Sublethal irradiation promotes the metastatic potential of hepatocellular carcinoma cells
Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the funct...
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| Vydané v: | Cancer science Ročník 112; číslo 1; s. 265 - 274 |
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| Hlavní autori: | , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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England
John Wiley & Sons, Inc
01.01.2021
John Wiley and Sons Inc |
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| ISSN: | 1347-9032, 1349-7006, 1349-7006 |
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| Abstract | Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA‐RH7777 hepatoma cells were irradiated with 6 Gy X‐ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib‐treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA‐RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA‐RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA‐RH7777 cells were enriched mostly in the AMP‐activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK‐621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase‐8 (MMP‐8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP‐8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation–induced HCC metastasis at the level of the tumor microenvironment.
In this work, we observed that conditioned media from sublethally irradiated liver nonparenchymal cells (NPCs) promoted the migration and invasion ability of sublethally irradiated McA‐RH7777 hepatoma cells. Further mechanistic studies revealed that matrix metalloproteinase‐8 (MMP‐8) secreted by NPCs enhanced the migration and invasion of hepatocellular carcinoma (HCC) by regulating the AMPK/mTOR signaling pathway. These findings might offer a new strategy for improving the therapeutic effect of radiotherapy. |
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| AbstractList | Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA‐RH7777 hepatoma cells were irradiated with 6 Gy X‐ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib‐treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA‐RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA‐RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA‐RH7777 cells were enriched mostly in the AMP‐activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK‐621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase‐8 (MMP‐8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP‐8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation–induced HCC metastasis at the level of the tumor microenvironment.
In this work, we observed that conditioned media from sublethally irradiated liver nonparenchymal cells (NPCs) promoted the migration and invasion ability of sublethally irradiated McA‐RH7777 hepatoma cells. Further mechanistic studies revealed that matrix metalloproteinase‐8 (MMP‐8) secreted by NPCs enhanced the migration and invasion of hepatocellular carcinoma (HCC) by regulating the AMPK/mTOR signaling pathway. These findings might offer a new strategy for improving the therapeutic effect of radiotherapy. Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA‐RH7777 hepatoma cells were irradiated with 6 Gy X‐ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib‐treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA‐RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA‐RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA‐RH7777 cells were enriched mostly in the AMP‐activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK‐621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase‐8 (MMP‐8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP‐8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation–induced HCC metastasis at the level of the tumor microenvironment. Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA‐RH7777 hepatoma cells were irradiated with 6 Gy X‐ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib‐treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA‐RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA‐RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA‐RH7777 cells were enriched mostly in the AMP‐activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK‐621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase‐8 (MMP‐8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP‐8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation–induced HCC metastasis at the level of the tumor microenvironment. In this work, we observed that conditioned media from sublethally irradiated liver nonparenchymal cells (NPCs) promoted the migration and invasion ability of sublethally irradiated McA‐RH7777 hepatoma cells. Further mechanistic studies revealed that matrix metalloproteinase‐8 (MMP‐8) secreted by NPCs enhanced the migration and invasion of hepatocellular carcinoma (HCC) by regulating the AMPK/mTOR signaling pathway. These findings might offer a new strategy for improving the therapeutic effect of radiotherapy. Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA-RH7777 hepatoma cells were irradiated with 6 Gy X-ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib-treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA-RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA-RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA-RH7777 cells were enriched mostly in the AMP-activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK-621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase-8 (MMP-8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP-8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation-induced HCC metastasis at the level of the tumor microenvironment. Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA-RH7777 hepatoma cells were irradiated with 6 Gy X-ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib-treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA-RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA-RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA-RH7777 cells were enriched mostly in the AMP-activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK-621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase-8 (MMP-8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP-8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation-induced HCC metastasis at the level of the tumor microenvironment.Radiotherapy (RT) represents one of the major treatment methods for cancers. However, many studies have observed that in descendant surviving tumor cells, sublethal irradiation can promote metastatic ability, which is closely related to the tumor microenvironment. We therefore investigated the functions and mechanisms of sublethal irradiated liver nonparenchymal cells (NPCs) in hepatocellular carcinoma (HCC). In this study, primary rat NPCs and McA-RH7777 hepatoma cells were irradiated with 6 Gy X-ray. Conditioned media (CM) from nonirradiated (SnonR), irradiated (SR), or irradiated plus radiosensitizer celecoxib-treated (S[R + D]) NPCs were collected and added to sublethal irradiated McA-RH7777 cells. We showed that CM from sublethal irradiated NPCs significantly promoted the migration and invasion ability of sublethal irradiated McA-RH7777 cells, which was reversed by celecoxib. The differentially expressed genes in differently treated McA-RH7777 cells were enriched mostly in the AMP-activated protein kinase/mammalian target of rapamycin (AMPK/mTOR) signaling pathway. SR increased the migration and invasion ability of HCC cells by inhibiting AMPK/mTOR signaling, which was enhanced by the AMPK inhibitor compound C and blocked by the AMPK activator GSK-621. Analyses of HCC tissues after neoadjuvant radiotherapy confirmed the effects of radiation on the AMPK/mTOR pathway. Cytokine antibody arrays and further functional investigations showed that matrix metalloproteinase-8 (MMP-8) partly mediates the promotion effects of SR on the migration and invasion ability of HCC cells by regulating AMPK/mTOR signaling. In summary, our data indicate that MMP-8 secreted by irradiated NPCs enhanced the migration and invasion of HCC by regulating AMPK/mTOR signaling, revealing a novel mechanism mediating sublethal irradiation-induced HCC metastasis at the level of the tumor microenvironment. |
| Author | Wang, Xue Zhang, Fuzheng Cao, Yulin Wu, Zhifeng Lin, Junhua Zhou, Leyuan Liu, Yuhang Yin, Yuan Huang, Zhaohui |
| AuthorAffiliation | 1 Department of Radiation Oncology Affiliated Hospital of Jiangnan University Wuxi China 2 Wuxi Cancer Institute Affiliated Hospital of Jiangnan University Wuxi China 3 Laboratory of Cancer Epigenetics Wuxi School of Medicine Jiangnan University Wuxi China 4 Experimental Research Center Zhongshan Hospital Fudan University Shanghai China |
| AuthorAffiliation_xml | – name: 2 Wuxi Cancer Institute Affiliated Hospital of Jiangnan University Wuxi China – name: 4 Experimental Research Center Zhongshan Hospital Fudan University Shanghai China – name: 1 Department of Radiation Oncology Affiliated Hospital of Jiangnan University Wuxi China – name: 3 Laboratory of Cancer Epigenetics Wuxi School of Medicine Jiangnan University Wuxi China |
| Author_xml | – sequence: 1 givenname: Yulin surname: Cao fullname: Cao, Yulin organization: Jiangnan University – sequence: 2 givenname: Yuan surname: Yin fullname: Yin, Yuan organization: Jiangnan University – sequence: 3 givenname: Xue surname: Wang fullname: Wang, Xue organization: Jiangnan University – sequence: 4 givenname: Zhifeng surname: Wu fullname: Wu, Zhifeng organization: Fudan University – sequence: 5 givenname: Yuhang surname: Liu fullname: Liu, Yuhang organization: Jiangnan University – sequence: 6 givenname: Fuzheng surname: Zhang fullname: Zhang, Fuzheng organization: Affiliated Hospital of Jiangnan University – sequence: 7 givenname: Junhua surname: Lin fullname: Lin, Junhua organization: Affiliated Hospital of Jiangnan University – sequence: 8 givenname: Zhaohui orcidid: 0000-0002-0117-9976 surname: Huang fullname: Huang, Zhaohui email: zhaohuihuang@jiangnan.edu.cn organization: Jiangnan University – sequence: 9 givenname: Leyuan surname: Zhou fullname: Zhou, Leyuan email: zhouleyuan99@126.com organization: Jiangnan University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33155388$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_yacr_2022_04_009 crossref_primary_10_1080_09553002_2021_1956005 crossref_primary_10_3390_cancers13071598 crossref_primary_10_1016_j_phymed_2022_154151 crossref_primary_10_3390_molecules28020525 crossref_primary_10_1080_15384101_2022_2131163 crossref_primary_10_3892_ijo_2025_5787 crossref_primary_10_1016_j_canrad_2024_07_002 crossref_primary_10_3389_fimmu_2023_1150416 |
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| Copyright | 2020 The Authors. published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association. 2020 The Authors. Cancer Science published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association. 2021. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| Keywords | cytokine radiotherapy hepatocellular carcinoma cells metastasis sublethal irradiation |
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| License | Attribution-NonCommercial 2020 The Authors. Cancer Science published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. |
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