XRCC1 prevents toxic PARP1 trapping during DNA base excision repair.

Animals Cell Line DNA / genetics DNA Breaks, Single-Stranded DNA Damage / drug effects DNA Ligase ATP / metabolism DNA Polymerase beta / metabolism DNA Repair / drug effects DNA-Binding Proteins / metabolism Fibroblasts / drug effects Humans Poly (ADP-Ribose) Polymerase-1 / metabolism Poly(ADP-ribose) Polymerase Inhibitors / pharmacology Poly(ADP-ribose) Polymerases / metabolism Protein Binding / drug effects X-ray Repair Cross Complementing Protein 1 / metabolism
PARP inhibitors PARP trapping PARP1 XRCC1 protein complexes base excision repair single-strand breaks

Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
15 07 2021
Historique:
received: 07 12 2020
revised: 08 03 2021
accepted: 10 05 2021
pubmed: 9 6 2021
medline: 31 7 2021
entrez: 8 6 2021
Statut: ppublish

Résumé

Mammalian DNA base excision repair (BER) is accelerated by poly(ADP-ribose) polymerases (PARPs) and the scaffold protein XRCC1. PARPs are sensors that detect single-strand break intermediates, but the critical role of XRCC1 during BER is unknown. Here, we show that protein complexes containing DNA polymerase β and DNA ligase III that are assembled by XRCC1 prevent excessive engagement and activity of PARP1 during BER. As a result, PARP1 becomes "trapped" on BER intermediates in XRCC1-deficient cells in a manner similar to that induced by PARP inhibitors, including in patient fibroblasts from XRCC1-mutated disease. This excessive PARP1 engagement and trapping renders BER intermediates inaccessible to enzymes such as DNA polymerase β and impedes their repair. Consequently, PARP1 deletion rescues BER and resistance to base damage in XRCC1

Identifiants

DOI: 10.1016/j.molcel.2021.05.009 PMID: 34102106 PMC: PMC8294329
pubmed: 34102106
pii: S1097-2765(21)00366-X
doi: 10.1016/j.molcel.2021.05.009
pmc: PMC8294329
pii:
doi:

Substances chimiques

DNA-Binding Proteins 0
Poly(ADP-ribose) Polymerase Inhibitors 0
X-ray Repair Cross Complementing Protein 1 0
XRCC1 protein, human 0
DNA 9007-49-2
PARP1 protein, human EC 2.4.2.30
Poly (ADP-Ribose) Polymerase-1 EC 2.4.2.30
Poly(ADP-ribose) Polymerases EC 2.4.2.30
DNA Polymerase beta EC 2.7.7.7
DNA Ligase ATP EC 6.5.1.1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3018-3030.e5

Subventions

Organisme : NCI NIH HHS
ID : R01 CA158073
Pays : United States
Organisme : European Research Council
ID : 694996
Pays : International
Organisme : Medical Research Council
ID : MR/P010121/1
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : R01 CA226852
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA215067
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA174653
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Annie A Demin (AA)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK.

Kouji Hirota (K)

Department of Radiation Genetics, Graduate School of Medicine, Kyoto University, Yoshidakonoe, Sakyo-ku, Kyoto 606-8501, Japan; Department of Chemistry, Tokyo Metropolitan University, Minami-Osawa, Hachioji-shi, Tokyo 192-0397, Japan.

Masataka Tsuda (M)

Department of Radiation Genetics, Graduate School of Medicine, Kyoto University, Yoshidakonoe, Sakyo-ku, Kyoto 606-8501, Japan; Program of Mathematical and Life Sciences, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi-Hiroshima 739-8526, Japan.

Marek Adamowicz (M)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK.

Richard Hailstone (R)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK.

Jan Brazina (J)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK.

William Gittens (W)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK.

Ilona Kalasova (I)

Department of Genome Dynamics, Institute of Molecular Genetics of the Czech Academy of Sciences, 142 20 Prague 4, Czech Republic.

Zhengping Shao (Z)

Institute for Cancer Genetics, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York City, NY 10032, USA.

Shan Zha (S)

Institute for Cancer Genetics, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York City, NY 10032, USA; Division of Pediatric Oncology, Hematology and Stem Cell Transplantation, Department of Pediatrics, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA.

Hiroyuki Sasanuma (H)

Department of Radiation Genetics, Graduate School of Medicine, Kyoto University, Yoshidakonoe, Sakyo-ku, Kyoto 606-8501, Japan.

Hana Hanzlikova (H)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK; Department of Genome Dynamics, Institute of Molecular Genetics of the Czech Academy of Sciences, 142 20 Prague 4, Czech Republic.

Shunichi Takeda (S)

Department of Radiation Genetics, Graduate School of Medicine, Kyoto University, Yoshidakonoe, Sakyo-ku, Kyoto 606-8501, Japan. Electronic address: stakeda@rg.med.kyoto-u.ac.jp.

Keith W Caldecott (KW)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9RQ, UK; Department of Genome Dynamics, Institute of Molecular Genetics of the Czech Academy of Sciences, 142 20 Prague 4, Czech Republic. Electronic address: k.w.caldecott@sussex.ac.uk.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Cellules › Cellules cultivées › Lignée cellulaire › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Phénomènes génétiques › Altération de l'ADN › Cassures de l'ADN › Cassures simple-brin de l'ADN › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Phénomènes génétiques › Altération de l'ADN › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Ligases › Polynucleotide ligases › DNA ligases › DNA ligase ATP › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › DNA nucleotidyltransferases › DNA-directed DNA polymerase › DNA polymerase beta › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Phénomènes génétiques › Réparation de l'ADN › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de liaison à l'ADN › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Cellules › Cellules du tissu conjonctif › Fibroblastes › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Glycosyltransferase › Pentosyltransferases › ADP ribose transferases › Poly(ADP-ribose) polymerases › Poly (ADP-Ribose) polymerase-1 › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Antinéoplasiques › Inhibiteurs de poly(ADP-ribose) polymérases › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Glycosyltransferase › Pentosyltransferases › ADP ribose transferases › Poly(ADP-ribose) polymerases › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Métabolisme › Liaison aux protéines › XRCC1 prevents toxic PARP1 trapping during DNA...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › Protéines liant le poly-adp-ribose › Protéine-1 de complémentation croisée de la réparation des lésions induites par les rayons X › XRCC1 prevents toxic PARP1 trapping during DNA...