Mechanism of DNA Lesion Homing and Recognition by the Uvr Nucleotide Excision Repair System

Lee, Seung-Joo; Sung, Rou-Jia; Verdine, Gregory L.

doi:10.34133/2019/5641746

Title: Mechanism of DNA Lesion Homing and Recognition by the Uvr Nucleotide Excision Repair System

Journal Article · Wed Aug 28 04:00:00 UTC 2019 · Research

DOI: https://doi.org/10.34133/2019/5641746 · OSTI ID:1837249

^[1]; Sung, Rou-Jia ^[2]; Verdine, Gregory L. ^[3]

Harvard Univ., Cambridge, MA (United States). Dept. of Stem Cell and Regenerative Biology
Harvard Univ., Cambridge, MA (United States). Dept. of Molecular and Cellular Biology
Harvard Univ., Cambridge, MA (United States). Dept. of Stem Cell and Regenerative Biology. Dept. of Molecular and Cellular Biology. Dept. of Chemistry and Chemical Biology

Nucleotide excision repair (NER) is an essential DNA repair system distinguished from other such systems by its extraordinary versatility. NER removes a wide variety of structurally dissimilar lesions having only their bulkiness in common. NER can also repair several less bulky nucleobase lesions, such as 8-oxoguanine. Thus, how a single DNA repair system distinguishes such a diverse array of structurally divergent lesions from undamaged DNA has been one of the great unsolved mysteries in the field of genome maintenance. Here we employ a synthetic crystallography approach to obtain crystal structures of the pivotal NER enzyme UvrB in complex with duplex DNA, trapped at the stage of lesion-recognition. These structures coupled with biochemical studies suggest that UvrB integrates the ATPase-dependent helicase/translocase and lesion-recognition activities. Our work also conclusively establishes the identity of the lesion-containing strand and provides a compelling insight to how UvrB recognizes a diverse array of DNA lesions.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC)

