Oral administration of a recombinant cholera toxin B subunit promotes mucosal healing in the colon
Cholera toxin B subunit (CTB) is a component of a licensed oral cholera vaccine. However, CTB has pleiotropic immunomodulatory effects whose impacts on the gut are not fully understood. Here, we found that oral administration in mice of a plant-made recombinant CTB (CTBp) significantly increased sev...
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| Veröffentlicht in: | Mucosal immunology 2017-07, Vol.10 (4), p.887-900 |
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| creator | Baldauf, K J Royal, J M Kouokam, J C Haribabu, B Jala, V R Yaddanapudi, K Hamorsky, K T Dryden, G W Matoba, N |
| description | Cholera toxin B subunit (CTB) is a component of a licensed oral cholera vaccine. However, CTB has pleiotropic immunomodulatory effects whose impacts on the gut are not fully understood. Here, we found that oral administration in mice of a plant-made recombinant CTB (CTBp) significantly increased several immune cell populations in the colon lamina propria. Global gene expression analysis revealed that CTBp had more pronounced impacts on the colon than the small intestine, with significant activation of TGFβ-mediated pathways in the colon epithelium. The clinical relevance of CTBp-induced impacts on colonic mucosa was examined. In a human colon epithelial model using Caco2 cells, CTBp, but not the non-GM1-binding mutant G33D-CTBp, induced TGFβ-mediated wound healing. In a dextran sodium sulfate (DSS) acute colitis mouse model, oral administration of CTBp protected against colon mucosal damage as manifested by mitigated body weight loss, decreased histopathological scores, and blunted escalation of inflammatory cytokine levels while inducing wound healing-related genes. Furthermore, biweekly oral administration of CTBp significantly reduced disease severity and tumorigenesis in the azoxymethane/DSS model of ulcerative colitis and colon cancer. Altogether, these results demonstrate CTBp’s ability to enhance mucosal healing in the colon, highlighting its potential application in ulcerative colitis therapy besides cholera vaccination. |
| doi_str_mv | 10.1038/mi.2016.95 |
| format | Article |
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However, CTB has pleiotropic immunomodulatory effects whose impacts on the gut are not fully understood. Here, we found that oral administration in mice of a plant-made recombinant CTB (CTBp) significantly increased several immune cell populations in the colon lamina propria. Global gene expression analysis revealed that CTBp had more pronounced impacts on the colon than the small intestine, with significant activation of TGFβ-mediated pathways in the colon epithelium. The clinical relevance of CTBp-induced impacts on colonic mucosa was examined. In a human colon epithelial model using Caco2 cells, CTBp, but not the non-GM1-binding mutant G33D-CTBp, induced TGFβ-mediated wound healing. In a dextran sodium sulfate (DSS) acute colitis mouse model, oral administration of CTBp protected against colon mucosal damage as manifested by mitigated body weight loss, decreased histopathological scores, and blunted escalation of inflammatory cytokine levels while inducing wound healing-related genes. Furthermore, biweekly oral administration of CTBp significantly reduced disease severity and tumorigenesis in the azoxymethane/DSS model of ulcerative colitis and colon cancer. Altogether, these results demonstrate CTBp’s ability to enhance mucosal healing in the colon, highlighting its potential application in ulcerative colitis therapy besides cholera vaccination.