Cytoskeleton-centric protein transportation by exosomes transforms tumor-favorable macrophages
The exosome is a key initiator of pre-metastatic niche in numerous cancers, where macrophages serve as primary inducers of tumor microenvironment. However, the proteome that can be exosomally transported from cancer cells to macrophages has not been sufficiently characterized so far. Here, we used c...
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creator | Chen, Zhipeng Yang, Lijuan Cui, Yizhi Zhou, Yanlong Yin, Xingfeng Guo, Jiahui Zhang, Gong Wang, Tong He, Qing-Yu |
description | The exosome is a key initiator of pre-metastatic niche in numerous cancers, where macrophages serve as primary inducers of tumor microenvironment. However, the proteome that can be exosomally transported from cancer cells to macrophages has not been sufficiently characterized so far. Here, we used colorectal cancer (CRC) exosomes to educate tumor-favorable macrophages. With a SILAC-based mass spectrometry strategy, we successfully traced the proteome transported from CRC exosomes to macrophages. Such a proteome primarily focused on promoting cytoskeleton rearrangement, which was biologically validated with multiple cell lines. We reproduced the exosomal transportation of functional vimentin as a proof-of-concept example. In addition, we found that some CRC exosomes could be recognized by macrophages via Fc receptors. Therefore, we revealed the active and necessary role of exosomes secreted from CRC cells to transform cancer-favorable macrophages, with the cytoskeleton-centric proteins serving as the top functional unit. |
doi_str_mv | 10.18632/oncotarget.11794 |
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However, the proteome that can be exosomally transported from cancer cells to macrophages has not been sufficiently characterized so far. Here, we used colorectal cancer (CRC) exosomes to educate tumor-favorable macrophages. With a SILAC-based mass spectrometry strategy, we successfully traced the proteome transported from CRC exosomes to macrophages. Such a proteome primarily focused on promoting cytoskeleton rearrangement, which was biologically validated with multiple cell lines. We reproduced the exosomal transportation of functional vimentin as a proof-of-concept example. In addition, we found that some CRC exosomes could be recognized by macrophages via Fc receptors. Therefore, we revealed the active and necessary role of exosomes secreted from CRC cells to transform cancer-favorable macrophages, with the cytoskeleton-centric proteins serving as the top functional unit.</description><identifier>ISSN: 1949-2553</identifier><identifier>EISSN: 1949-2553</identifier><identifier>DOI: 10.18632/oncotarget.11794</identifier><identifier>PMID: 27602764</identifier><language>eng</language><publisher>United States: Impact Journals LLC</publisher><subject>Animals ; Cell Line, Tumor ; Colorectal Neoplasms - metabolism ; Colorectal Neoplasms - pathology ; Cytoskeleton - metabolism ; Cytoskeleton - pathology ; Exosomes - metabolism ; Exosomes - pathology ; Heterografts ; Humans ; Macrophages - metabolism ; Macrophages - pathology ; Mice ; Mice, Inbred BALB C ; Protein Transport ; Research Paper ; Tumor Microenvironment - physiology</subject><ispartof>Oncotarget, 2016-10, Vol.7 (41), p.67387-67402</ispartof><rights>Copyright: © 2016 Chen et al. 2016</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c492t-a5043f23e7cd9bb887de42dfae65197c6bdbdc9240d0f75f8c01d87db7da3e5e3</citedby><cites>FETCH-LOGICAL-c492t-a5043f23e7cd9bb887de42dfae65197c6bdbdc9240d0f75f8c01d87db7da3e5e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5341883/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5341883/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27602764$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Zhipeng</creatorcontrib><creatorcontrib>Yang, Lijuan</creatorcontrib><creatorcontrib>Cui, Yizhi</creatorcontrib><creatorcontrib>Zhou, Yanlong</creatorcontrib><creatorcontrib>Yin, Xingfeng</creatorcontrib><creatorcontrib>Guo, Jiahui</creatorcontrib><creatorcontrib>Zhang, Gong</creatorcontrib><creatorcontrib>Wang, Tong</creatorcontrib><creatorcontrib>He, Qing-Yu</creatorcontrib><title>Cytoskeleton-centric protein transportation by exosomes transforms tumor-favorable macrophages</title><title>Oncotarget</title><addtitle>Oncotarget</addtitle><description>The exosome is a key initiator of pre-metastatic niche in numerous cancers, where macrophages serve as primary inducers of tumor microenvironment. 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Therefore, we revealed the active and necessary role of exosomes secreted from CRC cells to transform cancer-favorable macrophages, with the cytoskeleton-centric proteins serving as the top functional unit.