Aquaporins differentially regulate cell‐cell adhesion in MDCK cells
ABSTRACT Plasticity of epithelial cell‐cell adhesion is vital in epithelial homeostasis and is regulated in multiple processes associated with cell migration, such as embryogenesis and wound healing. In cancer, cell‐cell adhesion is compromised and is associated with increased cell migration and met...
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Veröffentlicht in: | The FASEB journal 2019-06, Vol.33 (6), p.6980-6994 |
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creator | Login, Frédéric H. Jensen, Helene H. Pedersen, Gitte A. Koffman, Jennifer S. Kwon, Tae-Hwan Parsons, Maddy Nejsum, Lene N. |
description | ABSTRACT
Plasticity of epithelial cell‐cell adhesion is vital in epithelial homeostasis and is regulated in multiple processes associated with cell migration, such as embryogenesis and wound healing. In cancer, cell‐cell adhesion is compromised and is associated with increased cell migration and metastasis. Aquaporin (AQP) water channels facilitate water transport across cell membranes and are essential in the regulation of body water homeostasis. Increased expression of several AQPs, especially AQP5, is associated with increased cancer cell migration, metastasis, and poor prognosis. We found that AQP5 overexpression in normal epithelial cells induced cell detachment and dissemination from migrating cell sheets. AQP5 reduced both cell‐cell coordination during collective migration and overall distance covered by the migrating cell sheets. AQP5 and the isoforms AQP1 and AQP4 decreased, whereas AQP3 increased, levels of plasma membrane‐associated lateral junctional proteins. This regulation was mediated by the cytoplasmic domains of the AQPs. This shows that the AQPs have dual functions in epithelial physiology: as channel proteins and as differential regulators of cell‐cell adhesiveness. This regulation may contribute to dynamic regulation of cell junctions in processes such as embryogenesis and wound healing and also explain the pivotal roles of AQPs in carcinogenesis and metastasis.—Login, F. H., Jensen, H. H., Pedersen, G. A., Koffman, J. S., Kwon, T.‐H., Parsons, M., Nejsum, L. N. Aquaporins differentially regulate cell‐cell adhesion in MDCK cells. FASEB J. 33, 6980–6994 (2019). www.fasebj.org |
doi_str_mv | 10.1096/fj.201802068RR |
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Plasticity of epithelial cell‐cell adhesion is vital in epithelial homeostasis and is regulated in multiple processes associated with cell migration, such as embryogenesis and wound healing. In cancer, cell‐cell adhesion is compromised and is associated with increased cell migration and metastasis. Aquaporin (AQP) water channels facilitate water transport across cell membranes and are essential in the regulation of body water homeostasis. Increased expression of several AQPs, especially AQP5, is associated with increased cancer cell migration, metastasis, and poor prognosis. We found that AQP5 overexpression in normal epithelial cells induced cell detachment and dissemination from migrating cell sheets. AQP5 reduced both cell‐cell coordination during collective migration and overall distance covered by the migrating cell sheets. AQP5 and the isoforms AQP1 and AQP4 decreased, whereas AQP3 increased, levels of plasma membrane‐associated lateral junctional proteins. This regulation was mediated by the cytoplasmic domains of the AQPs. This shows that the AQPs have dual functions in epithelial physiology: as channel proteins and as differential regulators of cell‐cell adhesiveness. This regulation may contribute to dynamic regulation of cell junctions in processes such as embryogenesis and wound healing and also explain the pivotal roles of AQPs in carcinogenesis and metastasis.—Login, F. H., Jensen, H. H., Pedersen, G. A., Koffman, J. S., Kwon, T.