Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin
Lactoferrin, a large multifunctional glycoprotein, is involved in many physiological functions but its immunomodulatory pathways are not well characterized in fish. The objective of the present study was to investigate the temporal effect of dietary bovine lactoferrin (BLf) at low (0.1%) and high (1...
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| Veröffentlicht in: | Fish & shellfish immunology 2017-12, Vol.71, p.359-371 |
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| creator | Khuyen, Trinh Dinh Mandiki, Syaghalirwa N.M. Cornet, Valérie Douxfils, Jessica Betoulle, Stéphane Bossier, Peter Reyes-López, Felipe E. Tort, Lluis Kestemont, Patrick |
| description | Lactoferrin, a large multifunctional glycoprotein, is involved in many physiological functions but its immunomodulatory pathways are not well characterized in fish. The objective of the present study was to investigate the temporal effect of dietary bovine lactoferrin (BLf) at low (0.1%) and high (1%) on immunological organs of rainbow trout juveniles. BLf diets did not affect specific growth rate, haematocrit, splenic index, spleen respiratory burst activity as well as humoral (mIgM) and neutrophils (MPO) gene expressions after short term - 35 days (D35) and long term nutrient test - 51 days (D51) of feeding. Both low and high BLf doses induced enhanced level of plasma alternative complement activity, plasma total immunoglobulin on D35 and D51, lymphocyte plus thrombocyte cell proportion on D35 and monocyte cell proportion in total blood leukocyte cells on D51. On D51 but not on D35, BLf diets upregulated the expression of inflammatory genes in kidney for il-1 at the low BLf dose, il-8 at both BLf doses and il-6 at the high BLf dose in spleen, and il-10 at both BLf doses in kidney. Moreover, the expression of T helper (cd4-2α; cd4-2β) genes was significantly upregulated only on D51 by both BLf doses in both spleen and kidney tissues. On D51, controls and BLf treated fish were intraperitoneally injected with A. salmonicida achromogenes. The expression of 13 immune genes was evaluated at 44 h post-injection (D54). The expression of lysozyme gene was upregulated by both BLf doses after bacterial infection both in spleen and kidney. The expression of mcsfrα (spleen) and tgf-β1 (kidney) was also modulated by both BLf doses. Low and high BLf doses enhanced disease resistance of rainbow trout juveniles with the cumulative survival rate of 36% and 38% respectively while those of the control was 19% after 14 days challenged with bacteria. The results indicate that BLf diets activated the humoral immunity, associated to blood leukocyte cells of rainbow trout after short term BLf administration, and the long term BLf administration was necessary for sensitizing other lymphoid organs such as in spleen and kidney. Only after long term test, BLf diets induced significantly higher levels of innate and adaptive immune gene expressions than those of the control. Dietary BLf activated more markedly the expression of innate immune genes than the adaptive ones; this upregulation of some immune genes could explain the high disease resistance observed in rainbow trout juvenile |
| doi_str_mv | 10.1016/j.fsi.2017.10.027 |
| format | Article |
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•BLf was positively affecting rainbow trout immune system in a time/dose dependant manner.•After short-term, BLf activated blood leukocyte cell and humoral responses.•After long-term, BLf diets increased pro-inflammatory gene expressions in spleen, kidney.•After bacterial challenge, BLf tends to provide a better protection against bacterial infection and survival.