</description><subject>Animals</subject><subject>Cell Line, Tumor</subject><subject>Colorectal Neoplasms - metabolism</subject><subject>Colorectal Neoplasms - pathology</subject><subject>Cytoskeleton - metabolism</subject><subject>Cytoskeleton - pathology</subject><subject>Exosomes - metabolism</subject><subject>Exosomes - pathology</subject><subject>Heterografts</subject><subject>Humans</subject><subject>Macrophages - metabolism</subject><subject>Macrophages - pathology</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Protein Transport</subject><subject>Research Paper</subject><subject>Tumor Microenvironment - physiology</subject><issn>1949-2553</issn><issn>1949-2553</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUUtLxDAQDqKoqD_Ai_TopWvz6Da5CLL4AsGLXg1pMt2ttp2aZMX994bd9TUwzMB8883jI-SUFhMqp5xd4GAxGj-HOKG0UmKHHFIlVM7Kku_-yQ_ISQivRbJSVJKpfXLAqmmRXBySl9kqYniDDiIOuYUh-tZmo8cI7ZBFb4Ywoo8mtjhk9SqDTwzYQ9iUGvR9Spc9-rwxH-hN3UHWG-txXJg5hGOy15guwMk2HpHnm-un2V3-8Hh7P7t6yK1QLOamLARvGIfKOlXXUlYOBHONgWlJVWWntaudVUwUrmiqspG2oC6B6soZDiXwI3K54R2XdQ9ufYfp9Ojb3viVRtPq_5WhXeg5fuiSCyolTwTnWwKP70sIUfdtsNB1ZgBcBk1l-iRTUokEpRtoujIED83PGFrotTT6Vxq9lib1nP3d76fjWwj-Ba0kkns</recordid><startdate>20161011</startdate><enddate>20161011</enddate><creator>Chen, Zhipeng</creator><creator>Yang, Lijuan</creator><creator>Cui, Yizhi</creator><creator>Zhou, Yanlong</creator><creator>Yin, Xingfeng</creator><creator>Guo, Jiahui</creator><creator>Zhang, Gong</creator><creator>Wang, Tong</creator><creator>He, Qing-Yu</creator><general>Impact Journals LLC</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20161011</creationdate><title>Cytoskeleton-centric protein transportation by exosomes transforms tumor-favorable macrophages</title><author>Chen, Zhipeng ; Yang, Lijuan ; Cui, Yizhi ; Zhou, Yanlong ; Yin, Xingfeng ; Guo, Jiahui ; Zhang, Gong ; Wang, Tong ; He, Qing-Yu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c492t-a5043f23e7cd9bb887de42dfae65197c6bdbdc9240d0f75f8c01d87db7da3e5e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Cell Line, Tumor</topic><topic>Colorectal Neoplasms - metabolism</topic><topic>Colorectal Neoplasms - pathology</topic><topic>Cytoskeleton - metabolism</topic><topic>Cytoskeleton - pathology</topic><topic>Exosomes - metabolism</topic><topic>Exosomes - pathology</topic><topic>Heterografts</topic><topic>Humans</topic><topic>Macrophages - metabolism</topic><topic>Macrophages - pathology</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Protein Transport</topic><topic>Research Paper</topic><topic>Tumor Microenvironment - physiology</topic><toplevel>online_resources</toplevel><creatorcontrib>Chen, Zhipeng</creatorcontrib><creatorcontrib>Yang, Lijuan</creatorcontrib><creatorcontrib>Cui, Yizhi</creatorcontrib><creatorcontrib>Zhou, Yanlong</creatorcontrib><creatorcontrib>Yin, Xingfeng</creatorcontrib><creatorcontrib>Guo, Jiahui</creatorcontrib><creatorcontrib>Zhang, Gong</creatorcontrib><creatorcontrib>Wang, Tong</creatorcontrib><creatorcontrib>He, Qing-Yu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Oncotarget</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Zhipeng</au><au>Yang, Lijuan</au><au>Cui, Yizhi</au><au>Zhou, Yanlong</au><au>Yin, Xingfeng</au><au>Guo, Jiahui</au><au>Zhang, Gong</au><au>Wang, Tong</au><au>He, Qing-Yu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cytoskeleton-centric protein transportation by exosomes transforms tumor-favorable macrophages</atitle><jtitle>Oncotarget</jtitle><addtitle>Oncotarget</addtitle><date>2016-10-11</date><risdate>2016</risdate><volume>7</volume><issue>41</issue><spage>67387</spage><epage>67402</epage><pages>67387-67402</pages><issn>1949-2553</issn><eissn>1949-2553</eissn><abstract>The exosome is a key initiator of pre-metastatic niche in numerous cancers, where macrophages serve as primary inducers of tumor microenvironment. However, the proteome that can be exosomally transported from cancer cells to macrophages has not been sufficiently characterized so far. Here, we used colorectal cancer (CRC) exosomes to educate tumor-favorable macrophages. With a SILAC-based mass spectrometry strategy, we successfully traced the proteome transported from CRC exosomes to macrophages. Such a proteome primarily focused on promoting cytoskeleton rearrangement, which was biologically validated with multiple cell lines. We reproduced the exosomal transportation of functional vimentin as a proof-of-concept example. In addition, we found that some CRC exosomes could be recognized by macrophages via Fc receptors. 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subjects | Animals Cell Line, Tumor Colorectal Neoplasms - metabolism Colorectal Neoplasms - pathology Cytoskeleton - metabolism Cytoskeleton - pathology Exosomes - metabolism Exosomes - pathology Heterografts Humans Macrophages - metabolism Macrophages - pathology Mice Mice, Inbred BALB C Protein Transport Research Paper Tumor Microenvironment - physiology |
title | Cytoskeleton-centric protein transportation by exosomes transforms tumor-favorable macrophages |
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