Microcirculation-on-a-Chip: A Microfluidic Platform for Assaying Blood- and Lymphatic-Vessel Permeability
Identifieur interne : 007823 ( Ncbi/Merge ); précédent : 007822; suivant : 007824Microcirculation-on-a-Chip: A Microfluidic Platform for Assaying Blood- and Lymphatic-Vessel Permeability
Auteurs : Miwa Sato [Japon] ; Naoki Sasaki [Japon] ; Manabu Ato [Japon] ; Satoshi Hirakawa [Japon] ; Kiichi Sato [Japon] ; Kae Sato [Japon]Source :
- PLoS ONE [ 1932-6203 ] ; 2015.
Abstract
We developed a microfluidic model of microcirculation containing both blood and lymphatic vessels for examining vascular permeability. The designed microfluidic device harbors upper and lower channels that are partly aligned and are separated by a porous membrane, and on this membrane, blood vascular endothelial cells (BECs) and lymphatic endothelial cells (LECs) were cocultured back-to-back. At cell-cell junctions of both BECs and LECs, claudin-5 and VE-cadherin were detected. The permeability coefficient measured here was lower than the value reported for isolated mammalian venules. Moreover, our results showed that the flow culture established in the device promoted the formation of endothelial cell-cell junctions, and that treatment with histamine, an inflammation-promoting substance, induced changes in the localization of tight and adherens junction-associated proteins and an increase in vascular permeability in the microdevice. These findings indicated that both BECs and LECs appeared to retain their functions in the microfluidic coculture platform. Using this microcirculation device, the vascular damage induced by habu snake venom was successfully assayed, and the assay time was reduced from 24 h to 30 min. This is the first report of a microcirculation model in which BECs and LECs were cocultured. Because the micromodel includes lymphatic vessels in addition to blood vessels, the model can be used to evaluate both vascular permeability and lymphatic return rate.
Url:
DOI: 10.1371/journal.pone.0137301
PubMed: 26332321
PubMed Central: 4558006
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Kantō</region></placeName></affiliation></author><author><name sortKey="Hirakawa, Satoshi" sort="Hirakawa, Satoshi" uniqKey="Hirakawa S" first="Satoshi" last="Hirakawa">Satoshi Hirakawa</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Dermatology at Hamamatsu University School of Medicine, Hamamatsu city, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Dermatology at Hamamatsu University School of Medicine, Hamamatsu city, Shizuoka</wicri:regionArea><wicri:noRegion>Shizuoka</wicri:noRegion></affiliation></author><author><name sortKey="Sato, Kiichi" sort="Sato, Kiichi" uniqKey="Sato K" first="Kiichi" last="Sato">Kiichi Sato</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Division of Molecular Science, School of Science and Technology, Gunma University, Kiryu, Gunma, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of Molecular Science, 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Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Sasaki, Naoki" sort="Sasaki, Naoki" uniqKey="Sasaki N" first="Naoki" last="Sasaki">Naoki Sasaki</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Ato, Manabu" sort="Ato, Manabu" uniqKey="Ato M" first="Manabu" last="Ato">Manabu Ato</name><affiliation wicri:level="3"><nlm:aff id="aff002"><addr-line>Department of Immunology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Immunology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Hirakawa, Satoshi" sort="Hirakawa, Satoshi" uniqKey="Hirakawa S" first="Satoshi" last="Hirakawa">Satoshi Hirakawa</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Dermatology at Hamamatsu University School of Medicine, Hamamatsu city, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Dermatology at Hamamatsu University School of Medicine, Hamamatsu city, Shizuoka</wicri:regionArea><wicri:noRegion>Shizuoka</wicri:noRegion></affiliation></author><author><name sortKey="Sato, Kiichi" sort="Sato, Kiichi" uniqKey="Sato K" first="Kiichi" last="Sato">Kiichi Sato</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Division of Molecular Science, School of Science and Technology, Gunma University, Kiryu, Gunma, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of Molecular Science, School of Science and Technology, Gunma University, Kiryu, Gunma</wicri:regionArea><wicri:noRegion>Gunma</wicri:noRegion></affiliation></author><author><name sortKey="Sato, Kae" sort="Sato, Kae" uniqKey="Sato K" first="Kae" last="Sato">Kae Sato</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We