Cancer cells copy migratory behavior and exchange signaling networks via extracellular vesicles
Recent data showed that cancer cells from different tumor subtypes with distinct metastatic potential influence each other's metastatic behavior by exchanging biomolecules through extracellular vesicles (EVs). However, it is debated how small amounts of cargo can mediate this effect, especially...
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| Veröffentlicht in: | The EMBO journal 2018-08, Vol.37 (15), p.n/a |
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| creator | Steenbeek, Sander C Pham, Thang V de Ligt, Joep Zomer, Anoek Knol, Jaco C Piersma, Sander R Schelfhorst, Tim Huisjes, Rick Schiffelers, Raymond M Cuppen, Edwin Jimenez, Connie R van Rheenen, Jacco |
| description | Recent data showed that cancer cells from different tumor subtypes with distinct metastatic potential influence each other's metastatic behavior by exchanging biomolecules through extracellular vesicles (EVs). However, it is debated how small amounts of cargo can mediate this effect, especially in tumors where all cells are from one subtype, and only subtle molecular differences drive metastatic heterogeneity. To study this, we have characterized the content of EVs shed
in vivo
by two clones of melanoma (B16) tumors with distinct metastatic potential. Using the Cre‐LoxP system and intravital microscopy, we show that cells from these distinct clones phenocopy their migratory behavior through EV exchange. By tandem mass spectrometry and RNA sequencing, we show that EVs shed by these clones into the tumor microenvironment contain thousands of different proteins and RNAs, and many of these biomolecules are from interconnected signaling networks involved in cellular processes such as migration. Thus, EVs contain numerous proteins and RNAs and act on recipient cells by invoking a multi‐faceted biological response including cell migration.
Synopsis
Imaging microscopy in live animals combined with transcriptome–proteome analyses are used to characterize the function and content of extracellular vesicles (EVs) shed
in vivo
by mouse melanoma tumors with distinct metastatic potential. These data suggest that EVs promote cell migration by transferring clusters of RNA and proteins acting in the same physiological signaling networks.
B16F1 and B16F10 melanoma cell clones with differential metastatic potencies functionally exchange EVs
in vivo
.
The less metastatic B16F1 cells display increased invasive potential after uptake of EVs from the more aggressive B16F10 cells.
EVs purified from B16F10 microenvironments contain more complex and distinct cargo networks of RNAs and proteins involved in cell migration than seen for B16F1.
Graphical Abstract
Melanoma cell subclones adopt increased migratory behavior
in vivo
by extracellular vesicle uptake, amplifying signaling nodes involved in cell motility. |
| doi_str_mv | 10.15252/embj.201798357 |
| format | Article |
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in vivo
by two clones of melanoma (B16) tumors with distinct metastatic potential. Using the Cre‐LoxP system and intravital microscopy, we show that cells from these distinct clones phenocopy their migratory behavior through EV exchange. By tandem mass spectrometry and RNA sequencing, we show that EVs shed by these clones into the tumor microenvironment contain thousands of different proteins and RNAs, and many of these biomolecules are from interconnected signaling networks involved in cellular processes such as migration. Thus, EVs contain numerous proteins and RNAs and act on recipient cells by invoking a multi‐faceted biological response including cell migration.
Synopsis
Imaging microscopy in live animals combined with transcriptome–proteome analyses are used to characterize the function and content of extracellular vesicles (EVs) shed
in vivo
by mouse melanoma tumors with distinct metastatic potential. These data suggest that EVs promote cell migration by transferring clusters of RNA and proteins acting in the same physiological signaling networks.
B16F1 and B16F10 melanoma cell clones with differential metastatic potencies functionally exchange EVs
in vivo
.
The less metastatic B16F1 cells display increased invasive potential after uptake of EVs from the more aggressive B16F10 cells.
EVs purified from B16F10 microenvironments contain more complex and distinct cargo networks of RNAs and proteins involved in cell migration than seen for B16F1.