OSTI ID:: 1837249

Journal Information:: Research, Journal Name: Research Vol. 2019; ISSN 2639-5274

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Structural and Functional Characterization of the Human DNA Repair Helicase XPD by Comparative Molecular Modeling and Site-directed Mutagenesis of the Bacterial Repair Protein UvrB Bienstock, Rachelle J.; Skorvaga, Milan; Mandavilli, Bhaskar S. Journal of Biological Chemistry, Vol. 278, Issue 7 https://doi.org/10.1074/jbc.m210159200	journal	November 2002
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Strand opening by the UvrA2B complex allows dynamic recognition of DNA damage Zou, Y. The EMBO Journal, Vol. 18, Issue 17 https://doi.org/10.1093/emboj/18.17.4889	journal	September 1999
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ATPase activity of the UvrA and UvrAB protein complexes of the Escherichia coli UvrABC endonuclease Oh, Euk Y.; Claassen, Lark; Thiagalingam, Sambasivamoorthy Nucleic Acids Research, Vol. 17, Issue 11 https://doi.org/10.1093/nar/17.11.4145	journal	January 1989
Crystal structure of the UvrB dimer: insights into the nature and functioning of the UvrAB damage engagement and UvrB–DNA complexes Webster, Matthew P. J.; Jukes, Rachael; Zamfir, Vlad S. Nucleic Acids Research, Vol. 40, Issue 17 https://doi.org/10.1093/nar/gks633	journal	June 2012
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Structure of a DNA Glycosylase Searching for Lesions Banerjee, A. Science, Vol. 311, Issue 5764 https://doi.org/10.1126/science.1120288	journal	February 2006
Structure of a Covalently Trapped Catalytic Complex of HIV-1 Reverse Transcriptase: Implications for Drug Resistance Huang, H. Science, Vol. 282, Issue 5394 https://doi.org/10.1126/science.282.5394.1669	journal	November 1998
Quality Control by DNA Repair Lindahl, T. Science, Vol. 286, Issue 5446 https://doi.org/10.1126/science.286.5446.1897	journal	December 1999
Covalent Trapping of Protein-DNA Complexes Verdine, Gregory L.; Norman, Derek P. G. Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161447	journal	June 2003
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PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Mechanism of action of theEscherichia coli UvrABC nuclease: Clues to the damage recognition problem Van Houten, Ben; Snowden, Amanda BioEssays, Vol. 15, Issue 1 https://doi.org/10.1002/bies.950150108	journal	January 1993
Prokaryotic Nucleotide Excision Repair: The UvrABC System Truglio, James J.; Croteau, Deborah L.; Van Houten, Bennett ChemInform, Vol. 37, Issue 20 https://doi.org/10.1002/chin.200620265	journal	May 2006
Helicase Motifs V and VI of the Escherichia coli UvrB Protein of the UvrABC Endonuclease Are Essential for the Formation of the Preincision Complex Moolenaar, Geri F.; Visse, Rob; Ortiz-Buysse, Mario Journal of Molecular Biology, Vol. 240, Issue 4 https://doi.org/10.1006/jmbi.1994.1447	journal	July 1994
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UvrABC nuclease complex repairs thymine glycol, an oxidative DNA base damage Kow, Yoke W.; Wallace, Susan S.; Van Houten, Bennett Mutation Research/DNA Repair, Vol. 235, Issue 2 https://doi.org/10.1016/0921-8777(90)90068-G	journal	March 1990
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The nucleotide excision repair protein UvrB, a helicase-like enzyme with a catch Theis, Karsten; Skorvaga, Milan; Machius, Mischa Mutation Research/DNA Repair, Vol. 460, Issue 3-4 https://doi.org/10.1016/S0921-8777(00)00032-X	journal	August 2000
Structural Basis for RNA Unwinding by the DEAD-Box Protein Drosophila Vasa Sengoku, Toru; Nureki, Osamu; Nakamura, Akira Cell, Vol. 125, Issue 2 https://doi.org/10.1016/j.cell.2006.01.054	journal	April 2006
The Crystal Structure of the Exon Junction Complex Reveals How It Maintains a Stable Grip on mRNA Bono, Fulvia; Ebert, Judith; Lorentzen, Esben Cell, Vol. 126, Issue 4 https://doi.org/10.1016/j.cell.2006.08.006	journal	August 2006
UvrD Helicase Unwinds DNA One Base Pair at a Time by a Two-Part Power Stroke Lee, Jae Young; Yang, Wei Cell, Vol. 127, Issue 7 https://doi.org/10.1016/j.cell.2006.10.049	journal	December 2006
Functions of base flipping in E. coli nucleotide excision repair Malta, E.; Verhagen, C.; Moolenaar, G. DNA Repair, Vol. 7, Issue 10 https://doi.org/10.1016/j.dnarep.2008.06.011	journal	October 2008
