Lattice light sheet imaging of membrane nanotubes between human breast cancer cells in culture and in brain metastases
Membrane nanotubes are cytosolic protrusions with diameters
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creator | Parker, Ian Evans, Katrina T. Ellefsen, Kyle Lawson, Devon A. Smith, Ian F. |
description | Membrane nanotubes are cytosolic protrusions with diameters |
doi_str_mv | 10.1038/s41598-017-11223-y |
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in vivo
relevance, and most studies have been confined to cell culture systems. Here, we introduce lattice-light sheet imaging of MDA-MB-231 human breast cancer cells genetically engineered to brightly express membrane–targeted GFP as a promising approach to visualize membrane nanotubes
in vitro
and
in situ
. We demonstrate that cultured cells form multiple nanotubes that mediate intercellular communication of Ca
2+
signals and actively traffic GFP-tagged membrane vesicles along their length. Furthermore, we directly visualize nanotubes
in situ
, interconnecting breast cancer cells in live acute brain slices from an experimental mouse model of breast cancer brain metastasis. This amenable experimental system should facilitate the transition of the study of intercellular communication by membrane nanotubes from cell culture to the whole animal.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-017-11223-y</identifier><identifier>PMID: 28887508</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14 ; 14/63 ; 631/67 ; 631/80 ; Animals ; Brain - pathology ; Brain cancer ; Brain Neoplasms - pathology ; Brain Neoplasms - secondary ; Brain slice preparation ; Breast cancer ; Breast Neoplasms - pathology ; Calcium signalling ; Cell culture ; Cell Culture Techniques ; Cell interactions ; Cell signaling ; Cell Surface Extensions - ultrastructure ; Communication ; Disease Models, Animal ; Genes, Reporter ; Genetic engineering ; Green Fluorescent Proteins - analysis ; Humanities and Social Sciences ; Humans ; Membrane trafficking ; Membrane vesicles ; Membranes ; Metastases ; Metastasis ; Mice ; multidisciplinary ; Nanotechnology ; Nanotubes ; Neoplasm Metastasis - pathology ; Neuroimaging ; Science ; Science (multidisciplinary) ; Staining and Labeling - methods ; Tumor Cells, Cultured - ultrastructure</subject><ispartof>Scientific reports, 2017-09, Vol.7 (1), p.11029-7, Article 11029</ispartof><rights>The Author(s) 2017</rights><rights>2017. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-8b8909fb8169a76adc25859d634064b0b5a51fa7f233abe9af999e04bfff7c443</citedby><cites>FETCH-LOGICAL-c540t-8b8909fb8169a76adc25859d634064b0b5a51fa7f233abe9af999e04bfff7c443</cites><orcidid>0000-0001-9910-195X</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/PMC5591308/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5591308/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,41120,42189,51576,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28887508$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Parker, Ian</creatorcontrib><creatorcontrib>Evans, Katrina T.</creatorcontrib><creatorcontrib>Ellefsen, Kyle</creatorcontrib><creatorcontrib>Lawson, Devon A.</creatorcontrib><creatorcontrib>Smith, Ian F.</creatorcontrib><title>Lattice light sheet imaging of membrane nanotubes between human breast cancer cells in culture and in brain metastases</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Membrane nanotubes are cytosolic protrusions with diameters <1 µm that extend between cells separated by tens of µm. They mediate several forms of intercellular communication and are upregulated in diverse diseases. Difficulties in visualizing and studying nanotubes within intact tissues have, however, prompted skepticism regarding their
in vivo
relevance, and most studies have been confined to cell culture systems. Here, we introduce lattice-light sheet imaging of MDA-MB-231 human breast cancer cells genetically engineered to brightly express membrane–targeted GFP as a promising approach to visualize membrane nanotubes
