Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout

Long-term immunity is of great importance for protection against pathogens and has been extensively studied in mammals. Successive heterologous infections can affect the maintenance of immune memory, inducing attrition of T memory cells and diminishing B cell mediated protection. In fish, the basis...

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Main Authors: Sofie Navelsaker, Susana Magadan, Luc Jouneau, Edwige Quillet, Niels J. Olesen, Hetron Mweemba Munang'andu, Pierre Boudinot, Øystein Evensen
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2019.02687/full
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spelling doaj-5802dfd5123d49ce89cee2a6d2a92d4c2020-11-25T01:50:24ZengFrontiers Media S.A.Frontiers in Immunology1664-32242019-11-011010.3389/fimmu.2019.02687491298Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow TroutSofie Navelsaker0Susana Magadan1Susana Magadan2Luc Jouneau3Edwige Quillet4Niels J. Olesen5Hetron Mweemba Munang'andu6Pierre Boudinot7Øystein Evensen8Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Oslo, NorwayVIM, INRA Centre Jouy-en-Josas, Jouy-en-Josas, FranceCentro de Investigaciones Biomédicas (CINBIO), University of Vigo, Vigo, SpainVIM, INRA Centre Jouy-en-Josas, Jouy-en-Josas, FranceGABI, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceDTU Veterinary Institute, Technical University of Denmark, Kongens Lyngby, DenmarkDepartment of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Oslo, NorwayVIM, INRA Centre Jouy-en-Josas, Jouy-en-Josas, FranceDepartment of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Oslo, NorwayLong-term immunity is of great importance for protection against pathogens and has been extensively studied in mammals. Successive heterologous infections can affect the maintenance of immune memory, inducing attrition of T memory cells and diminishing B cell mediated protection. In fish, the basis of immune memory and the mechanisms of immunization to heterologous pathogens remain poorly understood. We sequentially immunized isogenic rainbow trout with two immunologically distinct viruses, VHSV and IPNV, either with one virus only or in combination, and analyzed the antibody responses and repertoires. Neutralizing antibodies and ELISPOT did not reveal an effect of heterologous immunization. Using a consensus read sequencing approach that incorporates unique barcodes to each cDNA molecule, we focused on the diversity expressed by selected responding VH/C combinations. We identified both public and private responses against VHSV and/or IPNV in all groups of fish. In fish immunized with two viruses, we registered no significant reduction in the persistence of the response toward the primary immunization. Similarly, the response to the second immunization was not affected by a prior vaccination to the other virus. Our data suggest that heterologous immunization does not enforce attrition of pre-existing antibody producing cells, which may impair the protection afforded by multiple successive vaccinations. These observations are potentially important to improve vaccination strategies practiced in aquaculture.https://www.frontiersin.org/article/10.3389/fimmu.2019.02687/fullantibodiesB cell repertoireheterologous immunizationpublic responsefish immunologyRepSeq
collection DOAJ
language English
format Article
sources DOAJ
author Sofie Navelsaker
Susana Magadan
Susana Magadan
Luc Jouneau
Edwige Quillet
Niels J. Olesen
Hetron Mweemba Munang'andu
Pierre Boudinot
Øystein Evensen
spellingShingle Sofie Navelsaker
Susana Magadan
Susana Magadan
Luc Jouneau
Edwige Quillet
Niels J. Olesen
Hetron Mweemba Munang'andu
Pierre Boudinot
Øystein Evensen
Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
Frontiers in Immunology
antibodies
B cell repertoire
heterologous immunization
public response
fish immunology
RepSeq
author_facet Sofie Navelsaker
Susana Magadan
Susana Magadan
Luc Jouneau
Edwige Quillet
Niels J. Olesen
Hetron Mweemba Munang'andu
Pierre Boudinot
Øystein Evensen
author_sort Sofie Navelsaker
title Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
title_short Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
title_full Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
title_fullStr Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
title_full_unstemmed Sequential Immunization With Heterologous Viruses Does Not Result in Attrition of the B Cell Memory in Rainbow Trout
title_sort sequential immunization with heterologous viruses does not result in attrition of the b cell memory in rainbow trout
publisher Frontiers Media S.A.
series Frontiers in Immunology
issn 1664-3224
publishDate 2019-11-01
description Long-term immunity is of great importance for protection against pathogens and has been extensively studied in mammals. Successive heterologous infections can affect the maintenance of immune memory, inducing attrition of T memory cells and diminishing B cell mediated protection. In fish, the basis of immune memory and the mechanisms of immunization to heterologous pathogens remain poorly understood. We sequentially immunized isogenic rainbow trout with two immunologically distinct viruses, VHSV and IPNV, either with one virus only or in combination, and analyzed the antibody responses and repertoires. Neutralizing antibodies and ELISPOT did not reveal an effect of heterologous immunization. Using a consensus read sequencing approach that incorporates unique barcodes to each cDNA molecule, we focused on the diversity expressed by selected responding VH/C combinations. We identified both public and private responses against VHSV and/or IPNV in all groups of fish. In fish immunized with two viruses, we registered no significant reduction in the persistence of the response toward the primary immunization. Similarly, the response to the second immunization was not affected by a prior vaccination to the other virus. Our data suggest that heterologous immunization does not enforce attrition of pre-existing antibody producing cells, which may impair the protection afforded by multiple successive vaccinations. These observations are potentially important to improve vaccination strategies practiced in aquaculture.
topic antibodies
B cell repertoire
heterologous immunization
public response
fish immunology
RepSeq
url https://www.frontiersin.org/article/10.3389/fimmu.2019.02687/full
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