Tumor Exosomal RNAs Promote Lung Pre-metastatic Niche Formation by Activating Alveolar Epithelial TLR3 to Recruit Neutrophils

The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic niche formation and organ-specific metastatic tropism is not clearly defined. Here, we demonstrate that lung epithelial cells are critical for i...

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Published in	Cancer cell Vol. 30; no. 2; pp. 243 - 256
Main Authors	Liu, Yanfang, Gu, Yan, Han, Yanmei, Zhang, Qian, Jiang, Zhengping, Zhang, Xiang, Huang, Bo, Xu, Xiaoqing, Zheng, Jianming, Cao, Xuetao
Format	Journal Article
Language	English
Published	United States Elsevier Inc 08.08.2016
Subjects	alveolar epithelial cell Animals Base Sequence Carcinoma, Lewis Lung - genetics Carcinoma, Lewis Lung - metabolism Carcinoma, Lewis Lung - pathology Epithelial Cells - pathology exosomal RNA Exosomes Humans Lung Neoplasms - genetics Lung Neoplasms - metabolism Lung Neoplasms - pathology Lung Neoplasms - secondary Melanoma, Experimental - genetics Melanoma, Experimental - metabolism Melanoma, Experimental - pathology metastasis Mice Mice, Inbred C57BL Mice, Transgenic Neoplasm Metastasis Neutrophil Infiltration - genetics pre-metastatic niche RNA, Neoplasm - genetics RNA, Neoplasm - metabolism RNA, Small Nuclear - genetics RNA, Small Nuclear - metabolism TLR3 Toll-Like Receptor 3 - deficiency Toll-Like Receptor 3 - genetics Toll-Like Receptor 3 - metabolism pre-metastatic niche exosomal RNA metastasis TLR3 alveolar epithelial cell
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Abstract	The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic niche formation and organ-specific metastatic tropism is not clearly defined. Here, we demonstrate that lung epithelial cells are critical for initiating neutrophil recruitment and lung metastatic niche formation by sensing tumor exosomal RNAs via Toll-like receptor 3 (TLR3). TLR3-deficient mice show reduced lung metastasis in the spontaneous metastatic models. Mechanistically, primary tumor-derived exosomal RNAs, which are enriched in small nuclear RNAs, activate TLR3 in lung epithelial cells, consequently inducing chemokine secretion in the lung and promoting neutrophil recruitment. Identification of metastatic axis of tumor exosomal RNAs and host lung epithelial cell TLR3 activation provides potential targets to control cancer metastasis to the lung. [Display omitted] •TLR3 deficiency reduces lung metastasis in the spontaneous cancer metastatic models•Host TLR3 promotes lung pre-metastatic niche formation via neutrophil recruitment•Tumor exosomal RNAs activate alveolar epithelial TLR3 to induce chemokines•High TLR3 level and neutrophil infiltration in lung cancer predict poor prognosis Liu et al. demonstrate that TLR3 in host alveolar epithelial cells is critical for neutrophil recruitment and lung pre-metastatic niche formation. Mechanistically, small nuclear RNAs from primary tumor-derived exosomes activate TLR3, which leads to chemokine secretion and neutrophil infiltration.
