Cancer-Derived Succinate Promotes Macrophage Polarization and Cancer Metastasis via Succinate Receptor
Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the tumor-derived soluble molecules to promote tumor progression and metastasis. Here, we used comparative metabolomics coupled with biochemical and...
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| Vydané v: | Molecular cell Ročník 77; číslo 2; s. 213 |
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| Hlavní autori: | , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
16.01.2020
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| Predmet: | |
| ISSN: | 1097-4164, 1097-4164 |
| On-line prístup: | Zistit podrobnosti o prístupe |
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| Abstract | Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the tumor-derived soluble molecules to promote tumor progression and metastasis. Here, we used comparative metabolomics coupled with biochemical and animal studies to show that cancer cells release succinate into their microenvironment and activate succinate receptor (SUCNR1) signaling to polarize macrophages into TAM. Furthermore, the results from in vitro and in vivo studies revealed that succinate promotes not only cancer cell migration and invasion but also cancer metastasis. These effects are mediated by SUCNR1-triggered PI3K-hypoxia-inducible factor 1α (HIF-1α) axis. Compared with healthy subjects and tumor-free lung tissues, serum succinate levels and lung cancer SUCNR1 expression were elevated in lung cancer patients, suggesting an important clinical relevance. Collectively, our findings indicate that the secreted tumor-derived succinate belongs to a novel class of cancer progression factors, controlling TAM polarization and promoting tumorigenic signaling. |
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| AbstractList | Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the tumor-derived soluble molecules to promote tumor progression and metastasis. Here, we used comparative metabolomics coupled with biochemical and animal studies to show that cancer cells release succinate into their microenvironment and activate succinate receptor (SUCNR1) signaling to polarize macrophages into TAM. Furthermore, the results from in vitro and in vivo studies revealed that succinate promotes not only cancer cell migration and invasion but also cancer metastasis. These effects are mediated by SUCNR1-triggered PI3K-hypoxia-inducible factor 1α (HIF-1α) axis. Compared with healthy subjects and tumor-free lung tissues, serum succinate levels and lung cancer SUCNR1 expression were elevated in lung cancer patients, suggesting an important clinical relevance. Collectively, our findings indicate that the secreted tumor-derived succinate belongs to a novel class of cancer progression factors, controlling TAM polarization and promoting tumorigenic signaling. Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the tumor-derived soluble molecules to promote tumor progression and metastasis. Here, we used comparative metabolomics coupled with biochemical and animal studies to show that cancer cells release succinate into their microenvironment and activate succinate receptor (SUCNR1) signaling to polarize macrophages into TAM. Furthermore, the results from in vitro and in vivo studies revealed that succinate promotes not only cancer cell migration and invasion but also cancer metastasis. These effects are mediated by SUCNR1-triggered PI3K-hypoxia-inducible factor 1α (HIF-1α) axis. Compared with healthy subjects and tumor-free lung tissues, serum succinate levels and lung cancer SUCNR1 expression were elevated in lung cancer patients, suggesting an important clinical relevance. Collectively, our findings indicate that the secreted tumor-derived succinate belongs to a novel class of cancer progression factors, controlling TAM polarization and promoting tumorigenic signaling.Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the tumor-derived soluble molecules to promote tumor progression and metastasis. Here, we used comparative metabolomics coupled with biochemical and animal studies to show that cancer cells release succinate into their microenvironment and activate succinate receptor (SUCNR1) signaling to polarize macrophages into TAM. Furthermore, the results from in vitro and in vivo studies revealed that succinate promotes not only cancer cell migration and invasion but also cancer metastasis. These effects are mediated by SUCNR1-triggered PI3K-hypoxia-inducible factor 1α (HIF-1α) axis. Compared with healthy subjects and tumor-free lung tissues, serum succinate levels and lung cancer SUCNR1 expression were elevated in lung cancer patients, suggesting an important clinical relevance. Collectively, our findings indicate that the secreted tumor-derived succinate belongs to a novel class of cancer progression factors, controlling TAM polarization and promoting tumorigenic signaling. |
