroshnikova, Anastasia D.; Kuznetsova, Alexandra A.; Vorobjev, Yuri N. Molecular BioSystems, Vol. 12, Issue 5 https://doi.org/10.1039/c6mb00128a	journal	January 2016
Oxidative DNA damage is epigenetic by regulating gene transcription via base excision repair Fleming, Aaron M.; Ding, Yun; Burrows, Cynthia J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1619809114	journal	January 2017
Functions of the major abasic endonuclease (APE1) in cell viability and genotoxin resistance McNeill, Daniel R.; Whitaker, Amy M.; Stark, Wesley J. Mutagenesis, Vol. 35, Issue 1 https://doi.org/10.1093/mutage/gez046	journal	December 2019
New perspectives in cancer biology from a study of canonical and non-canonical functions of base excision repair proteins with a focus on early steps Malfatti, Matilde Clarissa; Antoniali, Giulia; Codrich, Marta Mutagenesis, Vol. 35, Issue 1 https://doi.org/10.1093/mutage/gez051	journal	December 2019
Reversal of DNA damage induced Topoisomerase 2 DNA–protein crosslinks by Tdp2 Schellenberg, Matthew J.; Perera, Lalith; Strom, Christina N. Nucleic Acids Research, Vol. 44, Issue 8 https://doi.org/10.1093/nar/gkw228	journal	April 2016
PARP1 changes from three-dimensional DNA damage searching to one-dimensional diffusion after auto-PARylation or in the presence of APE1 Liu, Lili; Kong, Muwen; Gassman, Natalie R. Nucleic Acids Research, Vol. 45, Issue 22 https://doi.org/10.1093/nar/gkx1047	journal	November 2017
The structure of human Nocturnin reveals a conserved ribonuclease domain that represses target transcript translation and abundance in cells Abshire, Elizabeth T.; Chasseur, Jennifer; Bohn, Jennifer A. Nucleic Acids Research, Vol. 46, Issue 12 https://doi.org/10.1093/nar/gky412	journal	June 2018
Substrate specificity of human apurinic/apyrimidinic endonuclease APE1 in the nucleotide incision repair pathway Kuznetsova, Alexandra A.; Matveeva, Anna G.; Milov, Alexander D. Nucleic Acids Research, Vol. 46, Issue 21 https://doi.org/10.1093/nar/gky912	journal	October 2018
Structural basis for recognition and repair of the 3′-phosphate by NExo, a base excision DNA repair nuclease from Neisseria meningitidis Silhan, Jan; Zhao, Qiyuan; Boura, Evzen Nucleic Acids Research, Vol. 46, Issue 22 https://doi.org/10.1093/nar/gky934	journal	October 2018
APE1 senses DNA single-strand breaks for repair and signaling Lin, Yunfeng; Raj, Jude; Li, Jia Nucleic Acids Research, Vol. 48, Issue 4 https://doi.org/10.1093/nar/gkz1175	journal	December 2019
Nucleotide excision repair of abasic DNA lesions Kitsera, Nataliya; Rodriguez-Alvarez, Marta; Emmert, Steffen Nucleic Acids Research, Vol. 47, Issue 16 https://doi.org/10.1093/nar/gkz558	journal	June 2019
Apurinic/apyrimidinic (AP) endonuclease 1 processing of AP sites with 5′ mismatches Fairlamb, Max S.; Whitaker, Amy M.; Freudenthal, Bret D. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 8 https://doi.org/10.1107/s2059798318003340	journal	July 2018
Thermococcus Eurythermalis Endonuclease IV Can Cleave Various Apurinic/Apyrimidinic Site Analogues in ssDNA and dsDNA Wang, Wei-Wei; Zhou, Huan; Xie, Juan-Juan International Journal of Molecular Sciences, Vol. 20, Issue 1 https://doi.org/10.3390/ijms20010069	journal	December 2018
