Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar

Cristian Oliver; José Leonardo Coronado; Danixa Martínez; Alexander Kashulin-Bekkelund; Leidy X. Lagos; Elia Ciani; Constanza Sanhueza-Oyarzún; Alejandra Mancilla-Nova; Ricardo Enríquez; Hanne C. Winther-Larsen; Alex Romero

doi:10.1016/j.fsi.2023.108887

Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar

Cristian Oliver^*, José Leonardo Coronado, Danixa Martínez, Alexander Kashulin-Bekkelund, Leidy X. Lagos, Elia Ciani, Constanza Sanhueza-Oyarzún, Alejandra Mancilla-Nova, Ricardo Enríquez, Hanne C. Winther-Larsen^*, Alex Romero^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

4 Scopus citations

Abstract

Piscirickettsiosis outbreaks due to Piscirickettsia salmonis occur globally in the Chilean salmon aquaculture generating significant monetary losses in the industry. P. salmonis secretes outer membrane vesicles (OMVs) which are naturally non-replicating and highly immunogenic spherical nanoparticles. P. salmonis OMVs has been shown to induce immune response in zebrafish; however, the immune response induced by these vesicles in salmonids has not been evaluated. In this study, we inoculated Atlantic salmon with 10 and 30 μg doses of P. salmonis OMVs and took samples for 12 days. qPCR analysis indicated an inflammatory response. Thus, the inflammatory genes evaluated were up- or down-regulated at several times in liver, head kidney and spleen. In addition, the liver was the organ most immune-induced, mainly in the 30 μg-dose. Interestingly, co-expression of pro- and anti-inflammatory cytokines was evidenced by the prominent expression of il-10 at day 1 in spleen and also in head kidney on days 3, 6 and 12, while il-10 and tgf-β were up-regulated on days 3, 6 and 12 in liver. Importantly, we detected the production of IgM against proteins of P. salmonis in the serum collected from immunized fish after 14 days. Thus, 40 and 400 μg OMVs induced the production of highest IgM levels; however, no statistical difference in the immunoglobulin levels produced by these OMVs doses were detected. The current study provides evidence that OMVs released by P. salmonis induced a pro-inflammatory responses and IgM production in S. salar, while regulatory genes were induced in order to regulate their effects and achieve the balance of the inflammatory response.

Original language	English
Article number	108887
Journal	Fish and Shellfish Immunology
Volume	139
DOIs	https://doi.org/10.1016/j.fsi.2023.108887
State	Published - 2023

Bibliographical note

Funding Information:
This work was financially supported by the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) [Grant No. 11180994], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849]. We are greatly thankful to the Bjørn Reidar Hansen, Harald Støkken and Bjørn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU). The authors also acknowledge the support provided by the Vicerrectoría de Investigación, Desarrollo y Creación Artística of the Universidad Austral de Chile (VIDCA-UACh). We also thank the technical assistance of Mr. Esteban Henríquez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile.

Funding Information:
This work was financially supported by the Fondo Nacional de Desarrollo Científico y Tecnológico ( FONDECYT ) [Grant No. 11180994 ], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004 ], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849 ]. We are greatly thankful to the Bjørn Reidar Hansen, Harald Støkken and Bjørn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU) . The authors also acknowledge the support provided by the Vicerrectoría de Investigación, Desarrollo y Creación Artística of the Universidad Austral de Chile (VIDCA- UACh ). We also thank the technical assistance of Mr. Esteban Henríquez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile.

Publisher Copyright:
© 2023 Elsevier Ltd

ASJC Scopus subject areas

Immunology
Environmental Chemistry
Aquatic Science
Immunology and Microbiology (miscellaneous)

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10.1016/j.fsi.2023.108887

Cite this

Oliver, C., Coronado, J. L., Martínez, D., Kashulin-Bekkelund, A., Lagos, L. X., Ciani, E., Sanhueza-Oyarzún, C., Mancilla-Nova, A., Enríquez, R., Winther-Larsen, H. C., & Romero, A. (2023). Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar. Fish and Shellfish Immunology, 139, Article 108887. https://doi.org/10.1016/j.fsi.2023.108887