| Author | Kung, Hsing-Jien Wang, Yi-Fu Lee, Guan-Lin Wu, Kenneth K Huang, Tsai-Wang Hsiao, Cheng-Wen Kuo, Cheng-Chin Lin, Hui-Chen Yen, Chia-Chien Wen, Hsiu-Ting Kuo, Ya-Yi Yeh, Chang-Ching Peng, Yi-Jen Hsu, Yu-Juei Hsieh, Yi-Ting Wu, Jing-Yiing |
| Author_xml | – sequence: 1 givenname: Jing-Yiing surname: Wu fullname: Wu, Jing-Yiing organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 2 givenname: Tsai-Wang surname: Huang fullname: Huang, Tsai-Wang organization: Division of Thoracic Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan – sequence: 3 givenname: Yi-Ting surname: Hsieh fullname: Hsieh, Yi-Ting organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 4 givenname: Yi-Fu surname: Wang fullname: Wang, Yi-Fu organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 5 givenname: Chia-Chien surname: Yen fullname: Yen, Chia-Chien organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 6 givenname: Guan-Lin surname: Lee fullname: Lee, Guan-Lin organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 7 givenname: Chang-Ching surname: Yeh fullname: Yeh, Chang-Ching organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan; Graduate Institutes of Life Sciences and Biochemistry, National Defense Medical Center, Taipei, Taiwan – sequence: 8 givenname: Yi-Jen surname: Peng fullname: Peng, Yi-Jen organization: Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan – sequence: 9 givenname: Ya-Yi surname: Kuo fullname: Kuo, Ya-Yi organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 10 givenname: Hsiu-Ting surname: Wen fullname: Wen, Hsiu-Ting organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 11 givenname: Hui-Chen surname: Lin fullname: Lin, Hui-Chen organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 12 givenname: Cheng-Wen surname: Hsiao fullname: Hsiao, Cheng-Wen organization: Division of Colorectal Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan – sequence: 13 givenname: Kenneth K surname: Wu fullname: Wu, Kenneth K organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan; Metabolomic Research Center, China Medical University Hospital, China Medical University, Taichung, Taiwan; Graduate Institute of Basic Medical Science, China Medical University, Taichung, Taiwan – sequence: 14 givenname: Hsing-Jien surname: Kung fullname: Kung, Hsing-Jien organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes, Zhunan, Taiwan – sequence: 15 givenname: Yu-Juei surname: Hsu fullname: Hsu, Yu-Juei organization: Division of Nephrology, Department of Medicine, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan – sequence: 16 givenname: Cheng-Chin surname: Kuo fullname: Kuo, Cheng-Chin email: kuocc@nhri.org.tw organization: Institute of Cellular and System Medicine, National Health Research Institutes, Zhunan, Taiwan; Graduate Institute of Basic Medical Science, China Medical University, Taichung, Taiwan; Graduate Institutes of Life Sciences and Biochemistry, National Defense Medical Center, Taipei, Taiwan. Electronic address: kuocc@nhri.org.tw |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31735641$$D View this record in MEDLINE/PubMed |
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| Keywords | succinate SUCNR1 metabolomics PI3K-HIF-1α axis tumor microenvironment cancer metastasis tumor-associated macrophages |
| Language | English |
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| Snippet | Macrophages form a major cell population in the tumor microenvironment. They can be activated and polarized into tumor-associated macrophages (TAM) by the... |
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| SubjectTerms | A549 Cells Animals Cell Line, Tumor Cell Movement - physiology HT29 Cells Humans Hypoxia-Inducible Factor 1, alpha Subunit - metabolism Lung Neoplasms - metabolism Lung Neoplasms - pathology Macrophages - metabolism Macrophages - pathology MCF-7 Cells Mice, Inbred C57BL Neoplasm Metastasis - pathology PC-3 Cells Receptors, G-Protein-Coupled - metabolism Signal Transduction - physiology Succinic Acid - metabolism Tumor Microenvironment - physiology |
| Title | Cancer-Derived Succinate Promotes Macrophage Polarization and Cancer Metastasis via Succinate Receptor |
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