Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB
Growing evidence links tumor progression with chronic inflammatory processes and dysregulated activity of various immune cells. In this study, we demonstrate that various types of macrophages internalize microvesicles, called exosomes, secreted by breast cancer and non-cancerous cell lines. Although...
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Published in | Scientific reports Vol. 4; no. 1; p. 5750 |
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Main Authors | , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
Nature Publishing Group
18.07.2014
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Abstract | Growing evidence links tumor progression with chronic inflammatory processes and dysregulated activity of various immune cells. In this study, we demonstrate that various types of macrophages internalize microvesicles, called exosomes, secreted by breast cancer and non-cancerous cell lines. Although both types of exosomes targeted macrophages, only cancer-derived exosomes stimulated NF-κB activation in macrophages resulting in secretion of pro-inflammatory cytokines such as IL-6, TNFα, GCSF, and CCL2. In vivo mouse experiments confirmed that intravenously injected exosomes are efficiently internalized by macrophages in the lung and brain, which correlated with upregulation of inflammatory cytokines. In mice bearing xenografted human breast cancers, tumor-derived exosomes were internalized by macrophages in axillary lymph nodes thereby triggering expression of IL-6. Genetic ablation of Toll-like receptor 2 (TLR2) or MyD88, a critical signaling adaptor in the NF-κB pathway, completely abolished the effect of tumor-derived exosomes. In contrast, inhibition of TLR4 or endosomal TLRs (TLR3/7/8/9) failed to abrogate NF-κB activation by exosomes. We further found that palmitoylated proteins present on the surface of tumor-secreted exosomes contributed to NF-κB activation. Thus, our results highlight a novel mechanism used by breast cancer cells to induce pro-inflammatory activity of distant macrophages through circulating exosomal vesicles secreted during cancer progression. |
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AbstractList | Growing evidence links tumor progression with chronic inflammatory processes and dysregulated activity of various immune cells. In this study, we demonstrate that various types of macrophages internalize microvesicles, called exosomes, secreted by breast cancer and non-cancerous cell lines. Although both types of exosomes targeted macrophages, only cancer-derived exosomes stimulated NF-κB activation in macrophages resulting in secretion of pro-inflammatory cytokines such as IL-6, TNFα, GCSF, and CCL2. In vivo mouse experiments confirmed that intravenously injected exosomes are efficiently internalized by macrophages in the lung and brain, which correlated with upregulation of inflammatory cytokines. In mice bearing xenografted human breast cancers, tumor-derived exosomes were internalized by macrophages in axillary lymph nodes thereby triggering expression of IL-6. Genetic ablation of Toll-like receptor 2 (TLR2) or MyD88, a critical signaling adaptor in the NF-κB pathway, completely abolished the effect of tumor-derived exosomes. In contrast, inhibition of TLR4 or endosomal TLRs (TLR3/7/8/9) failed to abrogate NF-κB activation by exosomes. We further found that palmitoylated proteins present on the surface of tumor-secreted exosomes contributed to NF-κB activation. Thus, our results highlight a novel mechanism used by breast cancer cells to induce pro-inflammatory activity of distant macrophages through circulating exosomal vesicles secreted during cancer progression. Growing evidence links tumor progression with chronic inflammatory processes and dysregulated activity of various immune cells. In this study, we demonstrate that various types of macrophages internalize microvesicles, called exosomes, secreted by breast cancer and non-cancerous cell lines. Although both types of exosomes targeted macrophages, only cancer-derived exosomes stimulated NF-κB activation in macrophages resulting in secretion of pro-inflammatory cytokines such as IL-6, TNFα, GCSF, and CCL2. In vivo mouse experiments confirmed that intravenously injected exosomes are efficiently internalized by macrophages in the lung and brain, which correlated with upregulation of inflammatory cytokines. In mice bearing xenografted human breast cancers, tumor-derived exosomes were internalized by macrophages in axillary lymph nodes thereby triggering expression of IL-6. Genetic ablation of Toll-like receptor 2 (TLR2) or MyD88, a critical signaling adaptor in the NF-κB pathway, completely abolished the effect of tumor-derived exosomes. In contrast, inhibition of TLR4 or endosomal TLRs (TLR3/7/8/9) failed to abrogate NF-κB activation by exosomes. We further found that palmitoylated proteins present on the surface of tumor-secreted exosomes contributed to NF-κB activation. Thus, our results highlight a novel mechanism used by breast cancer cells to induce pro-inflammatory activity of distant macrophages through circulating exosomal vesicles secreted during cancer progression. |
