Cargando…

Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity

Vibrio anguillarum, a marine bacterial pathogen that causes vibriosis, is a recurrent pathogen of lumpfish (Cyclopterus lumpus). Lumpfish is utilized as a cleaner fish in the Atlantic salmon (Salmo salar) aquaculture in the North Atlantic region because of its ability to visualize and prey on the ec...

Descripción completa

Detalles Bibliográficos
Autores principales: Dang, My, Cao, Trung, Vasquez, Ignacio, Hossain, Ahmed, Gnanagobal, Hajarooba, Kumar, Surendra, Hall, Jennifer R., Monk, Jennifer, Boyce, Danny, Westcott, Jillian, Santander, Javier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8402551/
https://www.ncbi.nlm.nih.gov/pubmed/34451944
http://dx.doi.org/10.3390/vaccines9080819
_version_ 1783745816943394816
author Dang, My
Cao, Trung
Vasquez, Ignacio
Hossain, Ahmed
Gnanagobal, Hajarooba
Kumar, Surendra
Hall, Jennifer R.
Monk, Jennifer
Boyce, Danny
Westcott, Jillian
Santander, Javier
author_facet Dang, My
Cao, Trung
Vasquez, Ignacio
Hossain, Ahmed
Gnanagobal, Hajarooba
Kumar, Surendra
Hall, Jennifer R.
Monk, Jennifer
Boyce, Danny
Westcott, Jillian
Santander, Javier
author_sort Dang, My
collection PubMed
description Vibrio anguillarum, a marine bacterial pathogen that causes vibriosis, is a recurrent pathogen of lumpfish (Cyclopterus lumpus). Lumpfish is utilized as a cleaner fish in the Atlantic salmon (Salmo salar) aquaculture in the North Atlantic region because of its ability to visualize and prey on the ectoparasite sea lice (Lepeophtheirus salmonis) on the skin of Atlantic salmon, and its performance in cold environments. Lumpfish immunity is critical for optimal performance and sea lice removal. Oral vaccine delivery at a young age is the desired method for fish immunization because is easy to use, reduces fish stress during immunization, and can be applied on a large scale while the fish are at a young age. However, the efficacy of orally delivered inactivated vaccines is controversial. In this study, we evaluated the effectiveness of a V. anguillarum bacterin orally delivered to cultured lumpfish and contrasted it to an intraperitoneal (i.p.) boost delivery. We bio-encapsulated V. anguillarum bacterin in Artemia salina live-feed and orally immunized lumpfish larvae. Vaccine intake and immune response were evaluated by microscopy and quantitative polymerase chain reaction (qPCR) analysis, respectively. qPCR analyses showed that the oral immunization of lumpfish larvae resulted in a subtle stimulation of canonical immune transcripts such as il8b, il10, igha, ighmc, ighb, ccl19, ccl20, cd8a, cd74, ifng, and lgp2. Nine months after oral immunization, one group was orally boosted, and a second group was both orally and i.p. boosted. Two months after boost immunization, lumpfish were challenged with V. anguillarum (7.8 × 10(5) CFU dose(−1)). Orally boosted fish showed a relative percentage of survival (RPS) of 2%. In contrast, the oral and i.p. boosted group showed a RPS of 75.5% (p < 0.0001). V. anguillarum bacterin that had been orally delivered was not effective in lumpfish, which is in contrast to the i.p. delivered bacterin that protected the lumpfish against vibriosis. This suggests that orally administered V. anguillarum bacterin did not reach the deep lymphoid tissues, either in the larvae or juvenile fish, therefore oral immunization was not effective. Oral vaccines that are capable of crossing the epithelium and reach deep lymphoid tissues are required to confer an effective protection to lumpfish against V. anguillarum
format Online
Article
Text
id pubmed-8402551
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-84025512021-08-29 Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity Dang, My Cao, Trung Vasquez, Ignacio Hossain, Ahmed Gnanagobal, Hajarooba Kumar, Surendra Hall, Jennifer R. Monk, Jennifer Boyce, Danny Westcott, Jillian Santander, Javier Vaccines (Basel) Article Vibrio anguillarum, a marine bacterial pathogen that causes vibriosis, is a recurrent pathogen of lumpfish (Cyclopterus lumpus). Lumpfish is utilized as a cleaner fish in the Atlantic salmon (Salmo salar) aquaculture in the North Atlantic region because of its ability to visualize and prey on the ectoparasite sea lice (Lepeophtheirus salmonis) on the skin of Atlantic salmon, and its performance in cold environments. Lumpfish immunity is critical for optimal performance and sea lice removal. Oral vaccine delivery at a young age is the desired method for fish immunization because is easy to use, reduces fish stress during immunization, and can be applied on a large scale while the fish are at a young age. However, the efficacy of orally delivered inactivated vaccines is controversial. In this study, we evaluated the effectiveness of a V. anguillarum bacterin orally delivered to cultured lumpfish and contrasted it to an intraperitoneal (i.p.) boost delivery. We bio-encapsulated V. anguillarum bacterin in Artemia salina live-feed and orally immunized lumpfish larvae. Vaccine intake and immune response were evaluated by microscopy and quantitative polymerase chain reaction (qPCR) analysis, respectively. qPCR analyses showed that the oral immunization of lumpfish larvae resulted in a subtle stimulation of canonical immune transcripts such as il8b, il10, igha, ighmc, ighb, ccl19, ccl20, cd8a, cd74, ifng, and lgp2. Nine months after oral immunization, one group was orally boosted, and a second group was both orally and i.p. boosted. Two months after boost immunization, lumpfish were challenged with V. anguillarum (7.8 × 10(5) CFU dose(−1)). Orally boosted fish showed a relative percentage of survival (RPS) of 2%. In contrast, the oral and i.p. boosted group showed a RPS of 75.5% (p < 0.0001). V. anguillarum bacterin that had been orally delivered was not effective in lumpfish, which is in contrast to the i.p. delivered bacterin that protected the lumpfish against vibriosis. This suggests that orally administered V. anguillarum bacterin did not reach the deep lymphoid tissues, either in the larvae or juvenile fish, therefore oral immunization was not effective. Oral vaccines that are capable of crossing the epithelium and reach deep lymphoid tissues are required to confer an effective protection to lumpfish against V. anguillarum MDPI 2021-07-23 /pmc/articles/PMC8402551/ /pubmed/34451944 http://dx.doi.org/10.3390/vaccines9080819 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Dang, My
Cao, Trung
Vasquez, Ignacio
Hossain, Ahmed
Gnanagobal, Hajarooba
Kumar, Surendra
Hall, Jennifer R.
Monk, Jennifer
Boyce, Danny
Westcott, Jillian
Santander, Javier
Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title_full Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title_fullStr Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title_full_unstemmed Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title_short Oral Immunization of Larvae and Juvenile of Lumpfish (Cyclopterus lumpus) against Vibrio anguillarum Does Not Influence Systemic Immunity
title_sort oral immunization of larvae and juvenile of lumpfish (cyclopterus lumpus) against vibrio anguillarum does not influence systemic immunity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8402551/
https://www.ncbi.nlm.nih.gov/pubmed/34451944
http://dx.doi.org/10.3390/vaccines9080819
work_keys_str_mv AT dangmy oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT caotrung oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT vasquezignacio oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT hossainahmed oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT gnanagobalhajarooba oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT kumarsurendra oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT halljenniferr oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT monkjennifer oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT boycedanny oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT westcottjillian oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity
AT santanderjavier oralimmunizationoflarvaeandjuvenileoflumpfishcyclopteruslumpusagainstvibrioanguillarumdoesnotinfluencesystemicimmunity