</description><identifier>ISSN: 1050-4648</identifier><identifier>EISSN: 1095-9947</identifier><identifier>DOI: 10.1016/j.fsi.2017.10.027</identifier><identifier>PMID: 29050988</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Administration, Oral ; Aeromonas salmonicida - physiology ; Animal Feed - analysis ; Animals ; Anti-Infective Agents - administration & dosage ; Anti-Infective Agents - pharmacology ; Bovine lactoferrin ; Diet - veterinary ; Disease resistance ; Disease Resistance - immunology ; Dose-Response Relationship, Immunologic ; Fish Diseases - immunology ; Gene Expression - immunology ; Gene Expression Profiling - veterinary ; Gene expressions ; Gram-Negative Bacterial Infections - immunology ; Gram-Negative Bacterial Infections - veterinary ; Immunity ; Immunity, Humoral ; Lactoferrin - administration & dosage ; Lactoferrin - pharmacology ; Leukocytes - immunology ; Oncorhynchus mykiss - genetics ; Oncorhynchus mykiss - growth & development ; Oncorhynchus mykiss - immunology ; Rainbow trout (Oncorhynchus mykiss) ; Time Factors</subject><ispartof>Fish & shellfish immunology, 2017-12, Vol.71, p.359-371</ispartof><rights>2017 Elsevier Ltd</rights><rights>Copyright © 2017 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c419t-94704452a3cda6ff409b445b6479510124aef62c24a3b972d509766dd251f2423</citedby><cites>FETCH-LOGICAL-c419t-94704452a3cda6ff409b445b6479510124aef62c24a3b972d509766dd251f2423</cites><orcidid>0000-0003-0066-669X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1050464817306332$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29050988$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Khuyen, Trinh Dinh</creatorcontrib><creatorcontrib>Mandiki, Syaghalirwa N.M.</creatorcontrib><creatorcontrib>Cornet, Valérie</creatorcontrib><creatorcontrib>Douxfils, Jessica</creatorcontrib><creatorcontrib>Betoulle, Stéphane</creatorcontrib><creatorcontrib>Bossier, Peter</creatorcontrib><creatorcontrib>Reyes-López, Felipe E.</creatorcontrib><creatorcontrib>Tort, Lluis</creatorcontrib><creatorcontrib>Kestemont, Patrick</creatorcontrib><title>Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin</title><title>Fish & shellfish immunology</title><addtitle>Fish Shellfish Immunol</addtitle><description>Lactoferrin, a large multifunctional glycoprotein, is involved in many physiological functions but its immunomodulatory pathways are not well characterized in fish. The objective of the present study was to investigate the temporal effect of dietary bovine lactoferrin (BLf) at low (0.1%) and high (1%) on immunological organs of rainbow trout juveniles. BLf diets did not affect specific growth rate, haematocrit, splenic index, spleen respiratory burst activity as well as humoral (mIgM) and neutrophils (MPO) gene expressions after short term - 35 days (D35) and long term nutrient test - 51 days (D51) of feeding. Both low and high BLf doses induced enhanced level of plasma alternative complement activity, plasma total immunoglobulin on D35 and D51, lymphocyte plus thrombocyte cell proportion on D35 and monocyte cell proportion in total blood leukocyte cells on D51. On D51 but not on D35, BLf diets upregulated the expression of inflammatory genes in kidney for il-1 at the low BLf dose, il-8 at both BLf doses and il-6 at the high BLf dose in spleen, and il-10 at both BLf doses in kidney. Moreover, the expression of T helper (cd4-2α; cd4-2β) genes was significantly upregulated only on D51 by both BLf doses in both spleen and kidney tissues. On D51, controls and BLf treated fish were intraperitoneally injected with A. salmonicida achromogenes. The expression of 13 immune genes was evaluated at 44 h post-injection (D54). The expression of lysozyme gene was upregulated by both BLf doses after bacterial infection both in spleen and kidney. The expression of mcsfrα (spleen) and tgf-β1 (kidney) was also modulated by both BLf doses. Low and high BLf doses enhanced disease resistance of rainbow trout juveniles with the cumulative survival rate of 36% and 38% respectively while those of the control was 19% after 14 days challenged with bacteria. The results indicate that BLf diets activated the humoral immunity, associated to blood leukocyte cells of rainbow trout after short term BLf administration, and the long term BLf administration was necessary for sensitizing other lymphoid organs such as in spleen and kidney. Only after long term test, BLf diets induced significantly higher levels of innate and adaptive immune gene expressions than those of the control. Dietary BLf activated more markedly the expression of innate immune genes than the adaptive ones; this upregulation of some immune genes could explain the high disease resistance observed in rainbow trout juveniles fed BLf.