Inferring joint sequence-structural determinants of protein functional specificity Neuwald, Andrew F.; Aravind, L.; Altschul, Stephen F. eLife, Vol. 7 https://doi.org/10.7554/elife.29880	journal	January 2018
Oxidative DNA damage is epigenetic by regulating gene transcription via base excision repair Fleming, Aaron M.; Ding, Yun; Burrows, Cynthia J. Proceedings of the National Academy of Sciences https://doi.org/10.1101/069955	journal	August 2016
Reversal of DNA damage induced Topoisomerase 2 DNA–protein crosslinks by Tdp2 G., Williams, Jason; N., Strom, Christina; Scott, Williams, R. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/5aq9-6x39	text	January 2016
Biochemical studies on pulmonary response to inhalation of methylene chloride Sahu, Saura; Lowther, Donnie; Ulsamer, Andrew Toxicology Letters, Vol. 7, Issue 1 https://doi.org/10.1016/0378-4274(80)90083-1	journal	November 1980
Smoking gun for a rare mutation mechanism Goodman, Myron F. Nature, Vol. 554, Issue 7691 https://doi.org/10.1038/d41586-018-00418-6	journal	January 2018
Molecular snapshots of APE1 proofreading mismatches and removing DNA damage Whitaker, Amy M.; Flynn, Tony S.; Freudenthal, Bret D. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02175-y	journal	January 2018
Polymorphism of apyrimidinic DNA structures in the nucleosome Osakabe, Akihisa; Arimura, Yasuhiro; Matsumoto, Syota Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep41783	journal	January 2017
Abasic and oxidized ribonucleotides embedded in DNA are processed by human APE1 and not by RNase H2 Malfatti, Matilde Clarissa; Balachander, Sathya; Antoniali, Giulia Nucleic Acids Research, Vol. 45, Issue 19 https://doi.org/10.1093/nar/gkx723	journal	August 2017
Human Apurinic/Apyrimidinic Endonuclease (APE1) Is Acetylated at DNA Damage Sites in Chromatin, and Acetylation Modulates Its DNA Repair Activity Roychoudhury, Shrabasti; Nath, Somsubhra; Song, Heyu Molecular and Cellular Biology, Vol. 37, Issue 6 https://doi.org/10.1128/mcb.00401-16	journal	March 2017
Insights into Mechanisms of Damage Recognition and Catalysis by APE1-like Enzymes Bulygin, Anatoly A.; Fedorova, Olga S.; Kuznetsov, Nikita A. International Journal of Molecular Sciences, Vol. 23, Issue 8 https://doi.org/10.3390/ijms23084361	journal	April 2022

Similar Records

Conserved structural chemistry for incision activity in structurally non-homologous apurinic/apyrimidinic endonuclease APE1 and endonuclease IV DNA repair enzymes.

Journal Article · Fri Mar 22 00:00:00 EDT 2013 · Journal of Biological Chemistry · OSTI ID:1261477

Tsutakawa, Susan E.; Shin, David S.; Mol, Clifford D.; +13 more

NMR studies of abasic sites in DNA duplexes: deoxyadenosine stacks into the helix opposite the cyclic analog of 2-deoxyribose

Journal Article · Tue Feb 09 00:00:00 EST 1988 · Biochemistry; (United States) · OSTI ID:1261477

Kalnik, M W; Chang, C N; Grollman, A P; +1 more

Selective inhibition by methoxyamine of the apurinic/apyrimidinic endonuclease activity associated with pyrimidine dimer-DNA glycosylases from Micrococcus luteus and bacteriophage T4

Journal Article · Tue Jun 16 00:00:00 EDT 1987 · Biochemistry; (United States) · OSTI ID:1261477

Liuzzi, M; Weinfeld, M; Paterson, M C

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Capturing snapshots of APE1 processing DNA damage

Citation Formats

References (63)

Cited By (26)

Similar Records

Related Subjects