Graphical Abstract
Melanoma cell subclones adopt increased migratory behavior
in vivo
by extracellular vesicle uptake, amplifying signaling nodes involved in cell motility.</description><identifier>ISSN: 0261-4189</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.15252/embj.201798357</identifier><identifier>PMID: 29907695</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Animals ; Biomolecules ; Cancer ; Cell adhesion & migration ; Cell Line, Tumor ; Cell migration ; Cell Movement - physiology ; Cellular communication ; Cre‐LoxP ; EMBO03 ; EMBO20 ; EMBO31 ; Exchanging ; Extracellular vesicles ; Extracellular Vesicles - metabolism ; Gene expression ; Gene sequencing ; Heterogeneity ; In vivo methods and tests ; intratumoral heterogeneity ; intravital microscopy ; Invasiveness ; Mass spectrometry ; Mass spectroscopy ; Melanoma ; Melanoma, Experimental - pathology ; Metastases ; Metastasis ; Mice ; Microenvironments ; Microscopy ; Neoplasm Metastasis - pathology ; Proteins ; Proteomes ; Ribonucleic acid ; RNA ; RNA, Messenger - genetics ; Signal Transduction - physiology ; Signaling ; signaling networks ; Tumor Microenvironment - physiology ; Tumors ; Vesicles</subject><ispartof>The EMBO journal, 2018-08, Vol.37 (15), p.n/a</ispartof><rights>The Author(s) 2018</rights><rights>2018 The Authors. Published under the terms of the CC BY 4.0 license</rights><rights>2018 The Authors. Published under the terms of the CC BY 4.0 license.</rights><rights>2018 EMBO</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5137-75adc0d3387eb09440221aa120c8d70bf2b95fe9689a6e2510c9d3c38ec9c68b3</citedby><cites>FETCH-LOGICAL-c5137-75adc0d3387eb09440221aa120c8d70bf2b95fe9689a6e2510c9d3c38ec9c68b3</cites><orcidid>0000-0002-0400-9542 ; 0000-0002-3103-4508 ; 0000-0001-8175-1647</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6068466/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6068466/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,1412,1428,27905,27906,41101,42170,45555,45556,46390,46814,51557,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29907695$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Steenbeek, Sander C</creatorcontrib><creatorcontrib>Pham, Thang V</creatorcontrib><creatorcontrib>de Ligt, Joep</creatorcontrib><creatorcontrib>Zomer, Anoek</creatorcontrib><creatorcontrib>Knol, Jaco C</creatorcontrib><creatorcontrib>Piersma, Sander R</creatorcontrib><creatorcontrib>Schelfhorst, Tim</creatorcontrib><creatorcontrib>Huisjes, Rick</creatorcontrib><creatorcontrib>Schiffelers, Raymond M</creatorcontrib><creatorcontrib>Cuppen, Edwin</creatorcontrib><creatorcontrib>Jimenez, Connie R</creatorcontrib><creatorcontrib>van Rheenen, Jacco</creatorcontrib><title>Cancer cells copy migratory behavior and exchange signaling networks via extracellular vesicles</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>Recent data showed that cancer cells from different tumor subtypes with distinct metastatic potential influence each other's metastatic behavior by exchanging biomolecules through extracellular vesicles (EVs). However, it is debated how small amounts of cargo can mediate this effect, especially in tumors where all cells are from one subtype, and only subtle molecular differences drive metastatic heterogeneity. To study this, we have characterized the content of EVs shed
in vivo
by two clones of melanoma (B16) tumors with distinct metastatic potential. Using the Cre‐LoxP system and intravital microscopy, we show that cells from these distinct clones phenocopy their migratory behavior through EV exchange. By tandem mass spectrometry and RNA sequencing, we show that EVs shed by these clones into the tumor microenvironment contain thousands of different proteins and RNAs, and many of these biomolecules are from interconnected signaling networks involved in cellular processes such as migration. Thus, EVs contain numerous proteins and RNAs and act on recipient cells by invoking a multi‐faceted biological response including cell migration.
Synopsis
Imaging microscopy in live animals combined with transcriptome–proteome analyses are used to characterize the function and content of extracellular vesicles (EVs) shed
in vivo
by mouse melanoma tumors with distinct metastatic potential. These data suggest that EVs promote cell migration by transferring clusters of RNA and proteins acting in the same physiological signaling networks.
B16F1 and B16F10 melanoma cell clones with differential metastatic potencies functionally exchange EVs
in vivo
.
The less metastatic B16F1 cells display increased invasive potential after uptake of EVs from the more aggressive B16F10 cells.
EVs purified from B16F10 microenvironments contain more complex and distinct cargo networks of RNAs and proteins involved in cell migration than seen for B16F1.
