Listeriolysin O Affects the Permeability of Caco-2 Monolayer in a Pore-Dependent and Ca2+-Independent Manner
Listeria monocytogenes is a food and soil-borne pathogen that secretes a pore-forming toxin listeriolysin O (LLO) as its major virulence factor. We tested the effects of LLO on an intestinal epithelial cell line Caco-2 and compared them to an unrelated pore-forming toxin equinatoxin II (EqtII). Resu...
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| Veröffentlicht in: | PloS one 2015-06, Vol.10 (6), p.e0130471-e0130471 |
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| creator | Cajnko, Miša Mojca Marušić, Maja Kisovec, Matic Rojko, Nejc Benčina, Mojca Caserman, Simon Anderluh, Gregor |
| description | Listeria monocytogenes is a food and soil-borne pathogen that secretes a pore-forming toxin listeriolysin O (LLO) as its major virulence factor. We tested the effects of LLO on an intestinal epithelial cell line Caco-2 and compared them to an unrelated pore-forming toxin equinatoxin II (EqtII). Results showed that apical application of both toxins causes a significant drop in transepithelial electrical resistance (TEER), with higher LLO concentrations or prolonged exposure time needed to achieve the same magnitude of response than with EqtII. The drop in TEER was due to pore formation and coincided with rearrangement of claudin-1 within tight junctions and associated actin cytoskeleton; however, no significant increase in permeability to fluorescein or 3 kDa FITC-dextran was observed. Influx of calcium after pore formation affected the magnitude of the drop in TEER. Both toxins exhibit similar effects on epithelium morphology and physiology. Importantly, LLO action upon the membrane is much slower and results in compromised epithelium on a longer time scale at lower concentrations than EqtII. This could favor listerial invasion in hosts resistant to E-cadherin related infection. |
| doi_str_mv | 10.1371/journal.pone.0130471 |
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We tested the effects of LLO on an intestinal epithelial cell line Caco-2 and compared them to an unrelated pore-forming toxin equinatoxin II (EqtII). Results showed that apical application of both toxins causes a significant drop in transepithelial electrical resistance (TEER), with higher LLO concentrations or prolonged exposure time needed to achieve the same magnitude of response than with EqtII. The drop in TEER was due to pore formation and coincided with rearrangement of claudin-1 within tight junctions and associated actin cytoskeleton; however, no significant increase in permeability to fluorescein or 3 kDa FITC-dextran was observed. Influx of calcium after pore formation affected the magnitude of the drop in TEER. Both toxins exhibit similar effects on epithelium morphology and physiology. Importantly, LLO action upon the membrane is much slower and results in compromised epithelium on a longer time scale at lower concentrations than EqtII. This could favor listerial invasion in hosts resistant to E-cadherin related infection.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0130471</identifier><identifier>PMID: 26087154</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actin ; Actins - metabolism ; Bacterial Toxins - metabolism ; Caco-2 Cells - metabolism ; Caco-2 Cells - microbiology ; Caco-2 Cells - pathology ; Calcium ; Calcium - metabolism ; Calcium influx ; Calcium ions ; Calcium permeability ; Cholesterol ; Claudin-1 - metabolism ; Cnidarian Venoms - metabolism ; Cytoskeleton ; Dextran ; E-cadherin ; Electrical junctions ; Epithelial cells ; Epithelium ; Fluorescein ; Forming ; Heat-Shock Proteins - metabolism ; Hemolysin Proteins - metabolism ; Humans ; Immunoglobulins ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - microbiology ; Intestinal Mucosa - pathology ; Intestine ; Laboratories ; Lipids ; Listeria ; Listeria monocytogenes ; Listeria monocytogenes - physiology ; Listeriolysin O ; Listeriosis - metabolism ; Listeriosis - pathology ; Membrane permeability ; Molecular biology ; Permeability ; Pore formation ; Proteins ; Soil permeability ; Streptococcus infections ; Tight junctions ; Toxins ; Virulence ; Virulence factors</subject><ispartof>PloS one, 2015-06, Vol.10 (6), p.e0130471-e0130471</ispartof><rights>2015 Cajnko et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Cajnko et al 2015 Cajnko et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c522t-3a7cc7561b58ef3065e0f3c6dd15aaf9e1e0311e120ed5532ad688b23c092b8f3</citedby><cites>FETCH-LOGICAL-c522t-3a7cc7561b58ef3065e0f3c6dd15aaf9e1e0311e120ed5532ad688b23c092b8f3</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/PMC4472510/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4472510/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23847,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26087154$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gillet, Daniel</contributor><creatorcontrib>Cajnko, Miša Mojca</creatorcontrib><creatorcontrib>Marušić, Maja</creatorcontrib><creatorcontrib>Kisovec, Matic</creatorcontrib><creatorcontrib>Rojko, Nejc</creatorcontrib><creatorcontrib>Benčina, Mojca</creatorcontrib><creatorcontrib>Caserman, Simon</creatorcontrib><creatorcontrib>Anderluh, Gregor</creatorcontrib><title>Listeriolysin O Affects the Permeability of Caco-2 Monolayer in a Pore-Dependent and Ca2+-Independent Manner</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Listeria monocytogenes is a food and soil-borne pathogen that secretes a pore-forming toxin listeriolysin O (LLO) as its major virulence factor. 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This could favor listerial invasion in hosts resistant to E-cadherin related infection.</description><subject>Actin</subject><subject>Actins - metabolism</subject><subject>Bacterial Toxins - metabolism</subject><subject>Caco-2 Cells - metabolism</subject><subject>Caco-2 Cells - microbiology</subject><subject>Caco-2 Cells - pathology</subject><subject>Calcium</subject><subject>Calcium - metabolism</subject><subject>Calcium influx</subject><subject>Calcium ions</subject><subject>Calcium permeability</subject><subject>Cholesterol</subject><subject>Claudin-1 - metabolism</subject><subject>Cnidarian Venoms - metabolism</subject><subject>Cytoskeleton</subject><subject>Dextran</subject><subject>E-cadherin</subject><subject>Electrical junctions</subject><subject>Epithelial cells</subject><subject>Epithelium</subject><subject>Fluorescein</subject><subject>Forming</subject><subject>Heat-Shock Proteins - metabolism</subject><subject>Hemolysin Proteins - metabolism</subject><subject>Humans</subject><subject>Immunoglobulins</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Intestinal Mucosa - pathology</subject><subject>Intestine</subject><subject>Laboratories</subject><subject>Lipids</subject><subject>Listeria</subject><subject>Listeria monocytogenes</subject><subject>Listeria monocytogenes - physiology</subject><subject>Listeriolysin O</subject><subject>Listeriosis - metabolism</subject><subject>Listeriosis - pathology</subject><subject>Membrane permeability</subject><subject>Molecular biology</subject><subject>Permeability</subject><subject>Pore formation</subject><subject>Proteins</subject><subject>Soil permeability</subject><subject>Streptococcus infections</subject><subject>Tight junctions</subject><subject>Toxins</subject><subject>Virulence</subject><subject>Virulence factors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUstuEzEUHSEQLYE_QGCJTSU0wY_xPDZIVcojUqp2AWvrjn3dTuTYwZ4g5e9xyKRqESvb1-cc3-N7iuIto3MmGvZpHXbRg5tvg8c5ZYJWDXtWnLNO8LLmVDx_tD8rXqW0plSKtq5fFme8pm3DZHVeuNWQRoxDcPs0eHJDLq1FPSYy3iO5xbhB6Ac3jHsSLFmADiUn18EHB3uMJDOA3IaI5RVu0Rv0IwFvMpB_LJf5fCpeg_cYXxcvLLiEb6Z1Vvz8-uXH4nu5uvm2XFyuSi05H0sBjdaNrFkvW7SC1hKpFbo2hkkA2yFDKhhDxikaKQUHU7dtz4WmHe9bK2bF-6Pu1oWkpo9KitVt11aykzwjlkeECbBW2zhsIO5VgEH9LYR4pyCOg3aosAHN0FRVX-lKUwHMAlpDe-gNgu2z1ufptV2_QaOz3wjuiejTGz_cq7vwW1VVwyWjWeBiEojh1w7TqDZD0ugceAy7Q98d5Xlaeciz4sM_0P-7q44oHUNKEe1DM4yqQ3hOLHUIj5rCk2nvHht5IJ3SIv4AsWnDzA</recordid><startdate>20150618</startdate><enddate>20150618</enddate><creator>Cajnko, Miša