in vitro
and
in situ
. We demonstrate that cultured cells form multiple nanotubes that mediate intercellular communication of Ca
2+
signals and actively traffic GFP-tagged membrane vesicles along their length. Furthermore, we directly visualize nanotubes
in situ
, interconnecting breast cancer cells in live acute brain slices from an experimental mouse model of breast cancer brain metastasis. This amenable experimental system should facilitate the transition of the study of intercellular communication by membrane nanotubes from cell culture to the whole animal.</description><subject>14</subject><subject>14/63</subject><subject>631/67</subject><subject>631/80</subject><subject>Animals</subject><subject>Brain - pathology</subject><subject>Brain cancer</subject><subject>Brain Neoplasms - pathology</subject><subject>Brain Neoplasms - secondary</subject><subject>Brain slice preparation</subject><subject>Breast cancer</subject><subject>Breast Neoplasms - pathology</subject><subject>Calcium signalling</subject><subject>Cell culture</subject><subject>Cell Culture Techniques</subject><subject>Cell interactions</subject><subject>Cell signaling</subject><subject>Cell Surface Extensions - ultrastructure</subject><subject>Communication</subject><subject>Disease Models, Animal</subject><subject>Genes, Reporter</subject><subject>Genetic engineering</subject><subject>Green Fluorescent Proteins - analysis</subject><subject>Humanities and Social Sciences</subject><subject>Humans</subject><subject>Membrane trafficking</subject><subject>Membrane vesicles</subject><subject>Membranes</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice</subject><subject>multidisciplinary</subject><subject>Nanotechnology</subject><subject>Nanotubes</subject><subject>Neoplasm Metastasis - pathology</subject><subject>Neuroimaging</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Staining and Labeling - methods</subject><subject>Tumor Cells, Cultured - ultrastructure</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kUtv1DAUhSMEolXpH2CBLLFhk-JnYm-QUFUe0khsYG1de64zqRKn2E7R_Pt6mFINSHjhh-53j318muY1o1eMCv0-S6aMbinrW8Y4F-3-WXPOqVQtF5w_P9mfNZc539I6FDeSmZfNGdda94rq8-Z-A6WMHsk0DrtC8g6xkHGGYYwDWQKZcXYJIpIIcSmrw0wcll-IkezWGSJxCSEX4iF6TMTjNGUyRuLXqawJCcTt4Vg16jxjqSxkzK-aFwGmjJeP60Xz49PN9-sv7ebb56_XHzetV5KWVjttqAlOs85A38HWc6WV2XZC0k466hQoFqAPXAhwaCAYY5BKF0LovZTiovlw1L1b3Yxbj7EkmOxdqhbT3i4w2r8rcdzZYbm3ShkmqK4C7x4F0vJzxVzsPOaDy_ony5otM6JXgnaaVvTtP-jtsqZY7VVKCaOFVH2l-JHyack5YXh6DKP2kKw9JmtrsvZ3snZfm96c2nhq-ZNjBcQRyLUUB0wnd_9f9gH4rrGI</recordid><startdate>20170908</startdate><enddate>20170908</enddate><creator>Parker, Ian</creator><creator>Evans, Katrina T.</creator><creator>Ellefsen, Kyle</creator><creator>Lawson, Devon A.</creator><creator>Smith, Ian F.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9910-195X</orcidid></search><sort><creationdate>20170908</creationdate><title>Lattice light sheet imaging of membrane nanotubes between human breast cancer cells in culture and in brain metastases</title><author>Parker, Ian ; Evans, Katrina T. ; Ellefsen, Kyle ; Lawson, Devon A. ; Smith, Ian F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-8b8909fb8169a76adc25859d634064b0b5a51fa7f233abe9af999e04bfff7c443</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>14</topic><topic>14/63</topic><topic>631/67</topic><topic>631/80</topic><topic>Animals</topic><topic>Brain - pathology</topic><topic>Brain cancer</topic><topic>Brain Neoplasms - pathology</topic><topic>Brain Neoplasms - secondary</topic><topic>Brain slice preparation</topic><topic>Breast cancer</topic><topic>Breast Neoplasms - pathology</topic><topic>Calcium signalling</topic><topic>Cell culture</topic><topic>Cell Culture Techniques</topic><topic>Cell interactions</topic><topic>Cell signaling</topic><topic>Cell Surface Extensions - ultrastructure</topic><topic>Communication</topic><topic>Disease Models, Animal</topic><topic>Genes, Reporter</topic><topic>Genetic