‐H., Parsons, M., Nejsum, L. N. Aquaporins differentially regulate cell‐cell adhesion in MDCK cells. FASEB J. 33, 6980–6994 (2019). www.fasebj.org</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.201802068RR</identifier><identifier>PMID: 30840830</identifier><language>eng</language><publisher>United States: Federation of American Societies for Experimental Biology</publisher><subject>Animals ; Aquaporins - genetics ; Aquaporins - metabolism ; cancer ; Cell Adhesion - physiology ; Cell Adhesion Molecules ; Cell Membrane ; cell migration ; Dogs ; Gene Expression Regulation ; junctional proteins ; Madin Darby Canine Kidney Cells ; metastasis</subject><ispartof>The FASEB journal, 2019-06, Vol.33 (6), p.6980-6994</ispartof><rights>FASEB</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c349R-b6c31d3c2216e0a28f935cfc46a96cb0228a23d0f1705fd089d62e06257937cb3</citedby><cites>FETCH-LOGICAL-c349R-b6c31d3c2216e0a28f935cfc46a96cb0228a23d0f1705fd089d62e06257937cb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.201802068RR$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.201802068RR$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30840830$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Login, Frédéric H.</creatorcontrib><creatorcontrib>Jensen, Helene H.</creatorcontrib><creatorcontrib>Pedersen, Gitte A.</creatorcontrib><creatorcontrib>Koffman, Jennifer S.</creatorcontrib><creatorcontrib>Kwon, Tae-Hwan</creatorcontrib><creatorcontrib>Parsons, Maddy</creatorcontrib><creatorcontrib>Nejsum, Lene N.</creatorcontrib><title>Aquaporins differentially regulate cell‐cell adhesion in MDCK cells</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><description>ABSTRACT
Plasticity of epithelial cell‐cell adhesion is vital in epithelial homeostasis and is regulated in multiple processes associated with cell migration, such as embryogenesis and wound healing. In cancer, cell‐cell adhesion is compromised and is associated with increased cell migration and metastasis. Aquaporin (AQP) water channels facilitate water transport across cell membranes and are essential in the regulation of body water homeostasis. Increased expression of several AQPs, especially AQP5, is associated with increased cancer cell migration, metastasis, and poor prognosis. We found that AQP5 overexpression in normal epithelial cells induced cell detachment and dissemination from migrating cell sheets. AQP5 reduced both cell‐cell coordination during collective migration and overall distance covered by the migrating cell sheets. AQP5 and the isoforms AQP1 and AQP4 decreased, whereas AQP3 increased, levels of plasma membrane‐associated lateral junctional proteins. This regulation was mediated by the cytoplasmic domains of the AQPs. This shows that the AQPs have dual functions in epithelial physiology: as channel proteins and as differential regulators of cell‐cell adhesiveness. This regulation may contribute to dynamic regulation of cell junctions in processes such as embryogenesis and wound healing and also explain the pivotal roles of AQPs in carcinogenesis and metastasis.—Login, F. H., Jensen, H. H., Pedersen, G. A., Koffman, J. S., Kwon, T.‐H., Parsons, M., Nejsum, L. N. Aquaporins differentially regulate cell‐cell adhesion in MDCK cells. FASEB J. 33, 6980–6994 (2019). www.fasebj.org</description><subject>Animals</subject><subject>Aquaporins - genetics</subject><subject>Aquaporins - metabolism</subject><subject>cancer</subject><subject>Cell Adhesion - physiology</subject><subject>Cell Adhesion Molecules</subject><subject>Cell Membrane</subject><subject>cell migration</subject><subject>Dogs</subject><subject>Gene Expression Regulation</subject><subject>junctional proteins</subject><subject>Madin Darby Canine Kidney Cells</subject><subject>metastasis</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkMtOAjEUhhujEUS3Ls28wIynLXPoLFwggjeMCep60ulFS8qALcSw8xF8Rp9EEDXsXP2L_3JOPkKOKWQUCjy144wBFcAAxWi0Q5o055CiQNglTRAFSxG5aJCDGMcAQIHiPmlwEG0QHJqk331dyNk0uDom2llrgqnnTnq_TIJ5Xng5N4ky3n--f6wlkfrFRDetE1cndxe9228zHpI9K300Rz_aIk-D_mPvKh3eX173usNU8XYxSitUnGquGKNoQDJhC54rq9ooC1QVMCYk4xos7UBu9ep9jcwAsrxT8I6qeItkm10VpjEGY8tZcBMZliWFcs2jtONyi8eqcLIpzBbVxOi_-C-AVeBsE3hz3iz_mSsHD-dscLN94AtB5G3P</recordid><startdate>201906</startdate><enddate>201906</enddate><creator>Login, Frédéric H.</creator><creator>Jensen, Helene H.</creator><creator>Pedersen, Gitte A.</creator><creator>Koffman, Jennifer S.</creator><creator>Kwon, Tae-Hwan</creator><creator>Parsons, Maddy</creator><creator>Nejsum, Lene N.