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The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer

Metabolic reprogramming is a malignant phenotype of cancer. Cancer cells utilize glycolysis to fuel rapid proliferation even in the presence of oxygen, and elevated glycolysis is coupled to lactate fermentation in the cancer microenvironment. Although lactate has been recognized as a metabolic waste...

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Autores principales: Ishihara, Shota, Hata, Kenji, Hirose, Katsutoshi, Okui, Tatsuo, Toyosawa, Satoru, Uzawa, Narikazu, Nishimura, Riko, Yoneda, Toshiyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9012857/
https://www.ncbi.nlm.nih.gov/pubmed/35428832
http://dx.doi.org/10.1038/s41598-022-10143-w
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author Ishihara, Shota
Hata, Kenji
Hirose, Katsutoshi
Okui, Tatsuo
Toyosawa, Satoru
Uzawa, Narikazu
Nishimura, Riko
Yoneda, Toshiyuki
author_facet Ishihara, Shota
Hata, Kenji
Hirose, Katsutoshi
Okui, Tatsuo
Toyosawa, Satoru
Uzawa, Narikazu
Nishimura, Riko
Yoneda, Toshiyuki
author_sort Ishihara, Shota
collection PubMed
description Metabolic reprogramming is a malignant phenotype of cancer. Cancer cells utilize glycolysis to fuel rapid proliferation even in the presence of oxygen, and elevated glycolysis is coupled to lactate fermentation in the cancer microenvironment. Although lactate has been recognized as a metabolic waste product, it has become evident that lactate functions as not only an energy source but a signaling molecule through the lactate receptor G-protein-coupled receptor 81 (GPR81) under physiological conditions. However, the pathological role of GPR81 in cancer remains unclear. Here, we show that GPR81 regulates the malignant phenotype of breast cancer cell by reprogramming energy metabolism. We found that GPR81 is highly expressed in breast cancer cell lines but not in normal breast epithelial cells. Knockdown of GPR81 decreased breast cancer cell proliferation, and tumor growth. Mechanistically, glycolysis and lactate-dependent ATP production were impaired in GPR81-silenced breast cancer cells. RNA sequencing accompanied by Gene Ontology enrichment analysis further demonstrated a significant decrease in genes associated with cell motility and silencing of GPR81 suppressed cell migration and invasion. Notably, histological examination showed strong expression of GPR81 in clinical samples of human breast cancer. Collectively, our findings suggest that GPR81 is critical for malignancy of breast cancer and may be a potential novel therapeutic target for breast carcinoma.
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spelling pubmed-90128572022-04-18 The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer Ishihara, Shota Hata, Kenji Hirose, Katsutoshi Okui, Tatsuo Toyosawa, Satoru Uzawa, Narikazu Nishimura, Riko Yoneda, Toshiyuki Sci Rep Article Metabolic reprogramming is a malignant phenotype of cancer. Cancer cells utilize glycolysis to fuel rapid proliferation even in the presence of oxygen, and elevated glycolysis is coupled to lactate fermentation in the cancer microenvironment. Although lactate has been recognized as a metabolic waste product, it has become evident that lactate functions as not only an energy source but a signaling molecule through the lactate receptor G-protein-coupled receptor 81 (GPR81) under physiological conditions. However, the pathological role of GPR81 in cancer remains unclear. Here, we show that GPR81 regulates the malignant phenotype of breast cancer cell by reprogramming energy metabolism. We found that GPR81 is highly expressed in breast cancer cell lines but not in normal breast epithelial cells. Knockdown of GPR81 decreased breast cancer cell proliferation, and tumor growth. Mechanistically, glycolysis and lactate-dependent ATP production were impaired in GPR81-silenced breast cancer cells. RNA sequencing accompanied by Gene Ontology enrichment analysis further demonstrated a significant decrease in genes associated with cell motility and silencing of GPR81 suppressed cell migration and invasion. Notably, histological examination showed strong expression of GPR81 in clinical samples of human breast cancer. Collectively, our findings suggest that GPR81 is critical for malignancy of breast cancer and may be a potential novel therapeutic target for breast carcinoma. Nature Publishing Group UK 2022-04-15 /pmc/articles/PMC9012857/ /pubmed/35428832 http://dx.doi.org/10.1038/s41598-022-10143-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ishihara, Shota
Hata, Kenji
Hirose, Katsutoshi
Okui, Tatsuo
Toyosawa, Satoru
Uzawa, Narikazu
Nishimura, Riko
Yoneda, Toshiyuki
The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title_full The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title_fullStr The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title_full_unstemmed The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title_short The lactate sensor GPR81 regulates glycolysis and tumor growth of breast cancer
title_sort lactate sensor gpr81 regulates glycolysis and tumor growth of breast cancer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9012857/
https://www.ncbi.nlm.nih.gov/pubmed/35428832
http://dx.doi.org/10.1038/s41598-022-10143-w
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