Mojca</creator><creator>Marušić, Maja</creator><creator>Kisovec, Matic</creator><creator>Rojko, Nejc</creator><creator>Benčina, Mojca</creator><creator>Caserman, Simon</creator><creator>Anderluh, Gregor</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150618</creationdate><title>Listeriolysin O Affects the Permeability of Caco-2 Monolayer in a Pore-Dependent and Ca2+-Independent Manner</title><author>Cajnko, Miša Mojca ; Marušić, Maja ; Kisovec, Matic ; Rojko, Nejc ; Benčina, Mojca ; Caserman, Simon ; Anderluh, Gregor</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c522t-3a7cc7561b58ef3065e0f3c6dd15aaf9e1e0311e120ed5532ad688b23c092b8f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Actin</topic><topic>Actins - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cajnko, Miša Mojca</au><au>Marušić, Maja</au><au>Kisovec, Matic</au><au>Rojko, Nejc</au><au>Benčina, Mojca</au><au>Caserman, Simon</au><au>Anderluh, Gregor</au><au>Gillet, Daniel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Listeriolysin O Affects the Permeability of Caco-2 Monolayer in a Pore-Dependent and Ca2+-Independent Manner</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-06-18</date><risdate>2015</risdate><volume>10</volume><issue>6</issue><spage>e0130471</spage><epage>e0130471</epage><pages>e0130471-e0130471</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Listeria monocytogenes is a food and soil-borne pathogen that secretes a pore-forming toxin listeriolysin O (LLO) as its major virulence factor. We tested the effects of LLO on an intestinal epithelial cell line Caco-2 and compared them to an unrelated pore-forming toxin equinatoxin II (EqtII). Results showed that apical application of both toxins causes a significant drop in transepithelial electrical resistance (TEER), with higher LLO concentrations or prolonged exposure time needed to achieve the same magnitude of response than with EqtII. The drop in TEER was due to pore formation and coincided with rearrangement of claudin-1 within tight junctions and associated actin cytoskeleton; however, no significant increase in permeability to fluorescein or 3 kDa FITC-dextran was observed. Influx of calcium after pore formation affected the magnitude of the drop in TEER. Both toxins exhibit similar effects on epithelium morphology and physiology. Importantly, LLO action upon the membrane is much slower and results in compromised epithelium on a longer time scale at lower concentrations than EqtII. This could favor listerial invasion in hosts resistant to E-cadherin related infection.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26087154</pmid><doi>10.1371/journal.pone.0130471</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Actins - metabolism Bacterial Toxins - metabolism Caco-2 Cells - metabolism Caco-2 Cells - microbiology Caco-2 Cells - pathology Calcium Calcium - metabolism Calcium influx Calcium ions Calcium permeability Cholesterol Claudin-1 - metabolism Cnidarian Venoms - metabolism Cytoskeleton Dextran E-cadherin Electrical junctions Epithelial cells Epithelium Fluorescein Forming Heat-Shock Proteins - metabolism Hemolysin Proteins - metabolism Humans Immunoglobulins Intestinal Mucosa - metabolism Intestinal Mucosa - microbiology Intestinal Mucosa - pathology Intestine Laboratories Lipids Listeria Listeria monocytogenes Listeria monocytogenes - physiology Listeriolysin O Listeriosis - metabolism Listeriosis - pathology Membrane permeability Molecular biology Permeability Pore formation Proteins Soil permeability Streptococcus infections Tight junctions Toxins Virulence Virulence factors |
| title | Listeriolysin O Affects the Permeability of Caco-2 Monolayer in a Pore-Dependent and Ca2+-Independent Manner |
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