AbstractList	The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic niche formation and organ-specific metastatic tropism is not clearly defined. Here, we demonstrate that lung epithelial cells are critical for initiating neutrophil recruitment and lung metastatic niche formation by sensing tumor exosomal RNAs via Toll-like receptor 3 (TLR3). TLR3-deficient mice show reduced lung metastasis in the spontaneous metastatic models. Mechanistically, primary tumor-derived exosomal RNAs, which are enriched in small nuclear RNAs, activate TLR3 in lung epithelial cells, consequently inducing chemokine secretion in the lung and promoting neutrophil recruitment. Identification of metastatic axis of tumor exosomal RNAs and host lung epithelial cell TLR3 activation provides potential targets to control cancer metastasis to the lung. The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic niche formation and organ-specific metastatic tropism is not clearly defined. Here, we demonstrate that lung epithelial cells are critical for initiating neutrophil recruitment and lung metastatic niche formation by sensing tumor exosomal RNAs via Toll-like receptor 3 (TLR3). TLR3-deficient mice show reduced lung metastasis in the spontaneous metastatic models. Mechanistically, primary tumor-derived exosomal RNAs, which are enriched in small nuclear RNAs, activate TLR3 in lung epithelial cells, consequently inducing chemokine secretion in the lung and promoting neutrophil recruitment. Identification of metastatic axis of tumor exosomal RNAs and host lung epithelial cell TLR3 activation provides potential targets to control cancer metastasis to the lung. [Display omitted] •TLR3 deficiency reduces lung metastasis in the spontaneous cancer metastatic models•Host TLR3 promotes lung pre-metastatic niche formation via neutrophil recruitment•Tumor exosomal RNAs activate alveolar epithelial TLR3 to induce chemokines•High TLR3 level and neutrophil infiltration in lung cancer predict poor prognosis Liu et al. demonstrate that TLR3 in host alveolar epithelial cells is critical for neutrophil recruitment and lung pre-metastatic niche formation. Mechanistically, small nuclear RNAs from primary tumor-derived exosomes activate TLR3, which leads to chemokine secretion and neutrophil infiltration. The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic niche formation and organ-specific metastatic tropism is not clearly defined. Here, we demonstrate that lung epithelial cells are critical for initiating neutrophil recruitment and lung metastatic niche formation by sensing tumor exosomal RNAs via Toll-like receptor 3 (TLR3). TLR3-deficient mice show reduced lung metastasis in the spontaneous metastatic models. Mechanistically, primary tumor-derived exosomal RNAs, which are enriched in small nuclear RNAs, activate TLR3 in lung epithelial cells, consequently inducing chemokine secretion in the lung and promoting neutrophil recruitment. Identification of metastatic axis of tumor exosomal RNAs and host lung epithelial cell TLR3 activation provides potential targets to control cancer metastasis to the lung.
Author	Xu, Xiaoqing Huang, Bo Zheng, Jianming Han, Yanmei Gu, Yan Zhang, Qian Jiang, Zhengping Liu, Yanfang Zhang, Xiang Cao, Xuetao
Author_xml	– sequence: 1 givenname: Yanfang surname: Liu fullname: Liu, Yanfang organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 2 givenname: Yan surname: Gu fullname: Gu, Yan organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 3 givenname: Yanmei surname: Han fullname: Han, Yanmei organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 4 givenname: Qian surname: Zhang fullname: Zhang, Qian organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 5 givenname: Zhengping surname: Jiang fullname: Jiang, Zhengping organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 6 givenname: Xiang surname: Zhang fullname: Zhang, Xiang organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China – sequence: 7 givenname: Bo surname: Huang fullname: Huang, Bo organization: National Key Laboratory of Medical Molecular Biology, Department of Immunology, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing 100005, China – sequence: 8 givenname: Xiaoqing surname: Xu fullname: Xu, Xiaoqing organization: National Key Laboratory of Medical Molecular Biology, Department of Immunology, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing 100005, China – sequence: 9 givenname: Jianming surname: Zheng fullname: Zheng, Jianming organization: Department of Pathology, Changhai Hospital, Second Military Medical University, Shanghai 200433, China – sequence: 10 givenname: Xuetao surname: Cao fullname: Cao, Xuetao email: caoxt@immunol.org organization: National Key Laboratory of Medical Immunology, Institute of Immunology, Second Military Medical University, 800 Xiangyin Road, Shanghai 200433, China
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/27505671$$D View this record in MEDLINE/PubMed
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Snippet	The pre-metastatic niche educated by primary tumor-derived elements contributes to cancer metastasis. However, the role of host stromal cells in metastatic...
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SubjectTerms	alveolar epithelial cell Animals Base Sequence Carcinoma, Lewis Lung - genetics Carcinoma, Lewis Lung - metabolism Carcinoma, Lewis Lung - pathology Epithelial Cells - pathology exosomal RNA Exosomes Humans Lung Neoplasms - genetics Lung Neoplasms - metabolism Lung Neoplasms - pathology Lung Neoplasms - secondary Melanoma, Experimental - genetics Melanoma, Experimental - metabolism Melanoma, Experimental - pathology metastasis Mice Mice, Inbred C57BL Mice, Transgenic Neoplasm Metastasis Neutrophil Infiltration - genetics pre-metastatic niche RNA, Neoplasm - genetics RNA, Neoplasm - metabolism RNA, Small Nuclear - genetics RNA, Small Nuclear - metabolism TLR3 Toll-Like Receptor 3 - deficiency Toll-Like Receptor 3 - genetics Toll-Like Receptor 3 - metabolism
Title	Tumor Exosomal RNAs Promote Lung Pre-metastatic Niche Formation by Activating Alveolar Epithelial TLR3 to Recruit Neutrophils
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