Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens
The objective of the present study was to assess the effect of alginate-encapsulated infectious pancreatic necrosis virus antigens in inducing the immune response of Atlantic salmon as booster vaccines. One year after intraperitoneal injection with an oil-adjuvanted vaccine, post-smolts were orally...
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| Veröffentlicht in: | PloS one 2014-10, Vol.9 (10), p.e109337-e109337 |
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| creator | Chen, Lihan Klaric, Goran Wadsworth, Simon Jayasinghe, Suwan Kuo, Tsun-Yung Evensen, Øystein Mutoloki, Stephen |
| description | The objective of the present study was to assess the effect of alginate-encapsulated infectious pancreatic necrosis virus antigens in inducing the immune response of Atlantic salmon as booster vaccines. One year after intraperitoneal injection with an oil-adjuvanted vaccine, post-smolts were orally boosted either by 1) alginate-encapsulated IPNV antigens (ENCAP); 2) soluble antigens (UNENCAP) or 3) untreated feed (control). This was done twice, seven weeks apart. Sampling was done twice, firstly at 7 weeks post 1st oral boost and the 2nd, at 4 weeks after the 2nd oral boost. Samples included serum, head kidney, spleen and hindgut. Serum antibodies were analyzed by ELISA while tissues were used to assess the expression of IgM, IgT, CD4, GATA3, FOXP3, TGF-β and IL-10 genes by quantitative PCR. Compared to controls, fish fed with ENCAP had a significant increase (p |
| doi_str_mv | 10.1371/journal.pone.0109337 |
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One year after intraperitoneal injection with an oil-adjuvanted vaccine, post-smolts were orally boosted either by 1) alginate-encapsulated IPNV antigens (ENCAP); 2) soluble antigens (UNENCAP) or 3) untreated feed (control). This was done twice, seven weeks apart. Sampling was done twice, firstly at 7 weeks post 1st oral boost and the 2nd, at 4 weeks after the 2nd oral boost. Samples included serum, head kidney, spleen and hindgut. Serum antibodies were analyzed by ELISA while tissues were used to assess the expression of IgM, IgT, CD4, GATA3, FOXP3, TGF-β and IL-10 genes by quantitative PCR. Compared to controls, fish fed with ENCAP had a significant increase (p<0.04) in serum antibodies following the 1st boost but not after the 2nd boost. This coincided with significant up-regulation of CD4 and GATA3 genes. In contrast, serum antibodies in the UNENCAP group decreased both after the 1st and 2nd oral boosts. This was associated with significant up-regulation of FOXP3, TGF-β and IL-10 genes. The expression of IgT was not induced in the hindgut after the 1st oral boost but was significantly up-regulated following the 2nd one. CD4 and GATA3 mRNA expressions exhibited a similar pattern to IgT in the hindgut. IgM mRNA expression on the other hand was not differentially regulated at any of the times examined. Our findings suggest that 1) Parenteral prime with oil-adjuvanted vaccines followed by oral boost with ENCAP results in augmentation of the systemic immune response; 2) Symmetrical prime and boost (mucosal) with ENCAP results in augmentation of mucosal immune response and 3) Symmetrical priming and boosting (mucosal) with soluble antigens results in the induction of systemic immune tolerance.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0109337</identifier><identifier>PMID: 25310804</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alginates ; Alginic acid ; Analysis ; Animal tissues ; Animals ; Antibodies ; Antibody response ; Antigens ; Augmentation ; B cells ; Biology and Life Sciences ; Birnaviridae Infections - immunology ; Birnaviridae Infections - prevention & control ; Birnaviridae Infections - veterinary ; Bone morphogenetic proteins ; CD4 antigen ; Encapsulation ; Enzyme-linked immunosorbent assay ; Fish ; Fish Diseases - immunology ; Fish Diseases - prevention & control ; Fishes ; Foxp3 protein ; GATA-3 protein ; Gene expression ; Genes ; Glucuronic Acid ; Hexuronic Acids ; Hindgut ; Immune response ; Immune system ; Immunity, Active - immunology ; Immunity, Mucosal - immunology ; Immunoglobulin M ; Immunological tolerance ; Immunotherapy ; Infectious pancreatic necrosis ; Infectious pancreatic necrosis virus - immunology ; Interleukin 10 ; Kidneys ; Medicine and Health Sciences ; Mucosal immunity ; Oral administration ; Pancreas ; Priming ; RNA ; Salmo salar ; Salmo salar - immunology ; Salmon ; Spleen ; Transforming growth factors ; Vaccination ; Vaccines ; Viruses</subject><ispartof>PloS one, 2014-10, Vol.9 (10), p.e109337-e109337</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Chen 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>2014 Chen et al 2014 Chen et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-a3a48ec6381134d35ebed42742aadd8b6dd7ecd7f88571e2526bb36d8e18e0f03</citedby><cites>FETCH-LOGICAL-c692t-a3a48ec6381134d35ebed42742aadd8b6dd7ecd7f88571e2526bb36d8e18e0f03</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/PMC4195674/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4195674/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25310804$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Stewart, James P.</contributor><creatorcontrib>Chen, Lihan</creatorcontrib><creatorcontrib>Klaric, Goran</creatorcontrib><creatorcontrib>Wadsworth, Simon</creatorcontrib><creatorcontrib>Jayasinghe, Suwan</creatorcontrib><creatorcontrib>Kuo, Tsun-Yung</creatorcontrib><creatorcontrib>Evensen, Øystein</creatorcontrib><creatorcontrib>Mutoloki, Stephen</creatorcontrib><title>Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The objective of the present study was to assess the effect of alginate-encapsulated infectious pancreatic necrosis virus antigens in inducing the immune response of Atlantic salmon as booster vaccines. One year after intraperitoneal injection with an oil-adjuvanted vaccine, post-smolts were orally boosted either by 1) alginate-encapsulated IPNV antigens (ENCAP); 2) soluble antigens (UNENCAP) or 3) untreated feed (control). This was done twice, seven weeks apart. Sampling was done twice, firstly at 7 weeks post 1st oral boost and the 2nd, at 4 weeks after the 2nd oral boost. Samples included serum, head kidney, spleen and hindgut. Serum antibodies were analyzed by ELISA while tissues were used to assess the expression of IgM, IgT, CD4, GATA3, FOXP3, TGF-β and IL-10 genes by quantitative PCR. Compared to controls, fish fed with ENCAP had a significant increase (p<0.04) in serum antibodies following the 1st boost but not after the 2nd boost. This coincided with significant up-regulation of CD4 and GATA3 genes. In contrast, serum antibodies in the UNENCAP group decreased both after the 1st and 2nd oral boosts. This was associated with significant up-regulation of FOXP3, TGF-β and IL-10 genes. The expression of IgT was not induced in the hindgut after the 1st oral boost but was significantly up-regulated following the 2nd one. CD4 and GATA3 mRNA expressions exhibited a similar pattern to IgT in the hindgut. IgM mRNA expression on the other hand was not differentially regulated at any of the times examined. Our findings suggest that 1) Parenteral prime with oil-adjuvanted vaccines followed by oral boost with ENCAP results in augmentation of the systemic immune response; 2) Symmetrical prime and boost (mucosal) with ENCAP results in augmentation of mucosal immune response and 3) Symmetrical priming and boosting (mucosal) with soluble antigens results in the induction of systemic immune tolerance.</description><subject>Alginates</subject><subject>Alginic acid</subject><subject>Analysis</subject><subject>Animal tissues</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Antibody response</subject><subject>Antigens</subject><subject>Augmentation</subject><subject>B cells</subject><subject>Biology and Life Sciences</subject><subject>Birnaviridae Infections - immunology</subject><subject>Birnaviridae Infections - prevention & control</subject><subject>Birnaviridae Infections - veterinary</subject><subject>Bone morphogenetic proteins</subject><subject>CD4 antigen</subject><subject>Encapsulation</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Fish</subject><subject>Fish Diseases - immunology</subject><subject>Fish Diseases - prevention & control</subject><subject>Fishes</subject><subject>Foxp3 protein</subject><subject>GATA-3 protein</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Glucuronic Acid</subject><subject>Hexuronic Acids</subject><subject>Hindgut</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Active - immunology</subject><subject>Immunity, Mucosal - immunology</subject><subject>Immunoglobulin M</subject><subject>Immunological tolerance</subject><subject>Immunotherapy</subject><subject>Infectious pancreatic necrosis</subject><subject>Infectious pancreatic necrosis virus - immunology</subject><subject>Interleukin 10</subject><subject>Kidneys</subject><subject>Medicine and Health Sciences</subject><subject>Mucosal immunity</subject><subject>Oral administration</subject><subject>Pancreas</subject><subject>Priming</subject><subject>RNA</subject><subject>Salmo salar</subject><subject>Salmo salar - immunology</subject><subject>Salmon</subject><subject>Spleen</subject><subject>Transforming growth factors</subject><subject>Vaccination</subject><subject>Vaccines</subject><subject>Viruses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk02P0zAQhiMEYpeFf4AgEhKCQ4sdJ45zQapWfFRasYiPvVqTeJK6cuJu7Kzov8dps1WL9oByiDV-5p3xa08UvaRkTllOP6zt0Hdg5hvb4ZxQUjCWP4rOacGSGU8Ie3y0PoueObcmJGOC86fRWZIxSgRJz6O7xdC02Hnw2naxrWO_whg6r0urtnGPLsg7HDcW3ozxKnZg2sCW29j2YGJQre608_1BAkyjO_A4w66CjRtMWKt4-f3bzU65wc49j57UYBy-mP4X0e_Pn35dfp1dXX9ZXi6uZhUvEj8DBqnAijNBKUsVy7BElSZ5mgAoJUquVI6VymshspxikiW8LBlXAqlAUhN2Eb3e626MdXKyzEnKg19FknMaiOWeUBbWctPrFvqttKDlLmD7RkIfjm1Qkip0A7zElNGUgYAsEwUEL5nIaFomQevjVG0oW1RV8DU4dCJ6utPplWzsnUxpkfE8DQLvJoHe3g7ovGy1q9AE59EOu76TRISbHmu9-Qd9-HQT1UA4gO5qG-pWo6hcpFRkoXdWBGr-ABU-ha2uwvuqdYifJLw_SQiMxz--gcE5ufz54__Z65tT9u0Ru0IwfuWsGcaX5U7BdA9WvXWux_pgMiVyHI97N-Q4HnIaj5D26viCDkn388D-AlN1C2s</recordid><startdate>20141013</startdate><enddate>20141013</enddate><creator>Chen, Lihan</creator><creator>Klaric, Goran</creator><creator>Wadsworth, Simon</creator><creator>Jayasinghe, Suwan</creator><creator>Kuo, Tsun-Yung</creator><creator>Evensen, Øystein</creator><creator>Mutoloki, Stephen</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>IOV</scope><scope>ISR</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141013</creationdate><title>Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens</title><author>Chen, Lihan ; Klaric, Goran ; Wadsworth, Simon ; Jayasinghe, Suwan ; Kuo, Tsun-Yung ; Evensen, Øystein ; Mutoloki, Stephen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-a3a48ec6381134d35ebed42742aadd8b6dd7ecd7f88571e2526bb36d8e18e0f03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Alginates</topic><topic>Alginic acid</topic><topic>Analysis</topic><topic>Animal tissues</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Antibody response</topic><topic>Antigens</topic><topic>Augmentation</topic><topic>B cells</topic><topic>Biology and Life Sciences</topic><topic>Birnaviridae Infections - immunology</topic><topic>Birnaviridae Infections - prevention & control</topic><topic>Birnaviridae Infections - veterinary</topic><topic>Bone morphogenetic proteins</topic><topic>CD4 antigen</topic><topic>Encapsulation</topic><topic>Enzyme-linked immunosorbent assay</topic><topic>Fish</topic><topic>Fish Diseases - immunology</topic><topic>Fish Diseases - prevention & control</topic><topic>Fishes</topic><topic>Foxp3 protein</topic><topic>GATA-3 protein</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Glucuronic Acid</topic><topic>Hexuronic Acids</topic><topic>Hindgut</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity, Active - immunology</topic><topic>Immunity, Mucosal - immunology</topic><topic>Immunoglobulin M</topic><topic>Immunological tolerance</topic><topic>Immunotherapy</topic><topic>Infectious pancreatic necrosis</topic><topic>Infectious pancreatic necrosis virus - immunology</topic><topic>Interleukin 10</topic><topic>Kidneys</topic><topic>Medicine and Health Sciences</topic><topic>Mucosal immunity</topic><topic>Oral administration</topic><topic>Pancreas</topic><topic>Priming</topic><topic>RNA</topic><topic>Salmo salar</topic><topic>Salmo salar - 