Modular antibodies reveal DNA damage-induced mono-ADP-ribosylation as a second wave of PARP1 signaling.

Histones / genetics Poly (ADP-Ribose) Polymerase-1 / genetics ADP-Ribosylation Chromatin DNA Damage Antibodies / genetics Signal Transduction
ADP-ribosylation DNA damage response HPF1 PARP1 RNF114 SpyTag antibodies telomere

Journal

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

Informations de publication

Date de publication:
18 05 2023
Historique:
received: 10 10 2022
revised: 14 02 2023
accepted: 27 03 2023
medline: 22 5 2023
pubmed: 29 4 2023
entrez: 28 4 2023
Statut: ppublish

Résumé

PARP1, an established anti-cancer target that regulates many cellular pathways, including DNA repair signaling, has been intensely studied for decades as a poly(ADP-ribosyl)transferase. Although recent studies have revealed the prevalence of mono-ADP-ribosylation upon DNA damage, it was unknown whether this signal plays an active role in the cell or is just a byproduct of poly-ADP-ribosylation. By engineering SpyTag-based modular antibodies for sensitive and flexible detection of mono-ADP-ribosylation, including fluorescence-based sensors for live-cell imaging, we demonstrate that serine mono-ADP-ribosylation constitutes a second wave of PARP1 signaling shaped by the cellular HPF1/PARP1 ratio. Multilevel chromatin proteomics reveals histone mono-ADP-ribosylation readers, including RNF114, a ubiquitin ligase recruited to DNA lesions through a zinc-finger domain, modulating the DNA damage response and telomere maintenance. Our work provides a technological framework for illuminating ADP-ribosylation in a wide range of applications and biological contexts and establishes mono-ADP-ribosylation by HPF1/PARP1 as an important information carrier for cell signaling.

Identifiants

DOI: 10.1016/j.molcel.2023.03.027 PMID: 37116497 PMC: PMC10205078
pubmed: 37116497
pii: S1097-2765(23)00240-X
doi: 10.1016/j.molcel.2023.03.027
pmc: PMC10205078
pii:
doi:

Substances chimiques

Histones 0
Poly (ADP-Ribose) Polymerase-1 EC 2.4.2.30
Chromatin 0
Antibodies 0

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

1743-1760.e11

Subventions

Organisme : NCI NIH HHS
ID : R01 CA262316
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/R007195/1
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : R01 CA207209
Pays : United States
Organisme : Cancer Research UK
ID : C35050/A22284
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 101794
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 210634
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P30 CA047904
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM133332
Pays : United States

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests E.J.L., H.D., J.J.B., T.C., and I.M. declare the following competing financial interests: Max-Planck-Innovation, the technology transfer center of the Max Planck Society, has licensed the antibodies AbD33204, AbD33205, AbD33644, AbD34251, AbD33641, and AbD43647 to Bio-Rad Laboratories.

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Auteurs

Edoardo José Longarini (EJ)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Helen Dauben (H)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Carolina Locatelli (C)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Anne R Wondisford (AR)

Department of Pharmacology and Chemical Biology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, PA, USA.

Rebecca Smith (R)

Univ Rennes, CNRS, IGDR (Institut de Génétique et Développement de Rennes) - UMR 6290, BIOSIT (Biologie, Santé, Innovation Technologique de Rennes) - UMS 3480, US 018, 35000 Rennes, France.

Charlotte Muench (C)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Andreas Kolvenbach (A)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Michelle Lee Lynskey (ML)

Department of Pharmacology and Chemical Biology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, PA, USA.

Alexis Pope (A)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Juan José Bonfiglio (JJ)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Eva Pinto Jurado (EP)

Univ Rennes, CNRS, IGDR (Institut de Génétique et Développement de Rennes) - UMR 6290, BIOSIT (Biologie, Santé, Innovation Technologique de Rennes) - UMS 3480, US 018, 35000 Rennes, France; Laboratory of DNA Damage and Nuclear Dynamics, Institute of Genetics, Biological Research Centre, Eötvös Loránd Research Network (ELKH), 6276 Szeged, Hungary; Doctoral School of Multidisciplinary Medical Sciences, University of Szeged, 6276 Szeged, Hungary.

Roberta Fajka-Boja (R)

Laboratory of DNA Damage and Nuclear Dynamics, Institute of Genetics, Biological Research Centre, Eötvös Loránd Research Network (ELKH), 6276 Szeged, Hungary; Department of Immunology, Albert Szent-Györgyi Medical School, Faculty of Science and Informatics, University of Szeged, 6720 Szeged, Hungary.

Thomas Colby (T)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany.

Marion Schuller (M)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Ivan Ahel (I)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Gyula Timinszky (G)

Laboratory of DNA Damage and Nuclear Dynamics, Institute of Genetics, Biological Research Centre, Eötvös Loránd Research Network (ELKH), 6276 Szeged, Hungary.

Roderick J O'Sullivan (RJ)

Department of Pharmacology and Chemical Biology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, PA, USA.

Sébastien Huet (S)

Univ Rennes, CNRS, IGDR (Institut de Génétique et Développement de Rennes) - UMR 6290, BIOSIT (Biologie, Santé, Innovation Technologique de Rennes) - UMS 3480, US 018, 35000 Rennes, France; Institut Universitaire de France, Paris, France. Electronic address: sebastien.huet@univ-rennes.fr.

Ivan Matic (I)

Research Group of Proteomics and ADP-Ribosylation Signaling, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany; Cologne Excellence Cluster for Stress Responses in Ageing-Associated Diseases (CECAD), University of Cologne, 50931 Cologne, Germany. Electronic address: imatic@age.mpg.de.

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Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Glycosyltransferase › Pentosyltransferases › ADP ribose transferases › Poly(ADP-ribose) polymerases › Poly (ADP-Ribose) polymerase-1 › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › ADP-Ribosylation › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Phénomènes génétiques › Altération de l'ADN › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Globulines › Sérum-globulines › Immunoglobulines › Anticorps › Modular antibodies reveal DNA damage-induced...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Modular antibodies reveal DNA damage-induced...