</description><identifier>ISSN: 1933-0219</identifier><identifier>EISSN: 1935-3456</identifier><identifier>DOI: 10.1038/mi.2016.95</identifier><identifier>PMID: 27805617</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/250/347 ; 631/61/51/1868 ; 692/699/249/2510/257/1389 ; 692/700/565 ; Administration, Oral ; Allergology ; Animals ; Antibodies ; Azoxymethane ; Biomedical and Life Sciences ; Biomedicine ; Body weight ; Body weight loss ; Caco-2 Cells ; Cholera ; Cholera - immunology ; Cholera - prevention & control ; Cholera toxin ; Cholera Toxin - immunology ; Cholera toxin B subunit ; Cholera Vaccines - immunology ; Colitis, Ulcerative - chemically induced ; Colitis, Ulcerative - complications ; Colitis, Ulcerative - immunology ; Colon ; Colon - pathology ; Colon cancer ; Colonic Neoplasms - etiology ; Colonic Neoplasms - immunology ; Colonic Neoplasms - prevention & control ; Colorectal cancer ; Dextran ; Dextran Sulfate ; Disease Models, Animal ; Epithelium ; Female ; Gastroenterology ; Gene expression ; Humans ; Immunology ; Immunomodulation ; Inflammatory bowel disease ; Inflammatory bowel diseases ; Lamina propria ; Mice ; Mice, Inbred C57BL ; Mucosa ; Mucous Membrane - immunology ; Oral administration ; Quorum sensing ; Rodents ; Signal Transduction ; Small intestine ; Sodium sulfate ; Transforming Growth Factor beta - metabolism ; Tumorigenesis ; Ulcerative colitis ; Vaccination ; Wound Healing</subject><ispartof>Mucosal immunology, 2017-07, Vol.10 (4), p.887-900</ispartof><rights>Society for Mucosal Immunology 2017</rights><rights>Copyright Nature Publishing Group Jul 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c453t-be7118b29580270e44f3479e5f0837bcc911cc6e9e4de45a6406dfd7b9402d063</citedby><cites>FETCH-LOGICAL-c453t-be7118b29580270e44f3479e5f0837bcc911cc6e9e4de45a6406dfd7b9402d063</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27805617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Baldauf, K J</creatorcontrib><creatorcontrib>Royal, J M</creatorcontrib><creatorcontrib>Kouokam, J C</creatorcontrib><creatorcontrib>Haribabu, B</creatorcontrib><creatorcontrib>Jala, V R</creatorcontrib><creatorcontrib>Yaddanapudi, K</creatorcontrib><creatorcontrib>Hamorsky, K T</creatorcontrib><creatorcontrib>Dryden, G W</creatorcontrib><creatorcontrib>Matoba, N</creatorcontrib><title>Oral administration of a recombinant cholera toxin B subunit promotes mucosal healing in the colon</title><title>Mucosal immunology</title><addtitle>Mucosal Immunol</addtitle><addtitle>Mucosal Immunol</addtitle><description>Cholera toxin B subunit (CTB) is a component of a licensed oral cholera vaccine. However, CTB has pleiotropic immunomodulatory effects whose impacts on the gut are not fully understood. Here, we found that oral administration in mice of a plant-made recombinant CTB (CTBp) significantly increased several immune cell populations in the colon lamina propria. Global gene expression analysis revealed that CTBp had more pronounced impacts on the colon than the small intestine, with significant activation of TGFβ-mediated pathways in the colon epithelium. The clinical relevance of CTBp-induced impacts on colonic mucosa was examined. In a human colon epithelial model using Caco2 cells, CTBp, but not the non-GM1-binding mutant G33D-CTBp, induced TGFβ-mediated wound healing. In a dextran sodium sulfate (DSS) acute colitis mouse model, oral administration of CTBp protected against colon mucosal damage as manifested by mitigated body weight loss, decreased histopathological scores, and blunted escalation of inflammatory cytokine levels while inducing wound healing-related genes. Furthermore, biweekly oral administration of CTBp significantly reduced disease severity and tumorigenesis in the azoxymethane/DSS model of ulcerative colitis and colon cancer. Altogether, these results demonstrate CTBp’s ability to enhance mucosal healing in the colon, highlighting its potential application in ulcerative colitis therapy besides cholera vaccination.