Membrane Vesicles Released by Intestinal Epithelial Cells Infected with Rotavirus Inhibit T-Cell Function
Rotavirus (RV) predominantly replicates in intestinal epithelial cells (IEC), and “danger signals” released by these cells may modulate viral immunity. We have recently shown that human model IEC (Caco-2 cells) infected with rhesus-RV release a non-inflammatory group of immunomodulators that include...
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| Veröffentlicht in: | Viral immunology 2010-12, Vol.23 (6), p.595-608 |
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| creator | Barreto, Alfonso Rodríguez, Luz-Stella Rojas, Olga Lucía Wolf, Marie Greenberg, Harry B. Franco, Manuel A. Angel, Juana |
| description | Rotavirus (RV) predominantly replicates in intestinal epithelial cells (IEC), and “danger signals” released by these cells may modulate viral immunity. We have recently shown that human model IEC (Caco-2 cells) infected with rhesus-RV release a non-inflammatory group of immunomodulators that includes heat shock proteins (HSPs) and TGF-β1. Here we show that both proteins are released in part in association with membrane vesicles (MV) obtained from filtrated Caco-2 supernatants concentrated by ultracentrifugation. These MV express markers of exosomes (CD63 and others), but not of the endoplasmic reticulum (ER) or nuclei. Larger quantities of proteins associated with MV were released by RV-infected cells than by non-infected cells. VP6 co-immunoprecipitated with CD63 present in these MV, and VP6 co-localized with CD63 in RV-infected cells, suggesting that this viral protein is associated with the MV, and that this association occurs intracellularly. CD63 present in MV preparations from stool samples from 36 children with gastroenteritis due or not due to RV were analyzed. VP6 co-immunoprecipitated with CD63 in 3/8 stool samples from RV-infected children, suggesting that these MV are released by RV-infected cells
in vivo
. Moreover, fractions that contained MV from RV-infected cells induced death and inhibited proliferation of CD4
+
T cells to a greater extent than fractions from non-infected cells. These effects were in part due to TGF-β, because they were reversed by treatment of the T cells with the TGF-β-receptor inhibitor ALK5i. MV from RV-infected and non-infected cells were heterogeneous, with morphologies and typical flotation densities described for exosomes (between 1.10 and 1.18 g/mL), and denser vesicles (>1.24 g/mL). Both types of MV from RV-infected cells were more efficient at inhibiting T-cell function than were those from non-infected cells. We propose that RV infection of IEC releases MV that modulate viral immunity. |
| doi_str_mv | 10.1089/vim.2009.0113 |
| format | Article |
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in vivo
. Moreover, fractions that contained MV from RV-infected cells induced death and inhibited proliferation of CD4
+
T cells to a greater extent than fractions from non-infected cells. These effects were in part due to TGF-β, because they were reversed by treatment of the T cells with the TGF-β-receptor inhibitor ALK5i. MV from RV-infected and non-infected cells were heterogeneous, with morphologies and typical flotation densities described for exosomes (between 1.10 and 1.18 g/mL), and denser vesicles (>1.24 g/mL). Both types of MV from RV-infected cells were more efficient at inhibiting T-cell function than were those from non-infected cells. We propose that RV infection of IEC releases MV that modulate viral immunity.</description><identifier>ISSN: 0882-8245</identifier><identifier>EISSN: 1557-8976</identifier><identifier>DOI: 10.1089/vim.2009.0113</identifier><identifier>PMID: 21142445</identifier><language>eng</language><publisher>United States: Mary Ann Liebert, Inc</publisher><subject>Adaptive Immunity ; Antigens, CD - metabolism ; Antigens, Viral - metabolism ; Blotting, Western ; Caco-2 Cells ; Capsid Proteins - metabolism ; CD4-Positive T-Lymphocytes - immunology ; Child, Preschool ; Epithelial cells ; Epitopes - immunology ; Epitopes - ultrastructure ; Exosomes - immunology ; Exosomes - metabolism ; Female ; Gastroenteritis - immunology ; Gastroenteritis - metabolism ; Gastroenteritis - virology ; Health aspects ; Heat-Shock Proteins - immunology ; Heat-Shock Proteins - metabolism ; Humans ; Immune response ; Immunity, Cellular ; Infant ; Intestinal Mucosa - virology ; Male ; Microscopy, Electron, Transmission ; Microscopy, Fluorescence ; Physiological aspects ; Platelet Membrane Glycoproteins - metabolism ; Rotavirus ; Rotavirus Infections - immunology ; Rotaviruses ; T cells ; Tetraspanin 30 ; Transforming Growth Factor beta1 - immunology ; Transforming Growth Factor beta1 - metabolism</subject><ispartof>Viral immunology, 2010-12, Vol.23 (6), p.595-608</ispartof><rights>2010, Mary Ann Liebert, Inc.