Targeting Xcr1 on Dendritic Cells Rapidly Induce Th1-Associated Immune Responses That Contribute to Protection Against Influenza Infection
Targeting antigen to conventional dendritic cells (cDCs) can improve antigen-specific immune responses and additionally be used to influence the polarization of the immune responses. However, the mechanisms by which this is achieved are less clear. To improve our understanding, we here evaluate mole...
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| Published in: | Frontiers in immunology Vol. 13; p. 752714 |
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| Main Authors: | , , , , , , , |
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| Language: | English |
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| Abstract | Targeting antigen to conventional dendritic cells (cDCs) can improve antigen-specific immune responses and additionally be used to influence the polarization of the immune responses. However, the mechanisms by which this is achieved are less clear. To improve our understanding, we here evaluate molecular and cellular requirements for CD4
T cell and antibody polarization after immunization with Xcl1-fusion vaccines that specifically target cDC1s. Xcl1-fusion vaccines induced an IgG2a/IgG2b-dominated antibody response and rapid polarization of Th1 cells both
and
. For comparison, we included fliC-fusion vaccines that almost exclusively induced IgG1, despite inducing a more mixed polarization of T cells. Th1 polarization and IgG2a induction with Xcl1-fusion vaccines required IL-12 secretion but were nevertheless maintained in BATF3
mice which lack IL-12-secreting migratory DCs. Interestingly, induction of IgG2a-dominated responses was highly dependent on the early kinetics of Th1 induction and was important for optimal protection in an influenza infection model. Early Th1 induction was dominant, since a combined Xcl1- and fliC-fusion vaccine induced IgG2a/IgG2b polarized antibody responses similar to Xcl1-fusion vaccines alone. In summary, our results demonstrate that targeting antigen to Xcr1
cDC1s is an efficient strategy for enhancing IgG2a antibody responses through rapid Th1 induction, which can be utilized for improved vaccine design. |
|---|---|
| AbstractList | Targeting antigen to conventional dendritic cells (cDCs) can improve antigen-specific immune responses and additionally be used to influence the polarization of the immune responses. However, the mechanisms by which this is achieved are less clear. To improve our understanding, we here evaluate molecular and cellular requirements for CD4
+
T cell and antibody polarization after immunization with Xcl1-fusion vaccines that specifically target cDC1s. Xcl1-fusion vaccines induced an IgG2a/IgG2b-dominated antibody response and rapid polarization of Th1 cells both
in vitro
and
in vivo
. For comparison, we included fliC-fusion vaccines that almost exclusively induced IgG1, despite inducing a more mixed polarization of T cells. Th1 polarization and IgG2a induction with Xcl1-fusion vaccines required IL-12 secretion but were nevertheless maintained in BATF3
-/-
mice which lack IL-12-secreting migratory DCs. Interestingly, induction of IgG2a-dominated responses was highly dependent on the early kinetics of Th1 induction and was important for optimal protection in an influenza infection model. Early Th1 induction was dominant, since a combined Xcl1- and fliC-fusion vaccine induced IgG2a/IgG2b polarized antibody responses similar to Xcl1-fusion vaccines alone. In summary, our results demonstrate that targeting antigen to Xcr1
+
cDC1s is an efficient strategy for enhancing IgG2a antibody responses through rapid Th1 induction, which can be utilized for improved vaccine design. Targeting antigen to conventional dendritic cells (cDCs) can improve antigen-specific immune responses and additionally be used to influence the polarization of the immune responses. However, the mechanisms by which this is achieved are less clear. To improve our understanding, we here evaluate molecular and cellular requirements for CD4+ T cell and antibody polarization after immunization with Xcl1-fusion vaccines that specifically target cDC1s. Xcl1-fusion vaccines induced an IgG2a/IgG2b-dominated antibody response and rapid polarization of Th1 cells both in vitro and in vivo. For comparison, we included fliC-fusion vaccines that almost exclusively induced IgG1, despite inducing a more mixed polarization of T cells. Th1 polarization and IgG2a induction with Xcl1-fusion vaccines required IL-12 secretion but were nevertheless maintained in BATF3-/- mice which lack IL-12-secreting migratory DCs. Interestingly, induction of IgG2a-dominated responses was highly dependent on the early kinetics of Th1 induction and was important for optimal protection in an influenza infection model. Early Th1 induction was dominant, since a combined Xcl1- and fliC-fusion vaccine induced IgG2a/IgG2b polarized antibody responses similar to Xcl1-fusion vaccines alone. In summary, our results demonstrate that targeting antigen to Xcr1+ cDC1s is an efficient strategy for enhancing IgG2a antibody responses through rapid Th1 induction, which can be utilized for improved vaccine design. Targeting antigen to conventional dendritic cells (cDCs) can improve antigen-specific immune responses and additionally be used to influence the