</description><subject>631/250/347</subject><subject>631/61/51/1868</subject><subject>692/699/249/2510/257/1389</subject><subject>692/700/565</subject><subject>Administration, Oral</subject><subject>Allergology</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Azoxymethane</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Body weight</subject><subject>Body weight loss</subject><subject>Caco-2 Cells</subject><subject>Cholera</subject><subject>Cholera - immunology</subject><subject>Cholera - prevention & control</subject><subject>Cholera toxin</subject><subject>Cholera Toxin - immunology</subject><subject>Cholera toxin B subunit</subject><subject>Cholera Vaccines - immunology</subject><subject>Colitis, Ulcerative - chemically induced</subject><subject>Colitis, Ulcerative - complications</subject><subject>Colitis, Ulcerative - immunology</subject><subject>Colon</subject><subject>Colon - pathology</subject><subject>Colon cancer</subject><subject>Colonic Neoplasms - etiology</subject><subject>Colonic Neoplasms - immunology</subject><subject>Colonic Neoplasms - prevention & control</subject><subject>Colorectal cancer</subject><subject>Dextran</subject><subject>Dextran Sulfate</subject><subject>Disease Models, Animal</subject><subject>Epithelium</subject><subject>Female</subject><subject>Gastroenterology</subject><subject>Gene expression</subject><subject>Humans</subject><subject>Immunology</subject><subject>Immunomodulation</subject><subject>Inflammatory bowel disease</subject><subject>Inflammatory bowel diseases</subject><subject>Lamina propria</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mucosa</subject><subject>Mucous Membrane - immunology</subject><subject>Oral administration</subject><subject>Quorum sensing</subject><subject>Rodents</subject><subject>Signal Transduction</subject><subject>Small intestine</subject><subject>Sodium sulfate</subject><subject>Transforming Growth Factor beta - metabolism</subject><subject>Tumorigenesis</subject><subject>Ulcerative colitis</subject><subject>Vaccination</subject><subject>Wound Healing</subject><issn>1933-0219</issn><issn>1935-3456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNplkE1LAzEURYMo1q-NP0AC7pSpySSZmSy1-AVCN7oOSSbTpswkNcmA_ntTW0Vw9R68w72PA8A5RlOMSHMz2GmJcDXlbA8cYU5YQSir9r93UqAS8wk4jnGFUIUQI4dgUtYNYhWuj4CaB9lD2Q7W2ZiCTNY76DsoYTDaD8o66RLUS9-bIGHyH9bBOxhHNTqb4Dr4wScT4TBqH3PQ0sjeugXMVFoaqH3v3Sk46GQfzdlunoC3h_vX2VPxMn98nt2-FJoykgplaowbVXLWoLJGhtKO0Job1qGG1EprjrHWleGGtoYyWVFUtV1bK05R2aKKnIDLbW7-6n00MYmVH4PLlQLzLAqTuiGZutpSOvgYg-nEOthBhk-BkdjoFIMVG52Cswxf7CJHNZj2F_3xl4HrLRDzyS1M-NP5P-4Lt25-bA</recordid><startdate>20170701</startdate><enddate>20170701</enddate><creator>Baldauf, K J</creator><creator>Royal, J M</creator><creator>Kouokam, J C</creator><creator>Haribabu, B</creator><creator>Jala, V R</creator><creator>Yaddanapudi, K</creator><creator>Hamorsky, K T</creator><creator>Dryden, G W</creator><creator>Matoba, N</creator><general>Nature Publishing Group US</general><general>Elsevier Limited</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>7X7</scope><scope>7XB</scope><scope>88E</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>PRINS</scope></search><sort><creationdate>20170701</creationdate><title>Oral administration of a recombinant cholera toxin B subunit promotes mucosal healing in the colon</title><author>Baldauf, K J ; Royal, J M ; Kouokam, J C ; Haribabu, B ; Jala, V R ; Yaddanapudi, K ; Hamorsky, K T ; Dryden, G W ; Matoba, N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c453t-be7118b29580270e44f3479e5f0837bcc911cc6e9e4de45a6406dfd7b9402d063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>631/250/347</topic><topic>631/61/51/1868</topic><topic>692/699/249/2510/257/1389</topic><topic>692/700/565</topic><topic>Administration, Oral</topic><topic>Allergology</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Azoxymethane</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Body weight</topic><topic>Body weight loss</topic><topic>Caco-2 Cells</topic><topic>Cholera</topic><topic>Cholera - 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immunology</topic><topic>Oral administration</topic><topic>Quorum sensing</topic><topic>Rodents</topic><topic>Signal Transduction</topic><topic>Small intestine</topic><topic>Sodium sulfate</topic><topic>Transforming Growth Factor beta - metabolism</topic><topic>Tumorigenesis</topic><topic>Ulcerative colitis</topic><topic>Vaccination</topic><topic>Wound Healing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Baldauf, K J</creatorcontrib><creatorcontrib>Royal, J M</creatorcontrib><creatorcontrib>Kouokam, J