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Structural and functional characterization of the PNKP–XRCC4–LigIV DNA repair complex

Journal Article · · Nucleic Acids Research
DOI:https://doi.org/10.1093/nar/gkx275· OSTI ID:1379659
 [1];  [2];  [1];  [1];  [2];  [2];  [1];  [2];  [3];  [3];  [4];  [5];  [2];  [2];  [1]
  1. Univ. of Alberta, Edmonton, AB (Canada). Dept. of Biochemistry
  2. Univ. of Calgary, AB (Canada). Dept. of Biochemistry and Molecular Biology
  3. Univ. of Alberta, Edmonton, AB (Canada). Dept. of Oncology
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging; Univ. of Texas, Houston, TX (United States). Dept. of Molecular and Cellular Oncology
Non-homologous end joining (NHEJ) repairs DNA double strand breaks in non-cycling eukaryotic cells. NHEJ relies on polynucleotide kinase/phosphatase (PNKP), which generates 5'-phosphate/3'-hydroxyl DNA termini that are critical for ligation by the NHEJ DNA ligase, LigIV. PNKP and LigIV require the NHEJ scaffolding protein, XRCC4. The PNKP FHA domain binds to the CK2-phosphorylated XRCC4 C-terminal tail, while LigIV uses its tandem BRCT repeats to bind the XRCC4 coiled-coil. Yet, the assembled PNKP-XRCC4-LigIV complex remains uncharacterized. Here, we report purification and characterization of a recombinant PNKP-XRCC4-LigIV complex. We show that the stable binding of PNKP in this complex requires XRCC4 phosphorylation and that only one PNKP protomer binds per XRCC4 dimer. Small angle X-ray scattering (SAXS) reveals a flexiblemultistate complex that suggests that both the PNKP FHA and catalytic domains contact the XRCC4 coiled-coil and LigIV BRCT repeats. Hydrogen-deuterium exchange indicates protection of a surface on the PNKP phosphatase domain that may contact XRCC4-LigIV. Amutation on this surface (E326K) causes the hereditary neuro-developmental disorder, MCSZ. This mutation impairs PNKP recruitment to damaged DNA in human cells and provides a possible disease mechanism. Together, this work unveils multipoint contacts between PNKP and XRCC4-LigIV that regulate PNKP recruitment and activity within NHEJ.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1379659
Journal Information:
Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 10 Vol. 45; ISSN 0305-1048
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (4)

Histone demethylase JMJD1A promotes expression of DNA repair factors and radio-resistance of prostate cancer cells journal April 2020
TDP1 suppresses mis-joining of radiomimetic DNA double-strand breaks and cooperates with Artemis to promote optimal nonhomologous end joining journal August 2018
Petri net–based model of the human DNA base excision repair pathway journal September 2019
DNA repair deficiency in neuropathogenesis: when all roads lead to mitochondria journal May 2019

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