Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin

Trinh Dinh Khuyen, Syaghalirwa N.M. Mandiki, Valérie Cornet, Jessica Douxfils, Stéphane Betoulle, Peter Bossier, Felipe E. Reyes-López, Lluis Tort, Patrick Kestemont

Résultats de recherche: Contribution à un journal/une revueArticle

Résumé

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.

langueAnglais
Pages359-371
Nombre de pages13
journalFish & shellfish immunology
Volume71
Date de mise en ligne précoce2017
Les DOIs
étatPublié - 1 déc. 2017

Empreinte digitale

Lactoferrin
lactoferrin
physiological response
immune response
rainbow
Oncorhynchus mykiss
cattle
spleen
dosage
Genes
kidneys
Nutrition
gene
bovine
diet
disease resistance
genes
Gene expression
gene expression
Fish

mots-clés

    Citer ceci

    @article{37aae7880c104279b5f7d21171648b8e,
    title = "Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin",
    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.",
    keywords = "Bovine lactoferrin, Disease resistance, Gene expressions, Immunity, Rainbow trout (Oncorhynchus mykiss)",
    author = "Khuyen, {Trinh Dinh} and Mandiki, {Syaghalirwa N.M.} and Val{\'e}rie Cornet and Jessica Douxfils and St{\'e}phane Betoulle and Peter Bossier and Reyes-L{\'o}pez, {Felipe E.} and Lluis Tort and Patrick Kestemont",
    year = "2017",
    month = "12",
    day = "1",
    doi = "10.1016/j.fsi.2017.10.027",
    language = "English",
    volume = "71",
    pages = "359--371",
    journal = "Fish and Shellfish Immunology",
    issn = "1050-4648",
    publisher = "Academic Press Inc.",

    }

    Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin. / Khuyen, Trinh Dinh; Mandiki, Syaghalirwa N.M.; Cornet, Valérie; Douxfils, Jessica; Betoulle, Stéphane; Bossier, Peter; Reyes-López, Felipe E.; Tort, Lluis; Kestemont, Patrick.

    Dans: Fish & shellfish immunology, Vol 71, 01.12.2017, p. 359-371.

    Résultats de recherche: Contribution à un journal/une revueArticle

    TY - JOUR

    T1 - Physiological and immune response of juvenile rainbow trout to dietary bovine lactoferrin

    AU - Khuyen,Trinh Dinh

    AU - Mandiki,Syaghalirwa N.M.

    AU - Cornet,Valérie

    AU - Douxfils,Jessica

    AU - Betoulle,Stéphane

    AU - Bossier,Peter

    AU - Reyes-López,Felipe E.

    AU - Tort,Lluis

    AU - Kestemont,Patrick

    PY - 2017/12/1

    Y1 - 2017/12/1

    N2 - 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.

    AB - 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.

    KW - Bovine lactoferrin

    KW - Disease resistance

    KW - Gene expressions

    KW - Immunity

    KW - Rainbow trout (Oncorhynchus mykiss)

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    U2 - 10.1016/j.fsi.2017.10.027

    DO - 10.1016/j.fsi.2017.10.027

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    JO - Fish and Shellfish Immunology

    T2 - Fish and Shellfish Immunology

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