•BLf was positively affecting rainbow trout immune system in a time/dose dependant manner.•After short-term, BLf activated blood leukocyte cell and humoral responses.•After long-term, BLf diets increased pro-inflammatory gene expressions in spleen, kidney.•After bacterial challenge, BLf tends to provide a better protection against bacterial infection and survival.</description><subject>Administration, Oral</subject><subject>Aeromonas salmonicida - physiology</subject><subject>Animal Feed - analysis</subject><subject>Animals</subject><subject>Anti-Infective Agents - administration & dosage</subject><subject>Anti-Infective Agents - pharmacology</subject><subject>Bovine lactoferrin</subject><subject>Diet - veterinary</subject><subject>Disease resistance</subject><subject>Disease Resistance - immunology</subject><subject>Dose-Response Relationship, Immunologic</subject><subject>Fish Diseases - immunology</subject><subject>Gene Expression - immunology</subject><subject>Gene Expression Profiling - veterinary</subject><subject>Gene expressions</subject><subject>Gram-Negative Bacterial Infections - immunology</subject><subject>Gram-Negative Bacterial Infections - veterinary</subject><subject>Immunity</subject><subject>Immunity, Humoral</subject><subject>Lactoferrin - administration & dosage</subject><subject>Lactoferrin - pharmacology</subject><subject>Leukocytes - immunology</subject><subject>Oncorhynchus mykiss - genetics</subject><subject>Oncorhynchus mykiss - growth & development</subject><subject>Oncorhynchus mykiss - immunology</subject><subject>Rainbow trout (Oncorhynchus mykiss)</subject><subject>Time Factors</subject><issn>1050-4648</issn><issn>1095-9947</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UD1PwzAUtBCIlsIPYEEeWVJs13FqMSHEl1QJBhiYLMd-BldJXOykqP8eVy2MTO_r7nTvEDqnZEoJFVfLqUt-ygit8jwlrDpAY0pkWUjJq8NtX5KCCz4foZOUloQQMRPkGI2YzBc5n4_R-8vnJvnQhA9vdIN1Z7Fv26EDHCGtQpcAB4eXwxo63-Sl9l0dvnEfw9DjPmDroddxg-uw9pnUaNMHBzH67hQdOd0kONvXCXq7v3u9fSwWzw9PtzeLwnAq-yI7JZyXTM-M1cI5TmSd51rwSpb5S8Y1OMFMrrNaVsxm45UQ1rKSOsbZbIIud7qrGL4GSL1qfTLQNLqDMCRFZcmJqComMpTuoCaGlCI4tYq-zfYVJWqbqFqqnKjaJrpd5UQz52IvP9Qt2D_Gb4QZcL0DQH5y7SGqZDx0BqyPYHplg_9H_geIbYay</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Khuyen, Trinh Dinh</creator><creator>Mandiki, Syaghalirwa N.M.</creator><creator>Cornet, Valérie</creator><creator>Douxfils, Jessica</creator><creator>Betoulle, Stéphane</creator><creator>Bossier, Peter</creator><creator>Reyes-López, Felipe E.</creator><creator>Tort, Lluis</creator><creator>Kestemont, Patrick</creator><general>Elsevier Ltd</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>7X8</scope><orcidid>https://orcid.org/0000-0003-0066-669X</orcidid></search><sort><creationdate>201712</creationdate><title>Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin</title><author>Khuyen, Trinh Dinh ; Mandiki, Syaghalirwa N.M. ; Cornet, Valérie ; Douxfils, Jessica ; Betoulle, Stéphane ; Bossier, Peter ; Reyes-López, Felipe E. ; Tort, Lluis ; Kestemont, Patrick</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c419t-94704452a3cda6ff409b445b6479510124aef62c24a3b972d509766dd251f2423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Administration, Oral</topic><topic>Aeromonas salmonicida - physiology</topic><topic>Animal Feed - analysis</topic><topic>Animals</topic><topic>Anti-Infective Agents - administration & dosage</topic><topic>Anti-Infective Agents - pharmacology</topic><topic>Bovine lactoferrin</topic><topic>Diet - veterinary</topic><topic>Disease resistance</topic><topic>Disease Resistance - immunology</topic><topic>Dose-Response Relationship, Immunologic</topic><topic>Fish Diseases - immunology</topic><topic>Gene Expression - immunology</topic><topic>Gene Expression Profiling - veterinary</topic><topic>Gene expressions</topic><topic>Gram-Negative Bacterial Infections - immunology</topic><topic>Gram-Negative Bacterial Infections - veterinary</topic><topic>Immunity</topic><topic>Immunity, Humoral</topic><topic>Lactoferrin - administration & dosage</topic><topic>Lactoferrin - pharmacology</topic><topic>Leukocytes - immunology</topic><topic>Oncorhynchus mykiss - genetics</topic><topic>Oncorhynchus mykiss - growth & development</topic><topic>Oncorhynchus mykiss - immunology</topic><topic>Rainbow trout (Oncorhynchus mykiss)</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Khuyen, Trinh Dinh</creatorcontrib><creatorcontrib>Mandiki, Syaghalirwa N.M.</creatorcontrib><creatorcontrib>Cornet, Valérie</creatorcontrib><creatorcontrib>Douxfils, Jessica</creatorcontrib><creatorcontrib>Betoulle, Stéphane</creatorcontrib><creatorcontrib>Bossier, Peter</creatorcontrib><creatorcontrib>Reyes-López, Felipe E.