</rights><rights>COPYRIGHT 2010 Mary Ann Liebert, Inc.</rights><rights>(©) Copyright 2010, Mary Ann Liebert, Inc.</rights><rights>Copyright 2010, Mary Ann Liebert, Inc. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c556t-3cdf177bf03ba27a355c3aec3161ed5fbb01e71ec9d12a4592bb0c29ee1c785d3</citedby><cites>FETCH-LOGICAL-c556t-3cdf177bf03ba27a355c3aec3161ed5fbb01e71ec9d12a4592bb0c29ee1c785d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21142445$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barreto, Alfonso</creatorcontrib><creatorcontrib>Rodríguez, Luz-Stella</creatorcontrib><creatorcontrib>Rojas, Olga Lucía</creatorcontrib><creatorcontrib>Wolf, Marie</creatorcontrib><creatorcontrib>Greenberg, Harry B.</creatorcontrib><creatorcontrib>Franco, Manuel A.</creatorcontrib><creatorcontrib>Angel, Juana</creatorcontrib><title>Membrane Vesicles Released by Intestinal Epithelial Cells Infected with Rotavirus Inhibit T-Cell Function</title><title>Viral immunology</title><addtitle>Viral Immunol</addtitle><description>Rotavirus (RV) predominantly replicates in intestinal epithelial cells (IEC), and “danger signals” released by these cells may modulate viral immunity. We have recently shown that human model IEC (Caco-2 cells) infected with rhesus-RV release a non-inflammatory group of immunomodulators that includes heat shock proteins (HSPs) and TGF-β1. Here we show that both proteins are released in part in association with membrane vesicles (MV) obtained from filtrated Caco-2 supernatants concentrated by ultracentrifugation. These MV express markers of exosomes (CD63 and others), but not of the endoplasmic reticulum (ER) or nuclei. Larger quantities of proteins associated with MV were released by RV-infected cells than by non-infected cells. VP6 co-immunoprecipitated with CD63 present in these MV, and VP6 co-localized with CD63 in RV-infected cells, suggesting that this viral protein is associated with the MV, and that this association occurs intracellularly. CD63 present in MV preparations from stool samples from 36 children with gastroenteritis due or not due to RV were analyzed. VP6 co-immunoprecipitated with CD63 in 3/8 stool samples from RV-infected children, suggesting that these MV are released by RV-infected cells
in vivo
. Moreover, fractions that contained MV from RV-infected cells induced death and inhibited proliferation of CD4
+
T cells to a greater extent than fractions from non-infected cells. These effects were in part due to TGF-β, because they were reversed by treatment of the T cells with the TGF-β-receptor inhibitor ALK5i. MV from RV-infected and non-infected cells were heterogeneous, with morphologies and typical flotation densities described for exosomes (between 1.10 and 1.18 g/mL), and denser vesicles (>1.24 g/mL). Both types of MV from RV-infected cells were more efficient at inhibiting T-cell function than were those from non-infected cells. We propose that RV infection of IEC releases MV that modulate viral immunity.</description><subject>Adaptive Immunity</subject><subject>Antigens, CD - metabolism</subject><subject>Antigens, Viral - metabolism</subject><subject>Blotting, Western</subject><subject>Caco-2 Cells</subject><subject>Capsid Proteins - metabolism</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>Child, Preschool</subject><subject>Epithelial cells</subject><subject>Epitopes - immunology</subject><subject>Epitopes - ultrastructure</subject><subject>Exosomes - immunology</subject><subject>Exosomes - metabolism</subject><subject>Female</subject><subject>Gastroenteritis - immunology</subject><subject>Gastroenteritis - metabolism</subject><subject>Gastroenteritis - virology</subject><subject>Health aspects</subject><subject>Heat-Shock Proteins - immunology</subject><subject>Heat-Shock Proteins - metabolism</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immunity, Cellular</subject><subject>Infant</subject><subject>Intestinal Mucosa - virology</subject><subject>Male</subject><subject>Microscopy, Electron, Transmission</subject><subject>Microscopy, Fluorescence</subject><subject>Physiological aspects</subject><subject>Platelet Membrane Glycoproteins - metabolism</subject><subject>Rotavirus</subject><subject>Rotavirus Infections - immunology</subject><subject>Rotaviruses</subject><subject>T cells</subject><subject>Tetraspanin 30</subject><subject>Transforming Growth Factor beta1 - immunology</subject><subject>Transforming Growth Factor beta1 - metabolism</subject><issn>0882-8245</issn><issn>1557-8976</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFks9rFDEUx4Modq0evcpgD55mzc-ZzEUoS6uFilCq15DJvOmmzGTWJLPS_943bC1WhJJDwnuffMn75kvIW0bXjOrm496Pa05ps6aMiWdkxZSqS93U1XOyolrzUnOpjsirlG4ppbrS4iU54oxJLqVaEf8VxjbaAMUPSN4NkIorGMAm6Ir2rrgIGVL2wQ7F2c7nLQwejxsYhoS9HlxG7hc2iqsp272P81Lf-tbn4rpcuOJ8Di77KbwmL3o7JHhzvx-T7-dn15sv5eW3zxeb08vSKVXlUriuZ3Xd9lS0ltdWKOWEBSdYxaBTfdtSBjUD13SMW6kajhXHGwDmaq06cUw-HXR3cztC5yDkaAezi3608c5M1pvHneC35mbaG6kYo3WDAh_uBeL0c8bxzeiTw1HQpWlORstaSsZF_TTJmUTHtUTy_T_k7TRHtBUhVknRyGqROzlAN3YA40M_4fvcImlO8RMF5UpSpNb_oXB1MHo3Beg91h9dKA8XXJxSitA_eMGoWTJkMENmyZBZMoT8u78NfKD_hAYBcQCWsg1h8NBCzE_I_gYvltN7</recordid><startdate>20101201</startdate><enddate>20101201</enddate><creator>Barreto, Alfonso</creator><creator>Rodríguez, Luz-Stella</creator><creator>Rojas, Olga Lucía</creator><creator>Wolf, Marie</creator><creator>Greenberg, Harry B.</creator><creator>Franco, Manuel A.</creator><creator>Angel, Juana</creator><general>Mary Ann Liebert, Inc</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>7T5</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8C1</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>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20101201</creationdate><title>Membrane Vesicles Released by Intestinal Epithelial Cells Infected with Rotavirus Inhibit T-Cell Function</title><author>Barreto, Alfonso ; Rodríguez, Luz-Stella ; Rojas, Olga Lucía ; Wolf, Marie ; Greenberg, Harry B. ; Franco, Manuel A. ; Angel, Juana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c556t-3cdf177bf03ba27a355c3aec3161ed5fbb01e71ec9d12a4592bb0c29ee1c785d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adaptive Immunity</topic><topic>Antigens, CD - metabolism</topic><topic>Antigens, Viral - metabolism</topic><topic>Blotting, Western</topic><topic>Caco-2 Cells</topic><topic>Capsid Proteins - metabolism</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>Child, Preschool</topic><topic>Epithelial cells</topic><topic>Epitopes - immunology</topic><topic>Epitopes - ultrastructure</topic><topic>Exosomes - immunology</topic><topic>Exosomes - metabolism</topic><topic>Female</topic><topic>Gastroenteritis - immunology</topic><topic>Gastroenteritis - metabolism</topic><topic>Gastroenteritis - virology</topic><topic>Health aspects</topic><topic>Heat-Shock Proteins - immunology</topic><topic>Heat-Shock Proteins - metabolism</topic><topic>Humans</topic><topic>Immune response</topic><topic>Immunity, Cellular</topic><topic>Infant</topic><topic>Intestinal Mucosa - virology</topic><topic>Male</topic><topic>Microscopy, Electron, Transmission</topic><topic>Microscopy, Fluorescence</topic><topic>Physiological aspects</topic><topic>Platelet Membrane Glycoproteins - metabolism</topic><topic>Rotavirus</topic><topic>Rotavirus Infections - immunology</topic><topic>Rotaviruses</topic><topic>T cells</topic><topic>Tetraspanin 30</topic><topic>Transforming Growth Factor beta1 - immunology</topic><topic>Transforming Growth Factor beta1 - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barreto, Alfonso</creatorcontrib><creatorcontrib>Rodríguez, Luz-Stella</creatorcontrib><creatorcontrib>Rojas, Olga Lucía</creatorcontrib><creatorcontrib>Wolf, Marie</creatorcontrib><creatorcontrib>Greenberg, Harry B.</creatorcontrib><creatorcontrib>Franco, Manuel A.