Cargando…

Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin

We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed...

Descripción completa

Detalles Bibliográficos
Autores principales: Emam, Mohamed, Eslamloo, Khalil, Caballero-Solares, Albert, Lorenz, Evandro Kleber, Xue, Xi, Umasuthan, Navaneethaiyer, Gnanagobal, Hajarooba, Santander, Javier, Taylor, Richard G., Balder, Rachel, Parrish, Christopher C., Rise, Matthew L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532746/
https://www.ncbi.nlm.nih.gov/pubmed/36213116
http://dx.doi.org/10.3389/fmolb.2022.931548
_version_ 1784802185616293888
author Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
author_facet Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
author_sort Emam, Mohamed
collection PubMed
description We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed by 4 weeks on the high-18:3ω3 diet and termed “switched-diet”. Following the second 4 weeks of feeding (i.e., at 8 weeks), head kidney tissues from all groups were sampled for FA analysis. Fish were then intraperitoneally injected with either a formalin-killed Renibacterium salmoninarum bacterin (5 × 10(7) cells mL(−1)) or phosphate-buffered saline (PBS control), and head kidney tissues for gene expression analysis were sampled at 24 h post-injection. FA analysis showed that the head kidney profile reflected the dietary FA, especially for C(18) FAs. The qPCR analyses of twenty-three genes showed that both the high-ω6 and high-ω3 groups had significant bacterin-dependent induction of some transcripts involved in lipid metabolism (ch25ha and lipe), pathogen recognition (clec12b and tlr5), and immune effectors (znrf1 and cish). In contrast, these transcripts did not significantly respond to the bacterin in the “switched-diet” group. Concurrently, biomarkers encoding proteins with putative roles in biotic inflammatory response (tnfrsf6b) and dendritic cell maturation (ccl13) were upregulated, and a chemokine receptor (cxcr1) was downregulated with the bacterin injection regardless of the experimental diets. On the other hand, an inflammatory regulator biomarker, bcl3, was only significantly upregulated in the high-ω3 fed group, and a C-type lectin family member (clec3a) was only significantly downregulated in the switched-diet group with the bacterin injection (compared with diet-matched PBS-injected controls). Transcript fold-change (FC: bacterin/PBS) showed that tlr5 was significantly over 2-fold higher in the high-18:2ω6 diet group compared with other diet groups. FC and FA associations highlighted the role of DGLA (20:3ω6; anti-inflammatory) and/or EPA (20:5ω3; anti-inflammatory) vs. ARA (20:4ω6; pro-inflammatory) as representative of the anti-inflammatory/pro-inflammatory balance between eicosanoid precursors. Also, the correlations revealed associations of FA proportions (% total FA) and FA ratios with several eicosanoid and immune receptor biomarkers (e.g., DGLA/ARA significant positive correlation with pgds, 5loxa, 5loxb, tlr5, and cxcr1). In summary, dietary FA profiles and/or regimens modulated the expression of some immune-relevant genes in Atlantic salmon injected with R. salmoninarum bacterin. The modulation of Atlantic salmon responses to bacterial pathogens and their associated antigens using high-ω6/high-ω3 diets warrants further investigation.
format Online
Article
Text
id pubmed-9532746
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-95327462022-10-06 Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin Emam, Mohamed Eslamloo, Khalil Caballero-Solares, Albert Lorenz, Evandro Kleber Xue, Xi Umasuthan, Navaneethaiyer Gnanagobal, Hajarooba Santander, Javier Taylor, Richard G. Balder, Rachel Parrish, Christopher C. Rise, Matthew L. Front Mol Biosci Molecular Biosciences We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed by 4 weeks on the high-18:3ω3 diet and termed “switched-diet”. Following the second 4 weeks of feeding (i.e., at 8 weeks), head kidney tissues from all groups were sampled for FA analysis. Fish were then intraperitoneally injected with either a formalin-killed Renibacterium salmoninarum bacterin (5 × 10(7) cells mL(−1)) or phosphate-buffered saline (PBS control), and head kidney tissues for gene expression analysis were sampled at 24 h post-injection. FA analysis showed that the head kidney profile reflected the dietary FA, especially for C(18) FAs. The qPCR analyses of twenty-three genes showed that both the high-ω6 and high-ω3 groups had significant bacterin-dependent induction of some transcripts involved in lipid metabolism (ch25ha and lipe), pathogen recognition (clec12b and tlr5), and immune effectors (znrf1 and cish). In contrast, these transcripts did not significantly respond to the bacterin in the “switched-diet” group. Concurrently, biomarkers encoding proteins with putative roles in biotic inflammatory response (tnfrsf6b) and dendritic cell maturation (ccl13) were upregulated, and a chemokine receptor (cxcr1) was downregulated with the bacterin injection regardless of the experimental diets. On the other hand, an inflammatory regulator biomarker, bcl3, was only significantly upregulated in the high-ω3 fed group, and a C-type lectin family member (clec3a) was only significantly downregulated in the switched-diet group with the bacterin injection (compared with diet-matched PBS-injected controls). Transcript fold-change (FC: bacterin/PBS) showed that tlr5 was significantly over 2-fold higher in the high-18:2ω6 diet group compared with other diet groups. FC and FA associations highlighted the role of DGLA (20:3ω6; anti-inflammatory) and/or EPA (20:5ω3; anti-inflammatory) vs. ARA (20:4ω6; pro-inflammatory) as representative of the anti-inflammatory/pro-inflammatory balance between eicosanoid precursors. Also, the correlations revealed associations of FA proportions (% total FA) and FA ratios with several eicosanoid and immune receptor biomarkers (e.g., DGLA/ARA significant positive correlation with pgds, 5loxa, 5loxb, tlr5, and cxcr1). In summary, dietary FA profiles and/or regimens modulated the expression of some immune-relevant genes in Atlantic salmon injected with R. salmoninarum bacterin. The modulation of Atlantic salmon responses to bacterial pathogens and their associated antigens using high-ω6/high-ω3 diets warrants further investigation. Frontiers Media S.A. 2022-09-21 /pmc/articles/PMC9532746/ /pubmed/36213116 http://dx.doi.org/10.3389/fmolb.2022.931548 Text en Copyright © 2022 Emam, Eslamloo, Caballero-Solares, Lorenz, Xue, Umasuthan, Gnanagobal, Santander, Taylor, Balder, Parrish and Rise. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Biosciences
Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_full Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_fullStr Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_full_unstemmed Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_short Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_sort nutritional immunomodulation of atlantic salmon response to renibacterium salmoninarum bacterin
topic Molecular Biosciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532746/
https://www.ncbi.nlm.nih.gov/pubmed/36213116
http://dx.doi.org/10.3389/fmolb.2022.931548
work_keys_str_mv AT emammohamed nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT eslamlookhalil nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT caballerosolaresalbert nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT lorenzevandrokleber nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT xuexi nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT umasuthannavaneethaiyer nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT gnanagobalhajarooba nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT santanderjavier nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT taylorrichardg nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT balderrachel nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT parrishchristopherc nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin
AT risematthewl nutritionalimmunomodulationofatlanticsalmonresponsetorenibacteriumsalmoninarumbacterin