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Title: Kinetic gating mechanism of DNA damage recognition by Rad4/XPC

Abstract

The xeroderma pigmentosum C (XPC) complex initiates nucleotide excision repair by recognizing DNA lesions before recruiting downstream factors. How XPC detects structurally diverse lesions embedded within normal DNA is unknown. Here we present a crystal structure that captures the yeast XPC orthologue (Rad4) on a single register of undamaged DNA. The structure shows that a disulphide-tethered Rad4 flips out normal nucleotides and adopts a conformation similar to that seen with damaged DNA. Contrary to many DNA repair enzymes that can directly reject non-target sites as structural misfits, our results suggest that Rad4/XPC uses a kinetic gating mechanism whereby lesion selectivity arises from the kinetic competition between DNA opening and the residence time of Rad4/XPC per site. This mechanism is further supported by measurements of Rad4-induced lesion-opening times using temperature-jump perturbation spectroscopy. Lastly, kinetic gating may be a general mechanism used by site-specific DNA-binding proteins to minimize time-consuming interrogations of non-target sites.

Authors:
 [1];  [1];  [2];  [1];  [1];  [3];  [4];  [4];  [2];  [1];  [1]
  1. Univ. of Illinois at Chicago, Chicago, IL (United States)
  2. The Univ. of Chicago, Chicago, IL (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States)
  4. Univ. of Pittsburgh, Pittsburgh, PA (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1225230
Alternate Identifier(s):
OSTI ID: 1253601
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biological sciences; biophysics; biochemistry

Citation Formats

Chen, Xuejing, Velmurugu, Yogambigai, Zheng, Guanqun, Park, Beomseok, Shim, Yoonjung, Kim, Youngchang, Liu, Lili, Van Houten, Bennett, He, Chuan, Ansari, Anjum, and Min, Jung -Hyun. Kinetic gating mechanism of DNA damage recognition by Rad4/XPC. United States: N. p., 2015. Web. doi:10.1038/ncomms6849.
Chen, Xuejing, Velmurugu, Yogambigai, Zheng, Guanqun, Park, Beomseok, Shim, Yoonjung, Kim, Youngchang, Liu, Lili, Van Houten, Bennett, He, Chuan, Ansari, Anjum, & Min, Jung -Hyun. Kinetic gating mechanism of DNA damage recognition by Rad4/XPC. United States. https://doi.org/10.1038/ncomms6849
Chen, Xuejing, Velmurugu, Yogambigai, Zheng, Guanqun, Park, Beomseok, Shim, Yoonjung, Kim, Youngchang, Liu, Lili, Van Houten, Bennett, He, Chuan, Ansari, Anjum, and Min, Jung -Hyun. Tue . "Kinetic gating mechanism of DNA damage recognition by Rad4/XPC". United States. https://doi.org/10.1038/ncomms6849. https://www.osti.gov/servlets/purl/1225230.
@article{osti_1225230,
title = {Kinetic gating mechanism of DNA damage recognition by Rad4/XPC},
author = {Chen, Xuejing and Velmurugu, Yogambigai and Zheng, Guanqun and Park, Beomseok and Shim, Yoonjung and Kim, Youngchang and Liu, Lili and Van Houten, Bennett and He, Chuan and Ansari, Anjum and Min, Jung -Hyun},
abstractNote = {The xeroderma pigmentosum C (XPC) complex initiates nucleotide excision repair by recognizing DNA lesions before recruiting downstream factors. How XPC detects structurally diverse lesions embedded within normal DNA is unknown. Here we present a crystal structure that captures the yeast XPC orthologue (Rad4) on a single register of undamaged DNA. The structure shows that a disulphide-tethered Rad4 flips out normal nucleotides and adopts a conformation similar to that seen with damaged DNA. Contrary to many DNA repair enzymes that can directly reject non-target sites as structural misfits, our results suggest that Rad4/XPC uses a kinetic gating mechanism whereby lesion selectivity arises from the kinetic competition between DNA opening and the residence time of Rad4/XPC per site. This mechanism is further supported by measurements of Rad4-induced lesion-opening times using temperature-jump perturbation spectroscopy. Lastly, kinetic gating may be a general mechanism used by site-specific DNA-binding proteins to minimize time-consuming interrogations of non-target sites.},
doi = {10.1038/ncomms6849},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {Tue Jan 06 00:00:00 EST 2015},
month = {Tue Jan 06 00:00:00 EST 2015}
}

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journal, July 2011


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Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory
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The XPC−HR23B Complex Displays High Affinity and Specificity for Damaged DNA in a True-Equilibrium Fluorescence Assay
journal, May 2002

  • Hey, Thomas; Lipps, Georg; Sugasawa, Kaoru
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Pre-Steady-State Binding of Damaged DNA by XPC−hHR23B Reveals a Kinetic Mechanism for Damage Discrimination
journal, February 2006

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  • Biochemistry, Vol. 45, Issue 6
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Detection of Damaged DNA Bases by DNA Glycosylase Enzymes
journal, June 2010

  • Friedman, Joshua I.; Stivers, James T.
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Kinetic Mechanism of Damage Site Recognition and Uracil Flipping by Escherichia coli Uracil DNA Glycosylase
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journal, February 2006

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Base Flipping Free Energy Profiles for Damaged and Undamaged DNA
journal, December 2010

  • Zheng, Han; Cai, Yuqin; Ding, Shuang
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  • DOI: 10.1021/tx1003613

The Efficiencies of Damage Recognition and Excision Correlate with Duplex Destabilization Induced by Acetylaminofluorene Adducts in Human Nucleotide Excision Repair
journal, August 2012