polarization of the immune responses. However, the mechanisms by which this is achieved are less clear. To improve our understanding, we here evaluate molecular and cellular requirements for CD4 T cell and antibody polarization after immunization with Xcl1-fusion vaccines that specifically target cDC1s. Xcl1-fusion vaccines induced an IgG2a/IgG2b-dominated antibody response and rapid polarization of Th1 cells both and . For comparison, we included fliC-fusion vaccines that almost exclusively induced IgG1, despite inducing a more mixed polarization of T cells. Th1 polarization and IgG2a induction with Xcl1-fusion vaccines required IL-12 secretion but were nevertheless maintained in BATF3 mice which lack IL-12-secreting migratory DCs. Interestingly, induction of IgG2a-dominated responses was highly dependent on the early kinetics of Th1 induction and was important for optimal protection in an influenza infection model. Early Th1 induction was dominant, since a combined Xcl1- and fliC-fusion vaccine induced IgG2a/IgG2b polarized antibody responses similar to Xcl1-fusion vaccines alone. In summary, our results demonstrate that targeting antigen to Xcr1 cDC1s is an efficient strategy for enhancing IgG2a antibody responses through rapid Th1 induction, which can be utilized for improved vaccine design. |
| Author | Tesfaye, Demo Yemane Bogen, Bjarne Braathen, Ranveig Bobic, Sonja Huszthy, Peter Csaba Gudjonsson, Arnar Fossum, Even Lysén, Anna |
| AuthorAffiliation | 2 Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital , Oslo , Norway 1 Department of Immunology, Division of Laboratory Medicine, Oslo University Hospital , Oslo , Norway 3 Center for Immune Regulation, Institute of Immunology, University of Oslo and Oslo University Hospital Rikshospitalet , Oslo , Norway |
| AuthorAffiliation_xml | – name: 3 Center for Immune Regulation, Institute of Immunology, University of Oslo and Oslo University Hospital Rikshospitalet , Oslo , Norway – name: 2 Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital , Oslo , Norway – name: 1 Department of Immunology, Division of Laboratory Medicine, Oslo University Hospital , Oslo , Norway |
| Author_xml | – sequence: 1 givenname: Demo Yemane surname: Tesfaye fullname: Tesfaye, Demo Yemane organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway – sequence: 2 givenname: Sonja surname: Bobic fullname: Bobic, Sonja organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway – sequence: 3 givenname: Anna surname: Lysén fullname: Lysén, Anna organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway – sequence: 4 givenname: Peter Csaba surname: Huszthy fullname: Huszthy, Peter Csaba organization: Center for Immune Regulation, Institute of Immunology, University of Oslo and Oslo University Hospital Rikshospitalet, Oslo, Norway – sequence: 5 givenname: Arnar surname: Gudjonsson fullname: Gudjonsson, Arnar organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway – sequence: 6 givenname: Ranveig surname: Braathen fullname: Braathen, Ranveig organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway – sequence: 7 givenname: Bjarne surname: Bogen fullname: Bogen, Bjarne organization: Center for Immune Regulation, Institute of Immunology, University of Oslo and Oslo University Hospital Rikshospitalet, Oslo, Norway – sequence: 8 givenname: Even surname: Fossum fullname: Fossum, Even organization: Kristian Gerhard Jebsen Center for Research on Influenza Vaccines, University of Oslo and Oslo University Hospital, Oslo, Norway |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35296089$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_smim_2023_101762 crossref_primary_10_1016_j_heliyon_2024_e31712 crossref_primary_10_3389_fimmu_2023_1221008 crossref_primary_10_1016_j_celrep_2023_113294 crossref_primary_10_14336_AD_2022_1102 |
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| Copyright | Copyright © 2022 Tesfaye, Bobic, Lysén, Huszthy, Gudjonsson, Braathen, Bogen and Fossum. info:eu-repo/semantics/openAccess Copyright © 2022 Tesfaye, Bobic, Lysén, Huszthy, Gudjonsson, Braathen, Bogen and Fossum 2022 Tesfaye, Bobic, Lysén, Huszthy, Gudjonsson, Braathen, Bogen and Fossum |
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| Keywords | targeting XCR1 dendritic cells IgG2a Th1 |
| Language | English |
| License | Copyright © 2022 Tesfaye, Bobic, Lysén, Huszthy, Gudjonsson, Braathen, Bogen and Fossum. 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. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 NFR/250884 This article was submitted to Antigen Presenting Cell Biology, a section of the journal Frontiers in Immunology Edited by: Maud Plantinga, University Medical Center Utrecht, Netherlands These authors have contributed equally to this work Reviewed by: Tsuneyasu Kaisho, Wakayama Medical University, Japan; Kohtaro Fujihashi, The University of Tokyo, Japan |
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| SubjectTerms | Animals Antibody Formation Antigens Dendritic Cells Humans IgG2a Immunoglobulin G Immunology Influenza Vaccines Influenza, Human Interleukin-12 Mice targeting Th1 XCR1 |
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| Title | Targeting Xcr1 on Dendritic Cells Rapidly Induce Th1-Associated Immune Responses That Contribute to Protection Against Influenza Infection |
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