@article{48e4d55465b44eb1ada41f50150990b5,

title = "Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar",

abstract = "Piscirickettsiosis outbreaks due to Piscirickettsia salmonis occur globally in the Chilean salmon aquaculture generating significant monetary losses in the industry. P. salmonis secretes outer membrane vesicles (OMVs) which are naturally non-replicating and highly immunogenic spherical nanoparticles. P. salmonis OMVs has been shown to induce immune response in zebrafish; however, the immune response induced by these vesicles in salmonids has not been evaluated. In this study, we inoculated Atlantic salmon with 10 and 30 μg doses of P. salmonis OMVs and took samples for 12 days. qPCR analysis indicated an inflammatory response. Thus, the inflammatory genes evaluated were up- or down-regulated at several times in liver, head kidney and spleen. In addition, the liver was the organ most immune-induced, mainly in the 30 μg-dose. Interestingly, co-expression of pro- and anti-inflammatory cytokines was evidenced by the prominent expression of il-10 at day 1 in spleen and also in head kidney on days 3, 6 and 12, while il-10 and tgf-β were up-regulated on days 3, 6 and 12 in liver. Importantly, we detected the production of IgM against proteins of P. salmonis in the serum collected from immunized fish after 14 days. Thus, 40 and 400 μg OMVs induced the production of highest IgM levels; however, no statistical difference in the immunoglobulin levels produced by these OMVs doses were detected. The current study provides evidence that OMVs released by P. salmonis induced a pro-inflammatory responses and IgM production in S. salar, while regulatory genes were induced in order to regulate their effects and achieve the balance of the inflammatory response.",

keywords = "Extracellular vesicles, Immune response, Piscirickettsia salmonis, Pro-inflammatory, SRS, Salmo salar",

author = "Cristian Oliver and Coronado, {Jos{\'e} Leonardo} and Danixa Mart{\'i}nez and Alexander Kashulin-Bekkelund and Lagos, {Leidy X.} and Elia Ciani and Constanza Sanhueza-Oyarz{\'u}n and Alejandra Mancilla-Nova and Ricardo Enr{\'i}quez and Winther-Larsen, {Hanne C.} and Alex Romero",

note = "Funding Information: This work was financially supported by the Fondo Nacional de Desarrollo Cient{\'i}fico y Tecnol{\'o}gico (FONDECYT) [Grant No. 11180994], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849]. We are greatly thankful to the Bj{\o}rn Reidar Hansen, Harald St{\o}kken and Bj{\o}rn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU). The authors also acknowledge the support provided by the Vicerrector{\'i}a de Investigaci{\'o}n, Desarrollo y Creaci{\'o}n Art{\'i}stica of the Universidad Austral de Chile (VIDCA-UACh). We also thank the technical assistance of Mr. Esteban Henr{\'i}quez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile. Funding Information: This work was financially supported by the Fondo Nacional de Desarrollo Cient{\'i}fico y Tecnol{\'o}gico ( FONDECYT ) [Grant No. 11180994 ], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004 ], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849 ]. We are greatly thankful to the Bj{\o}rn Reidar Hansen, Harald St{\o}kken and Bj{\o}rn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU) . The authors also acknowledge the support provided by the Vicerrector{\'i}a de Investigaci{\'o}n, Desarrollo y Creaci{\'o}n Art{\'i}stica of the Universidad Austral de Chile (VIDCA- UACh ). We also thank the technical assistance of Mr. Esteban Henr{\'i}quez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile. Publisher Copyright: {\textcopyright} 2023 Elsevier Ltd",

year = "2023",

month = jan,

doi = "10.1016/j.fsi.2023.108887",

language = "English",

volume = "139",

journal = "Fish and Shellfish Immunology",

issn = "1050-4648",

publisher = "Academic Press Inc.",

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Oliver, C, Coronado, JL, Martínez, D, Kashulin-Bekkelund, A, Lagos, LX, Ciani, E, Sanhueza-Oyarzún, C, Mancilla-Nova, A, Enríquez, R, Winther-Larsen, HC & Romero, A 2023, 'Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar', Fish and Shellfish Immunology, vol. 139, 108887. https://doi.org/10.1016/j.fsi.2023.108887

TY - JOUR

T1 - Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar

AU - Oliver, Cristian

AU - Coronado, José Leonardo

AU - Martínez, Danixa

AU - Kashulin-Bekkelund, Alexander

AU - Lagos, Leidy X.

AU - Ciani, Elia

AU - Sanhueza-Oyarzún, Constanza

AU - Mancilla-Nova, Alejandra

AU - Enríquez, Ricardo

AU - Winther-Larsen, Hanne C.