ArticleNumber | 5750 |
Author | Huang, Wendong Fong, Miranda Y Kortylewski, Marcin Liu, Liang Gugiu, Bogdan Gabriel Wang, Shizhen Emily Zhou, Weiying Van Haute, Desiree Chow, Amy Ngo, Vu Chin, Andrew R Meng, Zhipeng Ren, Xiubao Champer, Jackson |
Author_xml | – sequence: 1 givenname: Amy surname: Chow fullname: Chow, Amy organization: Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 2 givenname: Weiying surname: Zhou fullname: Zhou, Weiying organization: 1] Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A Department of Pharmacology, College of Pharmacy, The Third Military Medical University, Chongqing, 400038, China – sequence: 3 givenname: Liang surname: Liu fullname: Liu, Liang organization: 1] Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A Department of Biotherapy and Key Laboratory of Cancer Immunology, Tianjin Medical University Cancer Institute and Hospital, Tianjin, 300060, China – sequence: 4 givenname: Miranda Y surname: Fong fullname: Fong, Miranda Y organization: Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 5 givenname: Jackson surname: Champer fullname: Champer, Jackson organization: 1] Department of Immunology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A City of Hope Irell & Manella Graduate School of Biological Sciences, Duarte, California, 91010, U.S.A – sequence: 6 givenname: Desiree surname: Van Haute fullname: Van Haute, Desiree organization: 1] Departments of Molecular Medicine, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A City of Hope Irell & Manella Graduate School of Biological Sciences, Duarte, California, 91010, U.S.A – sequence: 7 givenname: Andrew R surname: Chin fullname: Chin, Andrew R organization: 1] Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A City of Hope Irell & Manella Graduate School of Biological Sciences, Duarte, California, 91010, U.S.A – sequence: 8 givenname: Xiubao surname: Ren fullname: Ren, Xiubao organization: Department of Biotherapy and Key Laboratory of Cancer Immunology, Tianjin Medical University Cancer Institute and Hospital, Tianjin, 300060, China – sequence: 9 givenname: Bogdan Gabriel surname: Gugiu fullname: Gugiu, Bogdan Gabriel organization: 1] Department of Immunology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A The Mass Spectrometry and Proteomics Core; City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 10 givenname: Zhipeng surname: Meng fullname: Meng, Zhipeng organization: Department of Molecular Diabetes Research, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 11 givenname: Wendong surname: Huang fullname: Huang, Wendong organization: Department of Molecular Diabetes Research, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 12 givenname: Vu surname: Ngo fullname: Ngo, Vu organization: Department of Stem Cell & Leukemia Research, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 13 givenname: Marcin surname: Kortylewski fullname: Kortylewski, Marcin organization: Department of Cancer Immunotherapeutics & Tumor Immunology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A – sequence: 14 givenname: Shizhen Emily surname: Wang fullname: Wang, Shizhen Emily organization: Department of Cancer Biology, City of Hope Beckman Research Institute, Duarte, California, 91010, U.S.A |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25034888$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals Breast Neoplasms - immunology Breast Neoplasms - metabolism Cell Communication Cytokines - metabolism Cytokines - secretion Exosomes - physiology Female Humans Immunomodulation Macrophages - immunology Macrophages - metabolism Macrophages - secretion MCF-7 Cells Mice, Inbred NOD Mice, Nude Mice, SCID Neoplasm Transplantation NF-kappa B - metabolism Signal Transduction Toll-Like Receptor 2 - metabolism |
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Title | Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB |
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