engineering</topic><topic>Green Fluorescent Proteins - analysis</topic><topic>Humanities and Social Sciences</topic><topic>Humans</topic><topic>Membrane trafficking</topic><topic>Membrane vesicles</topic><topic>Membranes</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Mice</topic><topic>multidisciplinary</topic><topic>Nanotechnology</topic><topic>Nanotubes</topic><topic>Neoplasm Metastasis - pathology</topic><topic>Neuroimaging</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Staining and Labeling - methods</topic><topic>Tumor Cells, Cultured - ultrastructure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Parker, Ian</creatorcontrib><creatorcontrib>Evans, Katrina T.</creatorcontrib><creatorcontrib>Ellefsen, Kyle</creatorcontrib><creatorcontrib>Lawson, Devon A.</creatorcontrib><creatorcontrib>Smith, Ian F.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database (ProQuest)</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Parker, Ian</au><au>Evans, Katrina T.</au><au>Ellefsen, Kyle</au><au>Lawson, Devon A.</au><au>Smith, Ian F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lattice light sheet imaging of membrane nanotubes between human breast cancer cells in culture and in brain metastases</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2017-09-08</date><risdate>2017</risdate><volume>7</volume><issue>1</issue><spage>11029</spage><epage>7</epage><pages>11029-7</pages><artnum>11029</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Membrane nanotubes are cytosolic protrusions with diameters <1 µm that extend between cells separated by tens of µm. They mediate several forms of intercellular communication and are upregulated in diverse diseases. Difficulties in visualizing and studying nanotubes within intact tissues have, however, prompted skepticism regarding their
in vivo
relevance, and most studies have been confined to cell culture systems. Here, we introduce lattice-light sheet imaging of MDA-MB-231 human breast cancer cells genetically engineered to brightly express membrane–targeted GFP as a promising approach to visualize membrane nanotubes
in vitro
and
in situ
. We demonstrate that cultured cells form multiple nanotubes that mediate intercellular communication of Ca
2+
signals and actively traffic GFP-tagged membrane vesicles along their length. Furthermore, we directly visualize nanotubes
in situ
, interconnecting breast cancer cells in live acute brain slices from an experimental mouse model of breast cancer brain metastasis. This amenable experimental system should facilitate the transition of the study of intercellular communication by membrane nanotubes from cell culture to the whole animal.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>28887508</pmid><doi>10.1038/s41598-017-11223-y</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0001-9910-195X</orcidid><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; DOAJ Directory of Open Access Journals; Springer Nature OA Free Journals; Nature Free; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | 14 14/63 631/67 631/80 Animals Brain - pathology Brain cancer Brain Neoplasms - pathology Brain Neoplasms - secondary Brain slice preparation Breast cancer Breast Neoplasms - pathology Calcium signalling Cell culture Cell Culture Techniques Cell interactions Cell signaling Cell Surface Extensions - ultrastructure Communication Disease Models, Animal Genes, Reporter Genetic engineering Green Fluorescent Proteins - analysis Humanities and Social Sciences Humans Membrane trafficking Membrane vesicles Membranes Metastases Metastasis Mice multidisciplinary Nanotechnology Nanotubes Neoplasm Metastasis - pathology Neuroimaging Science Science (multidisciplinary) Staining and Labeling - methods Tumor Cells, Cultured - ultrastructure |
title | Lattice light sheet imaging of membrane nanotubes between human breast cancer cells in culture and in brain metastases |
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