</creatorcontrib><creatorcontrib>Angel, Juana</creatorcontrib><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>Immunology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Public Health Database</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</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>AIDS and Cancer Research Abstracts</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>Biological Science 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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Viral immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barreto, Alfonso</au><au>Rodríguez, Luz-Stella</au><au>Rojas, Olga Lucía</au><au>Wolf, Marie</au><au>Greenberg, Harry B.</au><au>Franco, Manuel A.</au><au>Angel, Juana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Membrane Vesicles Released by Intestinal Epithelial Cells Infected with Rotavirus Inhibit T-Cell Function</atitle><jtitle>Viral immunology</jtitle><addtitle>Viral Immunol</addtitle><date>2010-12-01</date><risdate>2010</risdate><volume>23</volume><issue>6</issue><spage>595</spage><epage>608</epage><pages>595-608</pages><issn>0882-8245</issn><eissn>1557-8976</eissn><abstract>Rotavirus (RV) predominantly replicates in intestinal epithelial cells (IEC), and “danger signals” released by these cells may modulate viral immunity. We have recently shown that human model IEC (Caco-2 cells) infected with rhesus-RV release a non-inflammatory group of immunomodulators that includes heat shock proteins (HSPs) and TGF-β1. Here we show that both proteins are released in part in association with membrane vesicles (MV) obtained from filtrated Caco-2 supernatants concentrated by ultracentrifugation. These MV express markers of exosomes (CD63 and others), but not of the endoplasmic reticulum (ER) or nuclei. Larger quantities of proteins associated with MV were released by RV-infected cells than by non-infected cells. VP6 co-immunoprecipitated with CD63 present in these MV, and VP6 co-localized with CD63 in RV-infected cells, suggesting that this viral protein is associated with the MV, and that this association occurs intracellularly. CD63 present in MV preparations from stool samples from 36 children with gastroenteritis due or not due to RV were analyzed. VP6 co-immunoprecipitated with CD63 in 3/8 stool samples from RV-infected children, suggesting that these MV are released by RV-infected cells
in vivo
. Moreover, fractions that contained MV from RV-infected cells induced death and inhibited proliferation of CD4
+
T cells to a greater extent than fractions from non-infected cells. These effects were in part due to TGF-β, because they were reversed by treatment of the T cells with the TGF-β-receptor inhibitor ALK5i. MV from RV-infected and non-infected cells were heterogeneous, with morphologies and typical flotation densities described for exosomes (between 1.10 and 1.18 g/mL), and denser vesicles (>1.24 g/mL). Both types of MV from RV-infected cells were more efficient at inhibiting T-cell function than were those from non-infected cells. We propose that RV infection of IEC releases MV that modulate viral immunity.</abstract><cop>United States</cop><pub>Mary Ann Liebert, Inc</pub><pmid>21142445</pmid><doi>10.1089/vim.2009.0113</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
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| ispartof | Viral immunology, 2010-12, Vol.23 (6), p.595-608 |
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| source | MEDLINE; Alma/SFX Local Collection |
| subjects | Adaptive Immunity Antigens, CD - metabolism Antigens, Viral - metabolism Blotting, Western Caco-2 Cells Capsid Proteins - metabolism CD4-Positive T-Lymphocytes - immunology Child, Preschool Epithelial cells Epitopes - immunology Epitopes - ultrastructure Exosomes - immunology Exosomes - metabolism Female Gastroenteritis - immunology Gastroenteritis - metabolism Gastroenteritis - virology Health aspects Heat-Shock Proteins - immunology Heat-Shock Proteins - metabolism Humans Immune response Immunity, Cellular Infant Intestinal Mucosa - virology Male Microscopy, Electron, Transmission Microscopy, Fluorescence Physiological aspects Platelet Membrane Glycoproteins - metabolism Rotavirus Rotavirus Infections - immunology Rotaviruses T cells Tetraspanin 30 Transforming Growth Factor beta1 - immunology Transforming Growth Factor beta1 - metabolism |
| title | Membrane Vesicles Released by Intestinal Epithelial Cells Infected with Rotavirus Inhibit T-Cell Function |
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