AU - Romero, Alex

N1 - Funding Information: This work was financially supported by the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) [Grant No. 11180994], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849]. We are greatly thankful to the Bjørn Reidar Hansen, Harald Støkken and Bjørn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU). The authors also acknowledge the support provided by the Vicerrectoría de Investigación, Desarrollo y Creación Artística of the Universidad Austral de Chile (VIDCA-UACh). We also thank the technical assistance of Mr. Esteban Henríquez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile. Funding Information: This work was financially supported by the Fondo Nacional de Desarrollo Científico y Tecnológico ( FONDECYT ) [Grant No. 11180994 ], Fondecyt-Postdoctoral [Grant No. 3200418], Fondap-ANID [Grant No. 1522A0004 ], the University of Oslo and the Research Council of Norway (RCN) Biotek2021 Program [Grant No. 233849 ]. We are greatly thankful to the Bjørn Reidar Hansen, Harald Støkken and Bjørn Frode Eriksen for the assistance in organising fish trial and the aquariunm of Norwegian University of Life Sciences (NMBU) . The authors also acknowledge the support provided by the Vicerrectoría de Investigación, Desarrollo y Creación Artística of the Universidad Austral de Chile (VIDCA- UACh ). We also thank the technical assistance of Mr. Esteban Henríquez from the fish facilities at the Institute of Animal Pathology of the Austral University of Chile. Publisher Copyright: © 2023 Elsevier Ltd

PY - 2023/1

Y1 - 2023/1

N2 - Piscirickettsiosis outbreaks due to Piscirickettsia salmonis occur globally in the Chilean salmon aquaculture generating significant monetary losses in the industry. P. salmonis secretes outer membrane vesicles (OMVs) which are naturally non-replicating and highly immunogenic spherical nanoparticles. P. salmonis OMVs has been shown to induce immune response in zebrafish; however, the immune response induced by these vesicles in salmonids has not been evaluated. In this study, we inoculated Atlantic salmon with 10 and 30 μg doses of P. salmonis OMVs and took samples for 12 days. qPCR analysis indicated an inflammatory response. Thus, the inflammatory genes evaluated were up- or down-regulated at several times in liver, head kidney and spleen. In addition, the liver was the organ most immune-induced, mainly in the 30 μg-dose. Interestingly, co-expression of pro- and anti-inflammatory cytokines was evidenced by the prominent expression of il-10 at day 1 in spleen and also in head kidney on days 3, 6 and 12, while il-10 and tgf-β were up-regulated on days 3, 6 and 12 in liver. Importantly, we detected the production of IgM against proteins of P. salmonis in the serum collected from immunized fish after 14 days. Thus, 40 and 400 μg OMVs induced the production of highest IgM levels; however, no statistical difference in the immunoglobulin levels produced by these OMVs doses were detected. The current study provides evidence that OMVs released by P. salmonis induced a pro-inflammatory responses and IgM production in S. salar, while regulatory genes were induced in order to regulate their effects and achieve the balance of the inflammatory response.

AB - Piscirickettsiosis outbreaks due to Piscirickettsia salmonis occur globally in the Chilean salmon aquaculture generating significant monetary losses in the industry. P. salmonis secretes outer membrane vesicles (OMVs) which are naturally non-replicating and highly immunogenic spherical nanoparticles. P. salmonis OMVs has been shown to induce immune response in zebrafish; however, the immune response induced by these vesicles in salmonids has not been evaluated. In this study, we inoculated Atlantic salmon with 10 and 30 μg doses of P. salmonis OMVs and took samples for 12 days. qPCR analysis indicated an inflammatory response. Thus, the inflammatory genes evaluated were up- or down-regulated at several times in liver, head kidney and spleen. In addition, the liver was the organ most immune-induced, mainly in the 30 μg-dose. Interestingly, co-expression of pro- and anti-inflammatory cytokines was evidenced by the prominent expression of il-10 at day 1 in spleen and also in head kidney on days 3, 6 and 12, while il-10 and tgf-β were up-regulated on days 3, 6 and 12 in liver. Importantly, we detected the production of IgM against proteins of P. salmonis in the serum collected from immunized fish after 14 days. Thus, 40 and 400 μg OMVs induced the production of highest IgM levels; however, no statistical difference in the immunoglobulin levels produced by these OMVs doses were detected. The current study provides evidence that OMVs released by P. salmonis induced a pro-inflammatory responses and IgM production in S. salar, while regulatory genes were induced in order to regulate their effects and achieve the balance of the inflammatory response.

KW - Extracellular vesicles

KW - Immune response

KW - Piscirickettsia salmonis

KW - Pro-inflammatory

KW - SRS

KW - Salmo salar

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U2 - 10.1016/j.fsi.2023.108887

DO - 10.1016/j.fsi.2023.108887

M3 - Article

C2 - 37290611

AN - SCOPUS:85161683531

SN - 1050-4648

VL - 139

JO - Fish and Shellfish Immunology

JF - Fish and Shellfish Immunology

M1 - 108887

ER -

Outer membrane vesicles from Piscirickettsia salmonis induce the expression of inflammatory genes and production of IgM in Atlantic salmon Salmo salar

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