  • Yeo, Jung-Eun; Khoo, Andy; Fagbemi, Adebanke F.
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  • DOI: 10.1021/tx3003033

Adenine–DNA Adducts Derived from the Highly Tumorigenic Dibenzo[ a , l ]pyrene Are Resistant to Nucleotide Excision Repair while Guanine Adducts Are Not
journal, April 2013

  • Kropachev, Konstantin; Kolbanovskiy, Marina; Liu, Zhi
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  • DOI: 10.1021/tx400080k

Recognition of DNA damage by the Rad4 nucleotide excision repair protein
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Timing facilitated site transfer of an enzyme on DNA
journal, January 2012

  • Schonhoft, Joseph D.; Stivers, James T.
  • Nature Chemical Biology, Vol. 8, Issue 2
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Duplex interrogation by a direct DNA repair protein in search of base damage
journal, June 2012

  • Yi, Chengqi; Chen, Baoen; Qi, Bo
  • Nature Structural & Molecular Biology, Vol. 19, Issue 7
  • DOI: 10.1038/nsmb.2320

A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA
journal, April 2006

  • Blainey, P. C.; van Oijen, A. M.; Banerjee, A.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 15
  • DOI: 10.1073/pnas.0509723103

Direct observation of DNA bending/unbending kinetics in complex with DNA-bending protein IHF
journal, November 2006

  • Kuznetsov, S. V.; Sugimura, S.; Vivas, P.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 49
  • DOI: 10.1073/pnas.0608394103

Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity
journal, October 1974


Loop dependence of the stability and dynamics of nucleic acid hairpins
journal, December 2007

  • Kuznetsov, S. V.; Ren, C. -C.; Woodson, S. A.
  • Nucleic Acids Research, Vol. 36, Issue 4
  • DOI: 10.1093/nar/gkm1083

A multistep damage recognition mechanism for global genomic nucleotide excision repair
journal, March 2001


Structure of a DNA Glycosylase Searching for Lesions
journal, February 2006


Role of nucleotide excision repair proteins in oxidative DNA damage repair: an updating
journal, January 2011


Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC
journal, September 2008

  • Hoogstraten, Deborah; Bergink, Steven; Verbiest, Vincent H. M.
  • Journal of Cell Science, Vol. 121, Issue 17
  • DOI: 10.1242/jcs.03502

Regulation of Nucleotide Excision Repair by UV-DDB: Prioritization of Damage Recognition to Internucleosomal DNA
journal, October 2011


A Nuclear Magnetic Resonance Investigation of the Energetics of Basepair Opening Pathways in DNA
journal, November 2005


PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.45787

Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein
text, January 2009

  • Camenisch, U.; Träutlein, D.; Clement, F. C.
  • Nature Publishing Group
  • DOI: 10.5167/uzh-29904

Works referencing / citing this record:

Xeroderma pigmentosum group C sensor: unprecedented recognition strategy and tight spatiotemporal regulation
journal, October 2015

  • Puumalainen, Marjo-Riitta; Rüthemann, Peter; Min, Jun-Hyun
  • Cellular and Molecular Life Sciences, Vol. 73, Issue 3
  • DOI: 10.1007/s00018-015-2075-z

Single-molecule visualization reveals the damage search mechanism for the human NER protein XPC-RAD23B
journal, August 2019

  • Cheon, Na Young; Kim, Hyun-Suk; Yeo, Jung-Eun
  • Nucleic Acids Research, Vol. 47, Issue 16
  • DOI: 10.1093/nar/gkz629

The mTORC1-4E-BP-eIF4E axis controls de novo Bcl6 protein synthesis in T cells and systemic autoimmunity
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Mechanism and regulation of DNA damage recognition in nucleotide excision repair
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BmNPV infection correlates with the enhancement of the resistance of Bombyx mori cells to UV radiation
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Twist-open mechanism of DNA damage recognition by the Rad4/XPC nucleotide excision repair complex
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Xeroderma pigmentosum group C sensor: unprecedented recognition strategy and tight spatiotemporal regulation
text, January 2016

  • Puumalainen, Marjo-Riitta; Rüthemann, Peter; Min, Jun-Hyun
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Xeroderma pigmentosum group C sensor: unprecedented recognition strategy and tight spatiotemporal regulation
journal, October 2015

  • Puumalainen, Marjo-Riitta; Rüthemann, Peter; Min, Jun-Hyun
  • Cellular and Molecular Life Sciences, Vol. 73, Issue 3
  • DOI: 10.1007/s00018-015-2075-z

Recognition of Damaged DNA for Nucleotide Excision Repair: A Correlated Motion Mechanism with a Mismatched cis-syn Thymine Dimer Lesion
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The mTORC1-4E-BP-eIF4E axis controls de novo Bcl6 protein synthesis in T cells and systemic autoimmunity
journal, August 2017


Sequence specificity, energetics and mechanism of mismatch recognition by DNA damage sensing protein Rad4/XPC
journal, February 2020

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Structure and mechanism of pyrimidine–pyrimidone (6-4) photoproduct recognition by the Rad4/XPC nucleotide excision repair complex
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  • DOI: 10.1093/nar/gkz359

Single-molecule visualization reveals the damage search mechanism for the human NER protein XPC-RAD23B
journal, August 2019

  • Cheon, Na Young; Kim, Hyun-Suk; Yeo, Jung-Eun
  • Nucleic Acids Research, Vol. 47, Issue 16
  • DOI: 10.1093/nar/gkz629

Mechanism and regulation of DNA damage recognition in nucleotide excision repair
journal, January 2019


Dissociation Dynamics of XPC-RAD23B from Damaged DNA Is a Determining Factor of NER Efficiency
journal, June 2016