Graphical Abstract
Melanoma cell subclones adopt increased migratory behavior
in vivo
by extracellular vesicle uptake, amplifying signaling nodes involved in cell motility.</description><subject>Animals</subject><subject>Biomolecules</subject><subject>Cancer</subject><subject>Cell adhesion & migration</subject><subject>Cell Line, Tumor</subject><subject>Cell migration</subject><subject>Cell Movement - physiology</subject><subject>Cellular communication</subject><subject>Cre‐LoxP</subject><subject>EMBO03</subject><subject>EMBO20</subject><subject>EMBO31</subject><subject>Exchanging</subject><subject>Extracellular vesicles</subject><subject>Extracellular Vesicles - metabolism</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Heterogeneity</subject><subject>In vivo methods and tests</subject><subject>intratumoral heterogeneity</subject><subject>intravital microscopy</subject><subject>Invasiveness</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Melanoma</subject><subject>Melanoma, Experimental - pathology</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Microenvironments</subject><subject>Microscopy</subject><subject>Neoplasm Metastasis - pathology</subject><subject>Proteins</subject><subject>Proteomes</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Messenger - genetics</subject><subject>Signal Transduction - physiology</subject><subject>Signaling</subject><subject>signaling networks</subject><subject>Tumor Microenvironment - physiology</subject><subject>Tumors</subject><subject>Vesicles</subject><issn>0261-4189</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqFkU1vEzEQhi0EoqFw5oYsceGy7di79tockErU8qEiLnC2vN7JxmF3HexsSv59HVJCQUKcfJhnHr3jl5DnDM6Y4IKf49CszjiwWqtS1A_IjFUSCg61eEhmwCUrKqb0CXmS0goAhKrZY3LCtYZaajEjZm5Hh5E67PtEXVjv6OC7aDch7miDS7v1IVI7thR_uKUdO6TJd6Pt_djRETc3IX5LdOttnm-i3Wum3ka6xeRdj-kpebSwfcJnd-8p-Xp1-WX-vrj-_O7D_OK6cIKVdVEL2zpoy1LV2ICuKuCcWcs4ONXW0Cx4o8UCtVTaSuSCgdNt6UqFTjupmvKUvDl411MzYOtwzGl6s45-sHFngvXmz8nol6YLWyNBqkrKLHh1J4jh-4RpYwaf9ufYEcOUDAchS12qSmf05V_oKkwx_8meUpnL6SFT5wfKxZBSxMUxDAPzszyzL88cy8sbL-7fcOR_tZWB1wfgxve4-5_PXH56-_G-HQ7LKe_lHuPv1P8KdAv3nLiB</recordid><startdate>20180801</startdate><enddate>20180801</enddate><creator>Steenbeek, Sander C</creator><creator>Pham, Thang V</creator><creator>de Ligt, Joep</creator><creator>Zomer, Anoek</creator><creator>Knol, Jaco C</creator><creator>Piersma, Sander R</creator><creator>Schelfhorst, Tim</creator><creator>Huisjes, Rick</creator><creator>Schiffelers, Raymond M</creator><creator>Cuppen, Edwin</creator><creator>Jimenez, Connie R</creator><creator>van Rheenen, Jacco</creator><general>Nature Publishing Group UK</general><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>C6C</scope><scope>24P</scope><scope>WIN</scope><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0400-9542</orcidid><orcidid>https://orcid.org/0000-0002-3103-4508</orcidid><orcidid>https://orcid.org/0000-0001-8175-1647</orcidid></search><sort><creationdate>20180801</creationdate><title>Cancer cells copy migratory behavior and exchange signaling networks via extracellular vesicles</title><author>Steenbeek, Sander C ; Pham, Thang V ; de Ligt, Joep ; Zomer, Anoek ; Knol, Jaco C ; Piersma, Sander R ; Schelfhorst, Tim ; Huisjes, Rick ; Schiffelers, Raymond M ; Cuppen, Edwin ; Jimenez, Connie R ; van Rheenen, Jacco</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5137-75adc0d3387eb09440221aa120c8d70bf2b95fe9689a6e2510c9d3c38ec9c68b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Biomolecules</topic><topic>Cancer</topic><topic>Cell adhesion & migration</topic><topic>Cell Line, Tumor</topic><topic>Cell migration</topic><topic>Cell Movement - physiology</topic><topic>Cellular communication</topic><topic>Cre‐LoxP</topic><topic>EMBO03</topic><topic>EMBO20</topic><topic>EMBO31</topic><topic>Exchanging</topic><topic>Extracellular vesicles</topic><topic>Extracellular Vesicles - metabolism</topic><topic>Gene expression</topic><topic>Gene sequencing</topic><topic>Heterogeneity</topic><topic>In vivo methods and tests</topic><topic>intratumoral heterogeneity</topic><topic>intravital microscopy</topic><topic>Invasiveness</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Melanoma</topic><topic>Melanoma, Experimental - pathology</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Microenvironments</topic><topic>Microscopy</topic><topic>Neoplasm Metastasis - pathology</topic><topic>Proteins</topic><topic>Proteomes</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Messenger - genetics</topic><topic>Signal Transduction - physiology</topic><topic>Signaling</topic><topic>signaling networks</topic><topic>Tumor Microenvironment - physiology</topic><topic>Tumors</topic><topic>Vesicles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Steenbeek, Sander