C</creatorcontrib><creatorcontrib>Haribabu, B</creatorcontrib><creatorcontrib>Jala, V R</creatorcontrib><creatorcontrib>Yaddanapudi, K</creatorcontrib><creatorcontrib>Hamorsky, K T</creatorcontrib><creatorcontrib>Dryden, G W</creatorcontrib><creatorcontrib>Matoba, N</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>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical 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</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>ProQuest Central China</collection><jtitle>Mucosal immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Baldauf, K J</au><au>Royal, J M</au><au>Kouokam, J C</au><au>Haribabu, B</au><au>Jala, V R</au><au>Yaddanapudi, K</au><au>Hamorsky, K T</au><au>Dryden, G W</au><au>Matoba, N</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oral administration of a recombinant cholera toxin B subunit promotes mucosal healing in the colon</atitle><jtitle>Mucosal immunology</jtitle><stitle>Mucosal Immunol</stitle><addtitle>Mucosal Immunol</addtitle><date>2017-07-01</date><risdate>2017</risdate><volume>10</volume><issue>4</issue><spage>887</spage><epage>900</epage><pages>887-900</pages><issn>1933-0219</issn><eissn>1935-3456</eissn><abstract>Cholera toxin B subunit (CTB) is a component of a licensed oral cholera vaccine. However, CTB has pleiotropic immunomodulatory effects whose impacts on the gut are not fully understood. Here, we found that oral administration in mice of a plant-made recombinant CTB (CTBp) significantly increased several immune cell populations in the colon lamina propria. Global gene expression analysis revealed that CTBp had more pronounced impacts on the colon than the small intestine, with significant activation of TGFβ-mediated pathways in the colon epithelium. The clinical relevance of CTBp-induced impacts on colonic mucosa was examined. In a human colon epithelial model using Caco2 cells, CTBp, but not the non-GM1-binding mutant G33D-CTBp, induced TGFβ-mediated wound healing. In a dextran sodium sulfate (DSS) acute colitis mouse model, oral administration of CTBp protected against colon mucosal damage as manifested by mitigated body weight loss, decreased histopathological scores, and blunted escalation of inflammatory cytokine levels while inducing wound healing-related genes. Furthermore, biweekly oral administration of CTBp significantly reduced disease severity and tumorigenesis in the azoxymethane/DSS model of ulcerative colitis and colon cancer. Altogether, these results demonstrate CTBp’s ability to enhance mucosal healing in the colon, highlighting its potential application in ulcerative colitis therapy besides cholera vaccination.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>27805617</pmid><doi>10.1038/mi.2016.95</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 631/250/347 631/61/51/1868 692/699/249/2510/257/1389 692/700/565 Administration, Oral Allergology Animals Antibodies Azoxymethane Biomedical and Life Sciences Biomedicine Body weight Body weight loss Caco-2 Cells Cholera Cholera - immunology Cholera - prevention & control Cholera toxin Cholera Toxin - immunology Cholera toxin B subunit Cholera Vaccines - immunology Colitis, Ulcerative - chemically induced Colitis, Ulcerative - complications Colitis, Ulcerative - immunology Colon Colon - pathology Colon cancer Colonic Neoplasms - etiology Colonic Neoplasms - immunology Colonic Neoplasms - prevention & control Colorectal cancer Dextran Dextran Sulfate Disease Models, Animal Epithelium Female Gastroenterology Gene expression Humans Immunology Immunomodulation Inflammatory bowel disease Inflammatory bowel diseases Lamina propria Mice Mice, Inbred C57BL Mucosa Mucous Membrane - immunology Oral administration Quorum sensing Rodents Signal Transduction Small intestine Sodium sulfate Transforming Growth Factor beta - metabolism Tumorigenesis Ulcerative colitis Vaccination Wound Healing |
| title | Oral administration of a recombinant cholera toxin B subunit promotes mucosal healing in the colon |
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