Damage detection by the UvrABC pathway: Crystal structure of UvrB bound to fluorescein-adducted DNA Waters, Timothy R.; Eryilmaz, Jitka; Geddes, Stella FEBS Letters, Vol. 580, Issue 27 https://doi.org/10.1016/j.febslet.2006.10.051	journal	November 2006
Crystal Structure of Bacillus stearothermophilus UvrA Provides Insight into ATP-Modulated Dimerization, UvrB Interaction, and DNA Binding Pakotiprapha, Danaya; Inuzuka, Yoshihiko; Bowman, Brian R. Molecular Cell, Vol. 29, Issue 1 https://doi.org/10.1016/j.molcel.2007.10.026	journal	January 2008
Exploring Damage Recognition Models in Prokaryotic Nucleotide Excision Repair with a Benzo[ a ]pyrene-Derived Lesion in UvrB Jia, Lei; Kropachev, Konstantin; Ding, Shuang Biochemistry, Vol. 48, Issue 38 https://doi.org/10.1021/bi9010072	journal	September 2009
Prokaryotic Nucleotide Excision Repair: The UvrABC System Truglio, James J.; Croteau, Deborah L.; Van Houten, Bennett Chemical Reviews, Vol. 106, Issue 2 https://doi.org/10.1021/cr040471u	journal	February 2006
Repair of Hydantoin Lesions and Their Amine Adducts in DNA by Base and Nucleotide Excision Repair McKibbin, Paige L.; Fleming, Aaron M.; Towheed, Mohammad Atif Journal of the American Chemical Society, Vol. 135, Issue 37 https://doi.org/10.1021/ja4059469	journal	September 2013
Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase Fromme, J. Christopher; Banerjee, Anirban; Huang, Susan J. Nature, Vol. 427, Issue 6975 https://doi.org/10.1038/nature02306	journal	February 2004
Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA Banerjee, Anirban; Yang, Wei; Karplus, Martin Nature, Vol. 434, Issue 7033 https://doi.org/10.1038/nature03458	journal	March 2005
Crystal structures of DNA/RNA repair enzymes AlkB and ABH2 bound to dsDNA Yang, Cai-Guang; Yi, Chengqi; Duguid, Erica M. Nature, Vol. 452, Issue 7190 https://doi.org/10.1038/nature06889	journal	April 2008
Encounter and extrusion of an intrahelical lesion by a DNA repair enzyme Qi, Yan; Spong, Marie C.; Nam, Kwangho Nature, Vol. 462, Issue 7274 https://doi.org/10.1038/nature08561	journal	December 2009
Understanding nucleotide excision repair and its roles in cancer and ageing Marteijn, Jurgen A.; Lans, Hannes; Vermeulen, Wim Nature Reviews Molecular Cell Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nrm3822	journal	June 2014
Structural basis of HIV-1 resistance to AZT by excision Tu, Xiongying; Das, Kalyan; Han, Qianwei Nature Structural & Molecular Biology, Vol. 17, Issue 10 https://doi.org/10.1038/nsmb.1908	journal	September 2010
Structure of UvrA nucleotide excision repair protein in complex with modified DNA Jaciuk, Marcin; Nowak, Elżbieta; Skowronek, Krzysztof Nature Structural & Molecular Biology, Vol. 18, Issue 2 https://doi.org/10.1038/nsmb.1973	journal	January 2011
Structure and mechanism of the UvrA–UvrB DNA damage sensor Pakotiprapha, Danaya; Samuels, Martin; Shen, Koning Nature Structural & Molecular Biology, Vol. 19, Issue 3 https://doi.org/10.1038/nsmb.2240	journal	February 2012
Structural basis for DNA recognition and processing by UvrB Truglio, James J.; Karakas, Erkan; Rhau, Benjamin Nature Structural & Molecular Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nsmb1072	journal	March 2006
Structural basis for DNA duplex separation by a superfamily-2 helicase Büttner, Katharina; Nehring, Sebastian; Hopfner, Karl-Peter Nature Structural & Molecular Biology, Vol. 14, Issue 7 https://doi.org/10.1038/nsmb1246	journal	June 2007
Structural insights into the first incision reaction during nucleotide excision repair Truglio, James J.; Rhau, Benjamin; Croteau, Deborah L. The EMBO Journal, Vol. 24, Issue 5 https://doi.org/10.1038/sj.emboj.7600568	journal	February 2005
Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad Karakas, Erkan; Truglio, James J.; Croteau, Deborah The EMBO Journal, Vol. 26, Issue 2 https://doi.org/10.1038/sj.emboj.7601497	journal	January 2007
DNA Damage, Aging, and Cancer Hoeijmakers, Jan H. J. New England Journal of Medicine, Vol. 361, Issue 15 https://doi.org/10.1056/NEJMra0804615	journal	October 2009
DNA Damage, Aging, and Cancer Hoeijmakers, Jan H. J. New England Journal of Medicine, Vol. 361, Issue 15 https://doi.org/10.1056/nejmra0804615	journal	October 2009
Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism Gu, M.; Rice, C. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 2 https://doi.org/10.1073/pnas.0913380107	journal	December 2009
The Disappearance of Thymine Dimers from dna: an Error-Correcting Mechanism Setlow, R. B.; Carrier, W. L. Proceedings of the National Academy of Sciences, Vol. 51, Issue 2 https://doi.org/10.1073/pnas.51.2.226	journal	February 1964
Structural and Functional Characterization of the Human DNA Repair Helicase XPD by Comparative Molecular Modeling and Site-directed Mutagenesis of the Bacterial Repair Protein UvrB Bienstock, Rachelle J.; Skorvaga, Milan; Mandavilli, Bhaskar S. Journal of Biological Chemistry, Vol. 278, Issue 7 https://doi.org/10.1074/jbc.M210159200	journal	November 2002
Identification of Residues within UvrB That Are Important for Efficient DNA Binding and Damage Processing Skorvaga, Milan; DellaVecchia, Matthew J.; Croteau, Deborah L. Journal of Biological Chemistry, Vol. 279, Issue 49 https://doi.org/10.1074/jbc.M409266200	journal	December 2004
Base Flipping in Nucleotide Excision Repair Malta, Erik; Moolenaar, Geri F.; Goosen, Nora Journal of Biological Chemistry, Vol. 281, Issue 4 https://doi.org/10.1074/jbc.M508901200	journal	January 2006
Strand opening by the UvrA2B complex allows dynamic recognition of DNA damage Zou, Y. The EMBO Journal, Vol. 18, Issue 17 https://doi.org/10.1093/emboj/18.17.4889	journal	September 1999
Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair Theis, K. The EMBO Journal, Vol. 18, Issue 24 https://doi.org/10.1093/emboj/18.24.6899	journal	December 1999
Clue to damage recognition by UvrB: residues in the beta-hairpin structure prevent binding to non-damaged DNA Moolenaar, G. F. The EMBO Journal, Vol. 20, Issue 21 https://doi.org/10.1093/emboj/20.21.6140	journal	November 2001
The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands Verhoeven, E. E. A. The EMBO Journal, Vol. 21, Issue 15 https://doi.org/10.1093/emboj/cdf396	journal	August 2002
THREE LOCI IN ESCHERICHIA COLI K-12 THAT CONTROL THE EXCISION OF PYRIMIDINE DIMERS AND CERTAIN OTHER MUTAGEN PRODUCTS FROM DNA Howard-Flanders, Paul; Boyce, Richard P.; Theriot, Lee Genetics, Vol. 53, Issue 6 https://doi.org/10.1093/genetics/53.6.1119	journal	June 1966
ATPase activity of the UvrA and UvrAB protein complexes of the Escherichia coli UvrABC endonuclease Oh, Euk Y.; Claassen, Lark; Thiagalingam, Sambasivamoorthy Nucleic Acids Research, Vol. 17, Issue 11 https://doi.org/10.1093/nar/17.11.4145	journal	January 1989
Crystal structure of the UvrB dimer: insights into the nature and functioning of the UvrAB damage engagement and UvrB–DNA complexes Webster, Matthew P. J.; Jukes, Rachael; Zamfir, Vlad S. Nucleic Acids Research, Vol. 40, Issue 17 https://doi.org/10.1093/nar/gks633	journal	June 2012
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
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
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Structure of UvrA nucleotide excision repair protein in complex with modified DNA Nowak, E.; Jaciuk, M.; Skowronek, K. Acta Crystallographica Section A Foundations of Crystallography, Vol. 68, Issue a1 https://doi.org/10.1107/s0108767312097279	journal	August 2012
Structure of a DNA Glycosylase Searching for Lesions Banerjee, A. Science, Vol. 311, Issue 5764 https://doi.org/10.1126/science.1120288	journal	February 2006
Structure of a Covalently Trapped Catalytic Complex of HIV-1 Reverse Transcriptase: Implications for Drug Resistance Huang, H. Science, Vol. 282, Issue 5394 https://doi.org/10.1126/science.282.5394.1669	journal	November 1998
Quality Control by DNA Repair Lindahl, T. Science, Vol. 286, Issue 5446 https://doi.org/10.1126/science.286.5446.1897	journal	December 1999
Covalent Trapping of Protein-DNA Complexes Verdine, Gregory L.; Norman, Derek P. G. Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161447	journal	June 2003
Translocation and Unwinding Mechanisms of RNA and DNA Helicases Pyle, Anna Marie Annual Review of Biophysics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.biophys.37.032807.125908	journal	June 2008
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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Title: Mechanism of DNA Lesion Homing and Recognition by the Uvr Nucleotide Excision Repair System

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