Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses

Abstract Pathobionts have evolved many strategies to coexist with the host, but how immune evasion mechanisms contribute to the difficulty of developing vaccines against pathobionts is unclear. Meanwhile, Staphylococcus aureus (SA) has resisted human vaccine development to date. Here we show that pr...

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Main Authors: Irshad Ahmed Hajam, Chih-Ming Tsai, Cesia Gonzalez, Juan Raphael Caldera, María Lázaro Díez, Xin Du, April Aralar, Brian Lin, William Duong, George Y. Liu
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54644-w
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author Irshad Ahmed Hajam
Chih-Ming Tsai
Cesia Gonzalez
Juan Raphael Caldera
María Lázaro Díez
Xin Du
April Aralar
Brian Lin
William Duong
George Y. Liu
author_facet Irshad Ahmed Hajam
Chih-Ming Tsai
Cesia Gonzalez
Juan Raphael Caldera
María Lázaro Díez
Xin Du
April Aralar
Brian Lin
William Duong
George Y. Liu
author_sort Irshad Ahmed Hajam
collection DOAJ
description Abstract Pathobionts have evolved many strategies to coexist with the host, but how immune evasion mechanisms contribute to the difficulty of developing vaccines against pathobionts is unclear. Meanwhile, Staphylococcus aureus (SA) has resisted human vaccine development to date. Here we show that prior SA exposure induces non-protective CD4+ T cell imprints, leading to the blunting of protective IsdB vaccine responses. Mechanistically, these SA-experienced CD4+ T cells express IL-10, which is further amplified by vaccination and impedes vaccine protection by binding with IL-10Rα on CD4+ T cell and inhibit IL-17A production. IL-10 also mediates cross-suppression of IsdB and sdrE multi-antigen vaccine. By contrast, the inefficiency of SA IsdB, IsdA and MntC vaccines can be overcome by co-treatment with adjuvants that promote IL-17A and IFN-γ responses. We thus propose that IL-10 secreting, SA-experienced CD4+ T cell imprints represent a staphylococcal immune escaping mechanism that needs to be taken into consideration for future vaccine development.
format Article
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issn 2041-1723
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publishDate 2024-12-01
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series Nature Communications
spelling doaj-art-bef39520896347868e6bc6b1b802bac62024-12-22T12:35:54ZengNature PortfolioNature Communications2041-17232024-12-0115111610.1038/s41467-024-54644-wPathobiont-induced suppressive immune imprints thwart T cell vaccine responsesIrshad Ahmed Hajam0Chih-Ming Tsai1Cesia Gonzalez2Juan Raphael Caldera3María Lázaro Díez4Xin Du5April Aralar6Brian Lin7William Duong8George Y. Liu9Department of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoDepartment of Pediatrics, University of California San DiegoAbstract Pathobionts have evolved many strategies to coexist with the host, but how immune evasion mechanisms contribute to the difficulty of developing vaccines against pathobionts is unclear. Meanwhile, Staphylococcus aureus (SA) has resisted human vaccine development to date. Here we show that prior SA exposure induces non-protective CD4+ T cell imprints, leading to the blunting of protective IsdB vaccine responses. Mechanistically, these SA-experienced CD4+ T cells express IL-10, which is further amplified by vaccination and impedes vaccine protection by binding with IL-10Rα on CD4+ T cell and inhibit IL-17A production. IL-10 also mediates cross-suppression of IsdB and sdrE multi-antigen vaccine. By contrast, the inefficiency of SA IsdB, IsdA and MntC vaccines can be overcome by co-treatment with adjuvants that promote IL-17A and IFN-γ responses. We thus propose that IL-10 secreting, SA-experienced CD4+ T cell imprints represent a staphylococcal immune escaping mechanism that needs to be taken into consideration for future vaccine development.https://doi.org/10.1038/s41467-024-54644-w
spellingShingle Irshad Ahmed Hajam
Chih-Ming Tsai
Cesia Gonzalez
Juan Raphael Caldera
María Lázaro Díez
Xin Du
April Aralar
Brian Lin
William Duong
George Y. Liu
Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
Nature Communications
title Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
title_full Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
title_fullStr Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
title_full_unstemmed Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
title_short Pathobiont-induced suppressive immune imprints thwart T cell vaccine responses
title_sort pathobiont induced suppressive immune imprints thwart t cell vaccine responses
url https://doi.org/10.1038/s41467-024-54644-w
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