</creatorcontrib><creatorcontrib>Tort, Lluis</creatorcontrib><creatorcontrib>Kestemont, Patrick</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Fish & shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Khuyen, Trinh Dinh</au><au>Mandiki, Syaghalirwa N.M.</au><au>Cornet, Valérie</au><au>Douxfils, Jessica</au><au>Betoulle, Stéphane</au><au>Bossier, Peter</au><au>Reyes-López, Felipe E.</au><au>Tort, Lluis</au><au>Kestemont, Patrick</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin</atitle><jtitle>Fish & shellfish immunology</jtitle><addtitle>Fish Shellfish Immunol</addtitle><date>2017-12</date><risdate>2017</risdate><volume>71</volume><spage>359</spage><epage>371</epage><pages>359-371</pages><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>Lactoferrin, a large multifunctional glycoprotein, is involved in many physiological functions but its immunomodulatory pathways are not well characterized in fish. The objective of the present study was to investigate the temporal effect of dietary bovine lactoferrin (BLf) at low (0.1%) and high (1%) on immunological organs of rainbow trout juveniles. BLf diets did not affect specific growth rate, haematocrit, splenic index, spleen respiratory burst activity as well as humoral (mIgM) and neutrophils (MPO) gene expressions after short term - 35 days (D35) and long term nutrient test - 51 days (D51) of feeding. Both low and high BLf doses induced enhanced level of plasma alternative complement activity, plasma total immunoglobulin on D35 and D51, lymphocyte plus thrombocyte cell proportion on D35 and monocyte cell proportion in total blood leukocyte cells on D51. On D51 but not on D35, BLf diets upregulated the expression of inflammatory genes in kidney for il-1 at the low BLf dose, il-8 at both BLf doses and il-6 at the high BLf dose in spleen, and il-10 at both BLf doses in kidney. Moreover, the expression of T helper (cd4-2α; cd4-2β) genes was significantly upregulated only on D51 by both BLf doses in both spleen and kidney tissues. On D51, controls and BLf treated fish were intraperitoneally injected with A. salmonicida achromogenes. The expression of 13 immune genes was evaluated at 44 h post-injection (D54). The expression of lysozyme gene was upregulated by both BLf doses after bacterial infection both in spleen and kidney. The expression of mcsfrα (spleen) and tgf-β1 (kidney) was also modulated by both BLf doses. Low and high BLf doses enhanced disease resistance of rainbow trout juveniles with the cumulative survival rate of 36% and 38% respectively while those of the control was 19% after 14 days challenged with bacteria. The results indicate that BLf diets activated the humoral immunity, associated to blood leukocyte cells of rainbow trout after short term BLf administration, and the long term BLf administration was necessary for sensitizing other lymphoid organs such as in spleen and kidney. Only after long term test, BLf diets induced significantly higher levels of innate and adaptive immune gene expressions than those of the control. Dietary BLf activated more markedly the expression of innate immune genes than the adaptive ones; this upregulation of some immune genes could explain the high disease resistance observed in rainbow trout juveniles fed BLf.
•BLf was positively affecting rainbow trout immune system in a time/dose dependant manner.•After short-term, BLf activated blood leukocyte cell and humoral responses.•After long-term, BLf diets increased pro-inflammatory gene expressions in spleen, kidney.•After bacterial challenge, BLf tends to provide a better protection against bacterial infection and survival.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>29050988</pmid><doi>10.1016/j.fsi.2017.10.027</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-0066-669X</orcidid></addata></record> |
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| subjects | Administration, Oral Aeromonas salmonicida - physiology Animal Feed - analysis Animals Anti-Infective Agents - administration & dosage Anti-Infective Agents - pharmacology Bovine lactoferrin Diet - veterinary Disease resistance Disease Resistance - immunology Dose-Response Relationship, Immunologic Fish Diseases - immunology Gene Expression - immunology Gene Expression Profiling - veterinary Gene expressions Gram-Negative Bacterial Infections - immunology Gram-Negative Bacterial Infections - veterinary Immunity Immunity, Humoral Lactoferrin - administration & dosage Lactoferrin - pharmacology Leukocytes - immunology Oncorhynchus mykiss - genetics Oncorhynchus mykiss - growth & development Oncorhynchus mykiss - immunology Rainbow trout (Oncorhynchus mykiss) Time Factors |
| title | Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin |
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