C</creatorcontrib><creatorcontrib>Pham, Thang V</creatorcontrib><creatorcontrib>de Ligt, Joep</creatorcontrib><creatorcontrib>Zomer, Anoek</creatorcontrib><creatorcontrib>Knol, Jaco C</creatorcontrib><creatorcontrib>Piersma, Sander R</creatorcontrib><creatorcontrib>Schelfhorst, Tim</creatorcontrib><creatorcontrib>Huisjes, Rick</creatorcontrib><creatorcontrib>Schiffelers, Raymond M</creatorcontrib><creatorcontrib>Cuppen, Edwin</creatorcontrib><creatorcontrib>Jimenez, Connie R</creatorcontrib><creatorcontrib>van Rheenen, Jacco</creatorcontrib><collection>Springer Nature OA/Free Journals</collection><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Steenbeek, Sander C</au><au>Pham, Thang V</au><au>de Ligt, Joep</au><au>Zomer, Anoek</au><au>Knol, Jaco C</au><au>Piersma, Sander R</au><au>Schelfhorst, Tim</au><au>Huisjes, Rick</au><au>Schiffelers, Raymond M</au><au>Cuppen, Edwin</au><au>Jimenez, Connie R</au><au>van Rheenen, Jacco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cancer cells copy migratory behavior and exchange signaling networks via extracellular vesicles</atitle><jtitle>The EMBO journal</jtitle><stitle>EMBO J</stitle><addtitle>EMBO J</addtitle><date>2018-08-01</date><risdate>2018</risdate><volume>37</volume><issue>15</issue><epage>n/a</epage><issn>0261-4189</issn><eissn>1460-2075</eissn><abstract>Recent data showed that cancer cells from different tumor subtypes with distinct metastatic potential influence each other's metastatic behavior by exchanging biomolecules through extracellular vesicles (EVs). However, it is debated how small amounts of cargo can mediate this effect, especially in tumors where all cells are from one subtype, and only subtle molecular differences drive metastatic heterogeneity. To study this, we have characterized the content of EVs shed
in vivo
by two clones of melanoma (B16) tumors with distinct metastatic potential. Using the Cre‐LoxP system and intravital microscopy, we show that cells from these distinct clones phenocopy their migratory behavior through EV exchange. By tandem mass spectrometry and RNA sequencing, we show that EVs shed by these clones into the tumor microenvironment contain thousands of different proteins and RNAs, and many of these biomolecules are from interconnected signaling networks involved in cellular processes such as migration. Thus, EVs contain numerous proteins and RNAs and act on recipient cells by invoking a multi‐faceted biological response including cell migration.
Synopsis
Imaging microscopy in live animals combined with transcriptome–proteome analyses are used to characterize the function and content of extracellular vesicles (EVs) shed
in vivo
by mouse melanoma tumors with distinct metastatic potential. These data suggest that EVs promote cell migration by transferring clusters of RNA and proteins acting in the same physiological signaling networks.
B16F1 and B16F10 melanoma cell clones with differential metastatic potencies functionally exchange EVs
in vivo
.
The less metastatic B16F1 cells display increased invasive potential after uptake of EVs from the more aggressive B16F10 cells.
EVs purified from B16F10 microenvironments contain more complex and distinct cargo networks of RNAs and proteins involved in cell migration than seen for B16F1.
Graphical Abstract
Melanoma cell subclones adopt increased migratory behavior
in vivo
by extracellular vesicle uptake, amplifying signaling nodes involved in cell motility.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29907695</pmid><doi>10.15252/embj.201798357</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-0400-9542</orcidid><orcidid>https://orcid.org/0000-0002-3103-4508</orcidid><orcidid>https://orcid.org/0000-0001-8175-1647</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; PubMed Central; Springer Nature OA/Free Journals; Free Full-Text Journals in Chemistry |
| subjects | Animals Biomolecules Cancer Cell adhesion & migration Cell Line, Tumor Cell migration Cell Movement - physiology Cellular communication Cre‐LoxP EMBO03 EMBO20 EMBO31 Exchanging Extracellular vesicles Extracellular Vesicles - metabolism Gene expression Gene sequencing Heterogeneity In vivo methods and tests intratumoral heterogeneity intravital microscopy Invasiveness Mass spectrometry Mass spectroscopy Melanoma Melanoma, Experimental - pathology Metastases Metastasis Mice Microenvironments Microscopy Neoplasm Metastasis - pathology Proteins Proteomes Ribonucleic acid RNA RNA, Messenger - genetics Signal Transduction - physiology Signaling signaling networks Tumor Microenvironment - physiology Tumors Vesicles |
| title | Cancer cells copy migratory behavior and exchange signaling networks via extracellular vesicles |
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