Hypoxic glioma-derived exosomes deliver microRNA-1246 to induce M2 macrophage polarization by targeting TERF2IP via the STAT3 and NF-κB pathways

Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by which tumor exosomes facilitate the generation of the immunosuppressive microenvironment remain unclear. Here we investigated the effects of...

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Veröffentlicht in:	Oncogene Jg. 39; H. 2; S. 428 - 442
Hauptverfasser:	Qian, Mingyu, Wang, Shaobo, Guo, Xiaofan, Wang, Jian, Zhang, Zongpu, Qiu, Wei, Gao, Xiao, Chen, Zihang, Xu, Jianye, Zhao, Rongrong, Xue, Hao, Li, Gang
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England Nature Publishing Group 01.01.2020
Schlagworte:	Cell Line, Tumor Cell signaling Exosomes Exosomes - metabolism Glioma Glioma - pathology Humans Hypoxia Immunotherapy Intracellular signalling Investigations Leukocyte migration Macrophages Macrophages - cytology Macrophages - immunology MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA NF-kappa B - metabolism NF-κB protein Phagocytosis - genetics Polarization Sequence analysis Shelterin Complex Signal Transduction Stat3 protein STAT3 Transcription Factor - metabolism Telomere-Binding Proteins - genetics Tumor Hypoxia
ISSN:	0950-9232, 1476-5594, 1476-5594
Online-Zugang:	Volltext
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Abstract	Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by which tumor exosomes facilitate the generation of the immunosuppressive microenvironment remain unclear. Here we investigated the effects of glioma-derived exosomes (GDEs) on macrophage polarization and glioma progression. We also performed microRNA sequencing analysis of GDEs to identify the microRNA that mediated macrophage polarization. The microRNA-associated intracellular signaling pathway in macrophages was further investigated. Compared with normoxic glioma-derived exosomes (N-GDEs), hypoxic glioma-derived exosomes (H-GDEs) markedly induced M2 macrophage polarization, which subsequently promoted glioma proliferation, migration and invasion in vitro and in vivo. MicroRNA sequencing analysis identified miR-1246 as the most enriched microRNA in H-GDEs. Moreover, miR-1246 was enriched in the CSF of GBM patients and decreased after tumor resection. Further investigation determined that miR-1246 mediated H-GDE-induced M2 macrophage polarization by targeting TERF2IP to activate the STAT3 signaling pathway and inhibit the NF-κB signaling pathway. Our study elucidated a mechanism by which hypoxia and glioma influence M2 macrophage polarization via exosomes, which could facilitate the formation of the immunosuppressive microenvironment. Moreover, our results suggested that miR-1246 in the CSF of GBM patients may be a novel biomarker for GBM diagnosis and that treatment targeting microRNA-1246 may contribute to antitumor immunotherapy.
AbstractList	Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by which tumor exosomes facilitate the generation of the immunosuppressive microenvironment remain unclear. Here we investigated the effects of glioma-derived exosomes (GDEs) on macrophage polarization and glioma progression. We also performed microRNA sequencing analysis of GDEs to identify the microRNA that mediated macrophage polarization. The microRNA-associated intracellular signaling pathway in macrophages was further investigated. Compared with normoxic glioma-derived exosomes (N-GDEs), hypoxic glioma-derived exosomes (H-GDEs) markedly induced M2 macrophage polarization, which subsequently promoted glioma proliferation, migration and invasion in vitro and in vivo. MicroRNA sequencing analysis identified miR-1246 as the most enriched microRNA in H-GDEs. Moreover, miR-1246 was enriched in the CSF of GBM patients and decreased after tumor resection. Further investigation determined that miR-1246 mediated H-GDE-induced M2 macrophage polarization by targeting TERF2IP to activate the STAT3 signaling pathway and inhibit the NF-κB signaling pathway. Our study elucidated a mechanism by which hypoxia and glioma influence M2 macrophage polarization via exosomes, which could facilitate the formation of the immunosuppressive microenvironment. Moreover, our results suggested that miR-1246 in the CSF of GBM patients may be a novel biomarker for GBM diagnosis and that treatment targeting microRNA-1246 may contribute to antitumor immunotherapy. Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by which tumor exosomes facilitate the generation of the immunosuppressive microenvironment remain unclear. Here we investigated the effects of glioma-derived exosomes (GDEs) on macrophage polarization and glioma progression. We also performed microRNA sequencing analysis of GDEs to identify the microRNA that mediated macrophage polarization. The microRNA-associated intracellular signaling pathway in macrophages was further investigated. Compared with normoxic glioma-derived exosomes (N-GDEs), hypoxic glioma-derived exosomes (H-GDEs) markedly induced M2 macrophage polarization, which subsequently promoted glioma proliferation, migration and invasion in vitro and in vivo. MicroRNA sequencing analysis identified miR-1246 as the most enriched microRNA in H-GDEs. Moreover, miR-1246 was enriched in the CSF of GBM patients and decreased after tumor resection. Further investigation determined that miR-1246 mediated H-GDE-induced M2 macrophage polarization by targeting TERF2IP to activate the STAT3 signaling pathway and inhibit the NF-κB signaling pathway. Our study elucidated a mechanism by which hypoxia and glioma influence M2 macrophage polarization via exosomes, which could facilitate the formation of the immunosuppressive microenvironment. Moreover, our results suggested that miR-1246 in the CSF of GBM patients may be a novel biomarker for GBM diagnosis and that treatment targeting microRNA-1246 may contribute to antitumor immunotherapy.Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by which tumor exosomes facilitate the generation of the immunosuppressive microenvironment remain unclear. Here we investigated the effects of glioma-derived exosomes (GDEs) on macrophage polarization and glioma progression. We also performed microRNA sequencing analysis of GDEs to identify the microRNA that mediated macrophage polarization. The microRNA-associated intracellular signaling pathway in macrophages was further investigated. Compared with normoxic glioma-derived exosomes (N-GDEs), hypoxic glioma-derived exosomes (H-GDEs) markedly induced M2 macrophage polarization, which subsequently promoted glioma proliferation, migration and invasion in vitro and in vivo. MicroRNA sequencing analysis identified miR-1246 as the most enriched microRNA in H-GDEs. Moreover, miR-1246 was enriched in the CSF of GBM patients and decreased after tumor resection. Further investigation determined that miR-1246 mediated H-GDE-induced M2 macrophage polarization by targeting TERF2IP to activate the STAT3 signaling pathway and inhibit the NF-κB signaling pathway. Our study elucidated a mechanism by which hypoxia and glioma influence M2 macrophage polarization via exosomes, which could facilitate the formation of the immunosuppressive microenvironment. Moreover, our results suggested that miR-1246 in the CSF of GBM patients may be a novel biomarker for GBM diagnosis and that treatment targeting microRNA-1246 may contribute to antitumor immunotherapy.
Author	Wang, Jian Qian, Mingyu Wang, Shaobo Xu, Jianye Li, Gang Guo, Xiaofan Zhao, Rongrong Zhang, Zongpu Qiu, Wei Gao, Xiao Chen, Zihang Xue, Hao
Author_xml	– sequence: 1 givenname: Mingyu surname: Qian fullname: Qian, Mingyu organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 2 givenname: Shaobo orcidid: 0000-0001-7759-1687 surname: Wang fullname: Wang, Shaobo organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 3 givenname: Xiaofan surname: Guo fullname: Guo, Xiaofan organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 4 givenname: Jian orcidid: 0000-0002-9482-5227 surname: Wang fullname: Wang, Jian organization: Brain Tumor Research Centre, Department of Biomedicine, University of Bergen, Bergen, Norway – sequence: 5 givenname: Zongpu surname: Zhang fullname: Zhang, Zongpu organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 6 givenname: Wei surname: Qiu fullname: Qiu, Wei organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 7 givenname: Xiao surname: Gao fullname: Gao, Xiao organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 8 givenname: Zihang surname: Chen fullname: Chen, Zihang organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 9 givenname: Jianye orcidid: 0000-0001-7241-6994 surname: Xu fullname: Xu, Jianye organization: Shandong Key Laboratory of Brain Function Remodeling, Jinan, Shandong, China – sequence: 10 givenname: Rongrong surname: Zhao fullname: Zhao, Rongrong organization: Department of Neurosurgery, Qilu Hospital of Shandong University, Jinan, Shandong, China – sequence: 11 givenname: Hao surname: Xue fullname: Xue, Hao email: xuehao@sdu.edu.cn, xuehao@sdu.edu.cn, xuehao@sdu.edu.cn organization: Department of Neurosurgery, Qilu Hospital of Shandong University, Jinan, Shandong, China. xuehao@sdu.edu.cn – sequence: 12 givenname: Gang surname: Li fullname: Li, Gang email: ligangqiluhospital@163.com, ligangqiluhospital@163.com, ligangqiluhospital@163.com organization: Department of Neurosurgery, Qilu Hospital of Shandong University, Jinan, Shandong, China. ligangqiluhospital@163.com
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31485019$$D View this record in MEDLINE/PubMed
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Snippet	Exosomes are emerging as important elements that participate in intercellular communication and tumor microenvironment modulation, but the exact mechanisms by...
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SubjectTerms	Cell Line, Tumor Cell signaling Exosomes Exosomes - metabolism Glioma Glioma - pathology Humans Hypoxia Immunotherapy Intracellular signalling Investigations Leukocyte migration Macrophages Macrophages - cytology Macrophages - immunology MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA NF-kappa B - metabolism NF-κB protein Phagocytosis - genetics Polarization Sequence analysis Shelterin Complex Signal Transduction Stat3 protein STAT3 Transcription Factor - metabolism Telomere-Binding Proteins - genetics Tumor Hypoxia
Title	Hypoxic glioma-derived exosomes deliver microRNA-1246 to induce M2 macrophage polarization by targeting TERF2IP via the STAT3 and NF-κB pathways
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