Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer

We aimed to understand the role of G protein‐coupled receptor 4 (GPR4) in tumorigenesis. GPR4 is a pH‐sensing receptor that is activated by acidic extracellular pH. GPR4 is expressed primarily in vascular endothelial cells (ECs). Intestinal tissue from patients with inflammatory bowel disease (IBD)...

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Main Authors: Leonie Perren, Moana Busch, Pedro A. Ruiz, Ermanno Malagola, Valeria Baumeler, Federica Foti, Adelina Gross, Tobias Grütter, Hendrik Edel, Cordelia Schuler, Kristina Handler, Glenn De Lange, Isabelle C. Arnold, Cheryl deVallière, Klaus Seuwen, Martin Hausmann, Gerhard Rogler
Format: Article
Language:English
Published: Wiley 2025-08-01
Series:Molecular Oncology
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Online Access:https://doi.org/10.1002/1878-0261.70045
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author Leonie Perren
Moana Busch
Pedro A. Ruiz
Ermanno Malagola
Valeria Baumeler
Federica Foti
Adelina Gross
Tobias Grütter
Hendrik Edel
Cordelia Schuler
Kristina Handler
Glenn De Lange
Isabelle C. Arnold
Cheryl deVallière
Klaus Seuwen
Martin Hausmann
Gerhard Rogler
author_facet Leonie Perren
Moana Busch
Pedro A. Ruiz
Ermanno Malagola
Valeria Baumeler
Federica Foti
Adelina Gross
Tobias Grütter
Hendrik Edel
Cordelia Schuler
Kristina Handler
Glenn De Lange
Isabelle C. Arnold
Cheryl deVallière
Klaus Seuwen
Martin Hausmann
Gerhard Rogler
author_sort Leonie Perren
collection DOAJ
description We aimed to understand the role of G protein‐coupled receptor 4 (GPR4) in tumorigenesis. GPR4 is a pH‐sensing receptor that is activated by acidic extracellular pH. GPR4 is expressed primarily in vascular endothelial cells (ECs). Intestinal tissue from patients with inflammatory bowel disease (IBD) shows increased expression of GPR4. Patients with IBD have a significantly increased risk of developing colorectal cancer (CRC). In the MC38 model, Gpr4‐deficient mice showed significantly reduced tumor size and weight compared to wild‐type (WT) mice. This effect correlated with a significant increase in IL2 protein and natural killer (NK)1.1+ cells in tumor tissue in Gpr4−/− compared to WT. In the azoxymethane (AOM)/dextran sodium sulfate (DSS) model of CRC, Gpr4‐deficient mice showed significantly reduced tumor progression and number of apurinic/apyrimidinic (AP) sites. Gpr4‐deficient mice showed a significantly increased number of NKp46+ cells in tumor tissue, and increased numbers of NK cells were confirmed by qPCR and flow cytometry. The absence of GPR4 significantly attenuated tumor progression in the colon of mice, and this result correlated with increased cytotoxic cell activity and reduced presence of tumor‐associated macrophages and neutrophils. GPR4 represents a potential new target for therapeutic intervention.
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spelling doaj-art-6aec37da8a644500af2139d8a34346af2025-08-20T03:39:45ZengWileyMolecular Oncology1574-78911878-02612025-08-011982196221110.1002/1878-0261.70045Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancerLeonie Perren0Moana Busch1Pedro A. Ruiz2Ermanno Malagola3Valeria Baumeler4Federica Foti5Adelina Gross6Tobias Grütter7Hendrik Edel8Cordelia Schuler9Kristina Handler10Glenn De Lange11Isabelle C. Arnold12Cheryl deVallière13Klaus Seuwen14Martin Hausmann15Gerhard Rogler16Department of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandInstitute of Experimental Immunology University of Zurich Zurich SwitzerlandInstitute of Experimental Immunology University of Zurich Zurich SwitzerlandInstitute of Experimental Immunology University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandDepartment of Gastroenterology and Hepatology University Hospital of Zurich, University of Zurich Zurich SwitzerlandWe aimed to understand the role of G protein‐coupled receptor 4 (GPR4) in tumorigenesis. GPR4 is a pH‐sensing receptor that is activated by acidic extracellular pH. GPR4 is expressed primarily in vascular endothelial cells (ECs). Intestinal tissue from patients with inflammatory bowel disease (IBD) shows increased expression of GPR4. Patients with IBD have a significantly increased risk of developing colorectal cancer (CRC). In the MC38 model, Gpr4‐deficient mice showed significantly reduced tumor size and weight compared to wild‐type (WT) mice. This effect correlated with a significant increase in IL2 protein and natural killer (NK)1.1+ cells in tumor tissue in Gpr4−/− compared to WT. In the azoxymethane (AOM)/dextran sodium sulfate (DSS) model of CRC, Gpr4‐deficient mice showed significantly reduced tumor progression and number of apurinic/apyrimidinic (AP) sites. Gpr4‐deficient mice showed a significantly increased number of NKp46+ cells in tumor tissue, and increased numbers of NK cells were confirmed by qPCR and flow cytometry. The absence of GPR4 significantly attenuated tumor progression in the colon of mice, and this result correlated with increased cytotoxic cell activity and reduced presence of tumor‐associated macrophages and neutrophils. GPR4 represents a potential new target for therapeutic intervention.https://doi.org/10.1002/1878-0261.70045colorectal cancerGPR4inflammatory bowel diseasepH‐sensing G protein‐coupled receptors
spellingShingle Leonie Perren
Moana Busch
Pedro A. Ruiz
Ermanno Malagola
Valeria Baumeler
Federica Foti
Adelina Gross
Tobias Grütter
Hendrik Edel
Cordelia Schuler
Kristina Handler
Glenn De Lange
Isabelle C. Arnold
Cheryl deVallière
Klaus Seuwen
Martin Hausmann
Gerhard Rogler
Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
Molecular Oncology
colorectal cancer
GPR4
inflammatory bowel disease
pH‐sensing G protein‐coupled receptors
title Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
title_full Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
title_fullStr Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
title_full_unstemmed Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
title_short Loss of proton‐sensing GPR4 reduces tumor progression in mouse models of colon cancer
title_sort loss of proton sensing gpr4 reduces tumor progression in mouse models of colon cancer
topic colorectal cancer
GPR4
inflammatory bowel disease
pH‐sensing G protein‐coupled receptors
url https://doi.org/10.1002/1878-0261.70045
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