Nrf2 Mutation/Activation Is Dispensable for the Development of Chemically Induced Mouse HCC.


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:
2022
Historique:
received: 18 06 2021
revised: 11 08 2021
accepted: 12 08 2021
pubmed: 17 9 2021
medline: 5 4 2022
entrez: 16 9 2021
Statut: ppublish

Résumé

Activation of the kelch-like ECH-associated protein 1 (Keap1)-nuclear factor (erythroid-derived 2)-like 2 (Nrf2) pathway has been associated with metabolic reprogramming in many tumors, including hepatocellular carcinoma (HCC). However, the contribution of Nrf2 mutations in this process remains elusive. Here, we investigated the occurrence of Nrf2 mutations in distinct models of mouse hepatocarcinogenesis. HCCs were generated by experimental protocols consisting of the following: (1) a single dose of diethylnitrosamine (DEN), followed by repeated treatments with the nuclear-receptor agonist 1,4-bis-[2-(3,5-dichloropyridyloxy)]benzene; (2) repeated treatments with 1,4-bis-[2-(3,5-dichloropyridyloxy)]benzene alone; (3) a single dose of DEN followed by exposure to a choline-deficient L-amino acid-defined diet; and (4) a single dose of DEN with no further treatment. All of these protocols led to HCC development within 28-42 weeks. Activation of the Keap1-Nrf2 pathway was investigated by analyzing the presence of Nrf2 gene mutations, and the expression of Nrf2 target genes. Metabolic reprogramming was assessed by evaluating the expression of genes involved in glycolysis, the pentose phosphate pathway, and glutaminolysis. No Nrf2 mutations were found in any of the models of hepatocarcinogenesis analyzed. Intriguingly, despite the described cooperation between β-catenin and the Nrf2 pathway, we found no evidence of Nrf2 activation in both early dysplastic nodules and HCCs, characterized by the presence of up to 80%-90% β-catenin mutations. No HCC metabolic reprogramming was observed either. These results show that, unlike rat hepatocarcinogenesis, Nrf2 mutations do not occur in 4 distinct models of chemically induced mouse HCC. Interestingly, in the same models, metabolic reprogramming also was minimal or absent, supporting the concept that Nrf2 activation is critical for the switch from oxidative to glycolytic metabolism.

Sections du résumé

BACKGROUND & AIMS
Activation of the kelch-like ECH-associated protein 1 (Keap1)-nuclear factor (erythroid-derived 2)-like 2 (Nrf2) pathway has been associated with metabolic reprogramming in many tumors, including hepatocellular carcinoma (HCC). However, the contribution of Nrf2 mutations in this process remains elusive. Here, we investigated the occurrence of Nrf2 mutations in distinct models of mouse hepatocarcinogenesis.
METHODS
HCCs were generated by experimental protocols consisting of the following: (1) a single dose of diethylnitrosamine (DEN), followed by repeated treatments with the nuclear-receptor agonist 1,4-bis-[2-(3,5-dichloropyridyloxy)]benzene; (2) repeated treatments with 1,4-bis-[2-(3,5-dichloropyridyloxy)]benzene alone; (3) a single dose of DEN followed by exposure to a choline-deficient L-amino acid-defined diet; and (4) a single dose of DEN with no further treatment. All of these protocols led to HCC development within 28-42 weeks. Activation of the Keap1-Nrf2 pathway was investigated by analyzing the presence of Nrf2 gene mutations, and the expression of Nrf2 target genes. Metabolic reprogramming was assessed by evaluating the expression of genes involved in glycolysis, the pentose phosphate pathway, and glutaminolysis.
RESULTS
No Nrf2 mutations were found in any of the models of hepatocarcinogenesis analyzed. Intriguingly, despite the described cooperation between β-catenin and the Nrf2 pathway, we found no evidence of Nrf2 activation in both early dysplastic nodules and HCCs, characterized by the presence of up to 80%-90% β-catenin mutations. No HCC metabolic reprogramming was observed either.
CONCLUSIONS
These results show that, unlike rat hepatocarcinogenesis, Nrf2 mutations do not occur in 4 distinct models of chemically induced mouse HCC. Interestingly, in the same models, metabolic reprogramming also was minimal or absent, supporting the concept that Nrf2 activation is critical for the switch from oxidative to glycolytic metabolism.

Identifiants

pubmed: 34530178
pii: S2352-345X(21)00178-8
doi: 10.1016/j.jcmgh.2021.08.011
pmc: PMC8593617
pii:
doi:

Substances chimiques

Kelch-Like ECH-Associated Protein 1 0
NF-E2-Related Factor 2 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

113-127

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Sandra Mattu (S)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy.

Patrizia Zavattari (P)

Department of Biomedical Sciences, Unit of Biology and Genetics, University of Cagliari, Cagliari, Italy.

Marta Anna Kowalik (MA)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy.

Marina Serra (M)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy.

Pia Sulas (P)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy.

Rajesh Pal (R)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy.

Elisabetta Puliga (E)

Department of Oncology, Candiolo, Italy; Candiolo Cancer Institute, Fondazione Piemonte per l'Oncologia -Istituto di Ricovero e Cura a Carattere Scientifico, Candiolo, Torino, Italy.

Salvatore Sutti (S)

Department of Health Sciences, University of Piemonte Orientale, Novara, Italy.

Beatrice Foglia (B)

Department of Clinical and Biological Sciences, Unit of Experimental and Clinical Pathology, University of Torino, Candiolo, Italy.

Maurizio Parola (M)

Department of Clinical and Biological Sciences, Unit of Experimental and Clinical Pathology, University of Torino, Candiolo, Italy.

Emanuele Albano (E)

Department of Health Sciences, University of Piemonte Orientale, Novara, Italy.

Silvia Giordano (S)

Department of Oncology, Candiolo, Italy; Candiolo Cancer Institute, Fondazione Piemonte per l'Oncologia -Istituto di Ricovero e Cura a Carattere Scientifico, Candiolo, Torino, Italy.

Andrea Perra (A)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy. Electronic address: andrea.perra@unica.it.

Amedeo Columbano (A)

Department of Biomedical Sciences, Unit of Oncology and Molecular Pathology, Cagliari, Italy. Electronic address: columbano@unica.it.

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