Loss of RNF43 Function Contributes to Gastric Carcinogenesis by Impairing DNA Damage Response.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2021
Historique:
received: 25 06 2020
revised: 05 11 2020
accepted: 06 11 2020
pubmed: 15 11 2020
medline: 8 3 2022
entrez: 14 11 2020
Statut: ppublish

Résumé

RING finger protein 43 (RNF43) is a tumor suppressor that frequently is mutated in gastric tumors. The link between RNF43 and modulation of Wingless-related integration site (WNT) signaling has not been shown clearly in the stomach. Because mutations in RNF43 are highly enriched in microsatellite-unstable gastric tumors, which show defects in DNA damage response (DDR), we investigated whether RNF43 is involved in DDR in the stomach. DDR activation and cell viability upon γ-radiation was analyzed in gastric cells where expression of RNF43 was depleted. Response to chemotherapeutic agents 5-fluorouracil and cisplatin was analyzed in gastric cancer cell lines and xenograft tumors. In addition, involvement of RNF43 in DDR activation was analyzed upon Helicobacter pylori infection in wild-type and Rnf43 RNF43 depletion conferred resistance to γ-radiation and chemotherapy by dampening the activation of DDR, thereby preventing apoptosis in gastric cells. Upon Helicobacter pylori infection, RNF43 loss of function reduced activation of DDR and apoptosis. Furthermore, RNF43 expression correlated with DDR activation in human gastric biopsy specimens, and RNF43 mutations found in gastric tumors conferred resistance to DNA damage. When exploring the molecular mechanisms behind these findings, a direct interaction between RNF43 and phosphorylated H2A histone family member X (γH2AX) was observed. We identified a novel function for RNF43 in the stomach as a regulator of DDR. Loss of RNF43 function in gastric cells confers resistance to DNA damage-inducing radiotherapy and chemotherapy, suggesting RNF43 as a possible biomarker for therapy selection.

Sections du résumé

BACKGROUND & AIMS
RING finger protein 43 (RNF43) is a tumor suppressor that frequently is mutated in gastric tumors. The link between RNF43 and modulation of Wingless-related integration site (WNT) signaling has not been shown clearly in the stomach. Because mutations in RNF43 are highly enriched in microsatellite-unstable gastric tumors, which show defects in DNA damage response (DDR), we investigated whether RNF43 is involved in DDR in the stomach.
METHODS
DDR activation and cell viability upon γ-radiation was analyzed in gastric cells where expression of RNF43 was depleted. Response to chemotherapeutic agents 5-fluorouracil and cisplatin was analyzed in gastric cancer cell lines and xenograft tumors. In addition, involvement of RNF43 in DDR activation was analyzed upon Helicobacter pylori infection in wild-type and Rnf43
RESULTS
RNF43 depletion conferred resistance to γ-radiation and chemotherapy by dampening the activation of DDR, thereby preventing apoptosis in gastric cells. Upon Helicobacter pylori infection, RNF43 loss of function reduced activation of DDR and apoptosis. Furthermore, RNF43 expression correlated with DDR activation in human gastric biopsy specimens, and RNF43 mutations found in gastric tumors conferred resistance to DNA damage. When exploring the molecular mechanisms behind these findings, a direct interaction between RNF43 and phosphorylated H2A histone family member X (γH2AX) was observed.
CONCLUSIONS
We identified a novel function for RNF43 in the stomach as a regulator of DDR. Loss of RNF43 function in gastric cells confers resistance to DNA damage-inducing radiotherapy and chemotherapy, suggesting RNF43 as a possible biomarker for therapy selection.

Identifiants

pubmed: 33188943
pii: S2352-345X(20)30184-3
doi: 10.1016/j.jcmgh.2020.11.005
pmc: PMC7898035
pii:
doi:

Substances chimiques

RNF43 protein, human EC 2.3.2.27
RNF43 protein, mouse EC 2.3.2.27
Ubiquitin-Protein Ligases EC 2.3.2.27

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1071-1094

Commentaires et corrections

Type : CommentIn

Informations de copyright

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

Auteurs

Victoria Neumeyer (V)

Institute for Medical Microbiology, Immunology and Hygiene, School of Medicine, Technical University of Munich, Munich, Germany.

Anna Brutau-Abia (A)

Institute for Medical Microbiology, Immunology and Hygiene, School of Medicine, Technical University of Munich, Munich, Germany.

Michael Allgäuer (M)

Institute for Medical Microbiology, Immunology and Hygiene, School of Medicine, Technical University of Munich, Munich, Germany.

Nicole Pfarr (N)

Institute of Pathology, Technical University of Munich, Munich, Germany.

Wilko Weichert (W)

Institute of Pathology, Technical University of Munich, Munich, Germany.

Christina Falkeis-Veits (C)

Institute of Pathology, Klinikum Bayreuth, Bayreuth, Germany.

Elisabeth Kremmer (E)

Institute for Molecular Immunology, Helmholtz Zentrum Munich, German Research Center for Environmental Health (GmbH), Monoclonal Antibody Core Facility, Munich, Germany.

Michael Vieth (M)

Institute of Pathology, Klinikum Bayreuth, Bayreuth, Germany.

Markus Gerhard (M)

Institute for Medical Microbiology, Immunology and Hygiene, School of Medicine, Technical University of Munich, Munich, Germany.

Raquel Mejías-Luque (R)

Institute for Medical Microbiology, Immunology and Hygiene, School of Medicine, Technical University of Munich, Munich, Germany. Electronic address: raquel.mejias-luque@tum.de.

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Classifications MeSH