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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>Chen, Lihan</au><au>Klaric, Goran</au><au>Wadsworth, Simon</au><au>Jayasinghe, Suwan</au><au>Kuo, Tsun-Yung</au><au>Evensen, Øystein</au><au>Mutoloki, Stephen</au><au>Stewart, James P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-10-13</date><risdate>2014</risdate><volume>9</volume><issue>10</issue><spage>e109337</spage><epage>e109337</epage><pages>e109337-e109337</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The objective of the present study was to assess the effect of alginate-encapsulated infectious pancreatic necrosis virus antigens in inducing the immune response of Atlantic salmon as booster vaccines. One year after intraperitoneal injection with an oil-adjuvanted vaccine, post-smolts were orally boosted either by 1) alginate-encapsulated IPNV antigens (ENCAP); 2) soluble antigens (UNENCAP) or 3) untreated feed (control). This was done twice, seven weeks apart. Sampling was done twice, firstly at 7 weeks post 1st oral boost and the 2nd, at 4 weeks after the 2nd oral boost. Samples included serum, head kidney, spleen and hindgut. Serum antibodies were analyzed by ELISA while tissues were used to assess the expression of IgM, IgT, CD4, GATA3, FOXP3, TGF-β and IL-10 genes by quantitative PCR. Compared to controls, fish fed with ENCAP had a significant increase (p<0.04) in serum antibodies following the 1st boost but not after the 2nd boost. This coincided with significant up-regulation of CD4 and GATA3 genes. In contrast, serum antibodies in the UNENCAP group decreased both after the 1st and 2nd oral boosts. This was associated with significant up-regulation of FOXP3, TGF-β and IL-10 genes. The expression of IgT was not induced in the hindgut after the 1st oral boost but was significantly up-regulated following the 2nd one. CD4 and GATA3 mRNA expressions exhibited a similar pattern to IgT in the hindgut. IgM mRNA expression on the other hand was not differentially regulated at any of the times examined. Our findings suggest that 1) Parenteral prime with oil-adjuvanted vaccines followed by oral boost with ENCAP results in augmentation of the systemic immune response; 2) Symmetrical prime and boost (mucosal) with ENCAP results in augmentation of mucosal immune response and 3) Symmetrical priming and boosting (mucosal) with soluble antigens results in the induction of systemic immune tolerance.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25310804</pmid><doi>10.1371/journal.pone.0109337</doi><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Alginates Alginic acid Analysis Animal tissues Animals Antibodies Antibody response Antigens Augmentation B cells Biology and Life Sciences Birnaviridae Infections - immunology Birnaviridae Infections - prevention & control Birnaviridae Infections - veterinary Bone morphogenetic proteins CD4 antigen Encapsulation Enzyme-linked immunosorbent assay Fish Fish Diseases - immunology Fish Diseases - prevention & control Fishes Foxp3 protein GATA-3 protein Gene expression Genes Glucuronic Acid Hexuronic Acids Hindgut Immune response Immune system Immunity, Active - immunology Immunity, Mucosal - immunology Immunoglobulin M Immunological tolerance Immunotherapy Infectious pancreatic necrosis Infectious pancreatic necrosis virus - immunology Interleukin 10 Kidneys Medicine and Health Sciences Mucosal immunity Oral administration Pancreas Priming RNA Salmo salar Salmo salar - immunology Salmon Spleen Transforming growth factors Vaccination Vaccines Viruses |
| title | Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T02%3A19%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Augmentation%20of%20the%20antibody%20response%20of%20Atlantic%20salmon%20by%20oral%20administration%20of%20alginate-encapsulated%20IPNV%20antigens&rft.jtitle=PloS%20one&rft.au=Chen,%20Lihan&rft.date=2014-10-13&rft.volume=9&rft.issue=10&rft.spage=e109337&rft.epage=e109337&rft.pages=e109337-e109337&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0109337&rft_dat=%3Cgale_plos_%3EA418553339%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1610992761&rft_id=info:pmid/25310804&rft_galeid=A418553339&rft_doaj_id=oai_doaj_org_article_0ca48a6be43143a8a5589a25338514b2&rfr_iscdi=true |