developed a microfluidic model of microcirculation containing both blood and lymphatic vessels for examining vascular permeability. The designed microfluidic device harbors upper and lower channels that are partly aligned and are separated by a porous membrane, and on this membrane, blood vascular endothelial cells (BECs) and lymphatic endothelial cells (LECs) were cocultured back-to-back. At cell-cell junctions of both BECs and LECs, claudin-5 and VE-cadherin were detected. The permeability coefficient measured here was lower than the value reported for isolated mammalian venules. Moreover, our results showed that the flow culture established in the device promoted the formation of endothelial cell-cell junctions, and that treatment with histamine, an inflammation-promoting substance, induced changes in the localization of tight and adherens junction-associated proteins and an increase in vascular permeability in the microdevice. These findings indicated that both BECs and LECs appeared to retain their functions in the microfluidic coculture platform. Using this microcirculation device, the vascular damage induced by habu snake venom was successfully assayed, and the assay time was reduced from 24 h to 30 min. This is the first report of a microcirculation model in which BECs and LECs were cocultured. Because the micromodel includes lymphatic vessels in addition to blood vessels, the model can be used to evaluate both vascular permeability and lymphatic return rate.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Granger, Dn" uniqKey="Granger D">DN Granger</name></author><author><name sortKey="Senchenkova, E" uniqKey="Senchenkova E">E Senchenkova</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Saito, Y" uniqKey="Saito Y">Y Saito</name></author><author><name sortKey="Nakagami, H" uniqKey="Nakagami H">H Nakagami</name></author><author><name sortKey="Kaneda, Y" uniqKey="Kaneda Y">Y Kaneda</name></author><author><name sortKey="Morishita, R" uniqKey="Morishita R">R Morishita</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kano, Mr" uniqKey="Kano M">MR Kano</name></author><author><name sortKey="Komuta, Y" uniqKey="Komuta Y">Y Komuta</name></author><author><name 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article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26332321</article-id><article-id pub-id-type="pmc">4558006</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0137301</article-id><article-id pub-id-type="publisher-id">PONE-D-15-19060</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Microcirculation-on-a-Chip: A Microfluidic Platform for Assaying Blood- and Lymphatic-Vessel Permeability</article-title><alt-title alt-title-type="running-head">Microcirculation-on-a-Chip</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Sato</surname><given-names>Miwa</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sasaki</surname><given-names>Naoki</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="author-notes" rid="currentaff001"><sup>¤</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ato</surname><given-names>Manabu</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hirakawa</surname><given-names>Satoshi</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sato</surname><given-names>Kiichi</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sato</surname><given-names>Kae</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref rid="cor001" ref-type="corresp">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, Bunkyo, Tokyo, Japan</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Immunology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Department of Dermatology at Hamamatsu University School of Medicine, Hamamatsu city, Shizuoka, Japan</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Division of Molecular Science, School of Science and Technology, Gunma University, Kiryu, Gunma, Japan</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Eddington</surname><given-names>David T.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of Illinois at Chicago, UNITED STATES</addr-line></aff><author-notes><fn fn-type="conflict" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: MS NS SH Kiichi Sato Kae Sato. Performed the experiments: MS. Analyzed the data: MS Kae Sato. Contributed reagents/materials/analysis tools: MA. Wrote the paper: MS Kiichi Sato Kae Sato.