</creator><general>Federation of American Societies for Experimental Biology</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></search><sort><creationdate>201906</creationdate><title>Aquaporins differentially regulate cell‐cell adhesion in MDCK cells</title><author>Login, Frédéric H. ; Jensen, Helene H. ; Pedersen, Gitte A. ; Koffman, Jennifer S. ; Kwon, Tae-Hwan ; Parsons, Maddy ; Nejsum, Lene N.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c349R-b6c31d3c2216e0a28f935cfc46a96cb0228a23d0f1705fd089d62e06257937cb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Aquaporins - genetics</topic><topic>Aquaporins - metabolism</topic><topic>cancer</topic><topic>Cell Adhesion - physiology</topic><topic>Cell Adhesion Molecules</topic><topic>Cell Membrane</topic><topic>cell migration</topic><topic>Dogs</topic><topic>Gene Expression Regulation</topic><topic>junctional proteins</topic><topic>Madin Darby Canine Kidney Cells</topic><topic>metastasis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Login, Frédéric H.</creatorcontrib><creatorcontrib>Jensen, Helene H.</creatorcontrib><creatorcontrib>Pedersen, Gitte A.</creatorcontrib><creatorcontrib>Koffman, Jennifer S.</creatorcontrib><creatorcontrib>Kwon, Tae-Hwan</creatorcontrib><creatorcontrib>Parsons, Maddy</creatorcontrib><creatorcontrib>Nejsum, Lene N.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Login, Frédéric H.</au><au>Jensen, Helene H.</au><au>Pedersen, Gitte A.</au><au>Koffman, Jennifer S.</au><au>Kwon, Tae-Hwan</au><au>Parsons, Maddy</au><au>Nejsum, Lene N.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aquaporins differentially regulate cell‐cell adhesion in MDCK cells</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2019-06</date><risdate>2019</risdate><volume>33</volume><issue>6</issue><spage>6980</spage><epage>6994</epage><pages>6980-6994</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>ABSTRACT
Plasticity of epithelial cell‐cell adhesion is vital in epithelial homeostasis and is regulated in multiple processes associated with cell migration, such as embryogenesis and wound healing. In cancer, cell‐cell adhesion is compromised and is associated with increased cell migration and metastasis. Aquaporin (AQP) water channels facilitate water transport across cell membranes and are essential in the regulation of body water homeostasis. Increased expression of several AQPs, especially AQP5, is associated with increased cancer cell migration, metastasis, and poor prognosis. We found that AQP5 overexpression in normal epithelial cells induced cell detachment and dissemination from migrating cell sheets. AQP5 reduced both cell‐cell coordination during collective migration and overall distance covered by the migrating cell sheets. AQP5 and the isoforms AQP1 and AQP4 decreased, whereas AQP3 increased, levels of plasma membrane‐associated lateral junctional proteins. This regulation was mediated by the cytoplasmic domains of the AQPs. This shows that the AQPs have dual functions in epithelial physiology: as channel proteins and as differential regulators of cell‐cell adhesiveness. This regulation may contribute to dynamic regulation of cell junctions in processes such as embryogenesis and wound healing and also explain the pivotal roles of AQPs in carcinogenesis and metastasis.—Login, F. H., Jensen, H. H., Pedersen, G. A., Koffman, J. S., Kwon, T.‐H., Parsons, M., Nejsum, L. N. Aquaporins differentially regulate cell‐cell adhesion in MDCK cells. FASEB J. 33, 6980–6994 (2019). www.fasebj.org</abstract><cop>United States</cop><pub>Federation of American Societies for Experimental Biology</pub><pmid>30840830</pmid><doi>10.1096/fj.201802068RR</doi><tpages>15</tpages></addata></record> |
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subjects | Animals Aquaporins - genetics Aquaporins - metabolism cancer Cell Adhesion - physiology Cell Adhesion Molecules Cell Membrane cell migration Dogs Gene Expression Regulation junctional proteins Madin Darby Canine Kidney Cells metastasis |
title | Aquaporins differentially regulate cell‐cell adhesion in MDCK cells |
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