</p></fn><fn fn-type="current-aff" id="currentaff001"><label>¤</label><p>Current address: Department of Applied Chemistry, Faculty of Science and Engineering, Toyo University, Kawagoe, Saitama, Japan</p></fn><corresp id="cor001">* E-mail: <email>satouk@fc.jwu.ac.jp</email></corresp></author-notes><pub-date pub-type="epub"><day>2</day><month>9</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>10</volume><issue>9</issue><elocation-id>e0137301</elocation-id><history><date date-type="received"><day>2</day><month>5</month><year>2015</year></date><date date-type="accepted"><day>14</day><month>8</month><year>2015</year></date></history><permissions><copyright-year>2015</copyright-year><copyright-holder>Sato et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p></license></permissions><self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0137301.pdf"></self-uri><abstract><p>We developed a microfluidic model of microcirculation containing both blood and lymphatic vessels for examining vascular permeability. The designed microfluidic device harbors upper and lower channels that are partly aligned and are separated by a porous membrane, and on this membrane, blood vascular endothelial cells (BECs) and lymphatic endothelial cells (LECs) were cocultured back-to-back. At cell-cell junctions of both BECs and LECs, claudin-5 and VE-cadherin were detected. The permeability coefficient measured here was lower than the value reported for isolated mammalian venules. Moreover, our results showed that the flow culture established in the device promoted the formation of endothelial cell-cell junctions, and that treatment with histamine, an inflammation-promoting substance, induced changes in the localization of tight and adherens junction-associated proteins and an increase in vascular permeability in the microdevice. These findings indicated that both BECs and LECs appeared to retain their functions in the microfluidic coculture platform. Using this microcirculation device, the vascular damage induced by habu snake venom was successfully assayed, and the assay time was reduced from 24 h to 30 min. This is the first report of a microcirculation model in which BECs and LECs were cocultured. Because the micromodel includes lymphatic vessels in addition to blood vessels, the model can be used to evaluate both vascular permeability and lymphatic return rate.</p></abstract><funding-group><funding-statement>This work was supported in part by Tokyo Ohka Foundation for the Promotion of Science and Technology (to Kae S, <ext-link ext-link-type="uri" xlink:href="http://www.tok-foundation.or.jp/">http://www.tok-foundation.or.jp/</ext-link>), Banyu Foundation Research Grant (to Kae S, <ext-link ext-link-type="uri" xlink:href="http://www.banyu-zaidan.or.jp/">http://www.banyu-zaidan.or.jp/</ext-link>), The Science Research Promotion Fund (to Kae S, <ext-link ext-link-type="uri" xlink:href="http://www.shigaku.go.jp/s_shikin_menu.htm">http://www.shigaku.go.jp/s_shikin_menu.htm</ext-link>), Suzuken Memorial Foundation (to Kae S, <ext-link ext-link-type="uri" xlink:href="http://www.suzukenzaidan.or.jp/">http://www.suzukenzaidan.or.jp/</ext-link>), a Grant-in-Aid for Scientific Research (JSPS, KAKENHI; Grant Numbers 24350035 to Kiichi S and 25600065 to Kae S, <ext-link ext-link-type="uri" xlink:href="https://www.jsps.go.jp/english/e-grants/grants01.html">https://www.jsps.go.jp/english/e-grants/grants01.html</ext-link>), and the Core Research for Evolutional Science and Technology (JST, CREST) Program (to Kae S, <ext-link ext-link-type="uri" xlink:href="http://www.jst.go.jp/kisoken/crest/en/">http://www.jst.go.jp/kisoken/crest/en/</ext-link>).</funding-statement></funding-group><counts><fig-count count="7"></fig-count><table-count count="0"></table-count><page-count count="18"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc><affiliations><list><country><li>Japon</li></country><region><li>Région de Kantō</li></region><settlement><li>Tokyo</li></settlement></list><tree><country name="Japon"><region name="Région de Kantō"><name sortKey="Sato, Miwa" sort="Sato, Miwa" uniqKey="Sato M" first="Miwa" last="Sato">Miwa Sato</name></region><name sortKey="Ato, Manabu" sort="Ato, Manabu" uniqKey="Ato M" first="Manabu" last="Ato">Manabu Ato</name><name sortKey="Hirakawa, Satoshi" sort="Hirakawa, Satoshi" uniqKey="Hirakawa S" first="Satoshi" last="Hirakawa">Satoshi Hirakawa</name><name sortKey="Sasaki, Naoki" sort="Sasaki, Naoki" uniqKey="Sasaki N" first="Naoki" last="Sasaki">Naoki Sasaki</name><name sortKey="Sato, Kae" sort="Sato, Kae" uniqKey="Sato K" first="Kae" last="Sato">Kae Sato</name><name sortKey="Sato, Kiichi" sort="Sato, Kiichi" uniqKey="Sato K" first="Kiichi" last="Sato">Kiichi Sato</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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