Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination

Antigen recognition through the T cell receptor (TCR) αβ heterodimer is one of the primary determinants of the adaptive immune response. Vaccines activate naïve T cells with high specificity to expand and differentiate into memory T cells. However, antigen-specific memory CD4 T cells exist in unexpo...

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Main Authors: George Elias, Pieter Meysman, Esther Bartholomeus, Nicolas De Neuter, Nina Keersmaekers, Arvid Suls, Hilde Jansens, Aisha Souquette, Hans De Reu, Marie-Paule Emonds, Evelien Smits, Eva Lion, Paul G Thomas, Geert Mortier, Pierre Van Damme, Philippe Beutels, Kris Laukens, Viggo Van Tendeloo, Benson Ogunjimi
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/68388
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author George Elias
Pieter Meysman
Esther Bartholomeus
Nicolas De Neuter
Nina Keersmaekers
Arvid Suls
Hilde Jansens
Aisha Souquette
Hans De Reu
Marie-Paule Emonds
Evelien Smits
Eva Lion
Paul G Thomas
Geert Mortier
Pierre Van Damme
Philippe Beutels
Kris Laukens
Viggo Van Tendeloo
Benson Ogunjimi
author_facet George Elias
Pieter Meysman
Esther Bartholomeus
Nicolas De Neuter
Nina Keersmaekers
Arvid Suls
Hilde Jansens
Aisha Souquette
Hans De Reu
Marie-Paule Emonds
Evelien Smits
Eva Lion
Paul G Thomas
Geert Mortier
Pierre Van Damme
Philippe Beutels
Kris Laukens
Viggo Van Tendeloo
Benson Ogunjimi
author_sort George Elias
collection DOAJ
description Antigen recognition through the T cell receptor (TCR) αβ heterodimer is one of the primary determinants of the adaptive immune response. Vaccines activate naïve T cells with high specificity to expand and differentiate into memory T cells. However, antigen-specific memory CD4 T cells exist in unexposed antigen-naïve hosts. In this study, we use high-throughput sequencing of memory CD4 TCRβ repertoire and machine learning to show that individuals with preexisting vaccine-reactive memory CD4 T cell clonotypes elicited earlier and higher antibody titers and mounted a more robust CD4 T cell response to hepatitis B vaccine. In addition, integration of TCRβ sequence patterns into a hepatitis B epitope-specific annotation model can predict which individuals will have an early and more vigorous vaccine-elicited immunity. Thus, the presence of preexisting memory T cell clonotypes has a significant impact on immunity and can be used to predict immune responses to vaccination.
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spelling doaj.art-ef8d3322e4b24849bf9e4eef3c1cad402022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2022-01-011110.7554/eLife.68388Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccinationGeorge Elias0https://orcid.org/0000-0001-8419-9544Pieter Meysman1https://orcid.org/0000-0001-5903-633XEsther Bartholomeus2Nicolas De Neuter3https://orcid.org/0000-0002-6011-6457Nina Keersmaekers4Arvid Suls5Hilde Jansens6Aisha Souquette7Hans De Reu8Marie-Paule Emonds9Evelien Smits10Eva Lion11Paul G Thomas12Geert Mortier13Pierre Van Damme14Philippe Beutels15Kris Laukens16Viggo Van Tendeloo17Benson Ogunjimi18https://orcid.org/0000-0002-0831-2063Laboratory of Experimental Hematology (LEH), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium; Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium; Biomedical Informatics Research Network Antwerp, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Department of Medical Genetics, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium; Biomedical Informatics Research Network Antwerp, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Centre for Health Economics Research & Modeling Infectious Diseases, Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Department of Medical Genetics, University of Antwerp, Antwerp, BelgiumDepartment of Clinical Microbiology, Antwerp University Hospital, Antwerp, BelgiumDepartment of Immunology, St. Jude Children's Research Hospital, Memphis, United StatesLaboratory of Experimental Hematology (LEH), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium; Center for Cell Therapy and Regenerative Medicine, Antwerp University Hospital, Antwerp, BelgiumHistocompatibility and Immunogenetic Laboratory, Rode Kruis-Vlaanderen, Mechelen, BelgiumLaboratory of Experimental Hematology (LEH), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium; Center for Cell Therapy and Regenerative Medicine, Antwerp University Hospital, Antwerp, BelgiumLaboratory of Experimental Hematology (LEH), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium; Center for Cell Therapy and Regenerative Medicine, Antwerp University Hospital, Antwerp, BelgiumDepartment of Immunology, St. Jude Children's Research Hospital, Memphis, United StatesAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Department of Medical Genetics, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Centre for the Evaluation of Vaccination (CEV), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Centre for Health Economics Research & Modeling Infectious Diseases, Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium; Biomedical Informatics Research Network Antwerp, University of Antwerp, Antwerp, BelgiumLaboratory of Experimental Hematology (LEH), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, BelgiumAntwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium; Centre for Health Economics Research & Modeling Infectious Diseases, Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, Belgium; Antwerp Center for Translational Immunology and Virology (ACTIV), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium; Department of Paediatrics, Antwerp University Hospital, Antwerp, BelgiumAntigen recognition through the T cell receptor (TCR) αβ heterodimer is one of the primary determinants of the adaptive immune response. Vaccines activate naïve T cells with high specificity to expand and differentiate into memory T cells. However, antigen-specific memory CD4 T cells exist in unexposed antigen-naïve hosts. In this study, we use high-throughput sequencing of memory CD4 TCRβ repertoire and machine learning to show that individuals with preexisting vaccine-reactive memory CD4 T cell clonotypes elicited earlier and higher antibody titers and mounted a more robust CD4 T cell response to hepatitis B vaccine. In addition, integration of TCRβ sequence patterns into a hepatitis B epitope-specific annotation model can predict which individuals will have an early and more vigorous vaccine-elicited immunity. Thus, the presence of preexisting memory T cell clonotypes has a significant impact on immunity and can be used to predict immune responses to vaccination.https://elifesciences.org/articles/68388CD4 T cellT cell receptorTCR repertoirevaccination
spellingShingle George Elias
Pieter Meysman
Esther Bartholomeus
Nicolas De Neuter
Nina Keersmaekers
Arvid Suls
Hilde Jansens
Aisha Souquette
Hans De Reu
Marie-Paule Emonds
Evelien Smits
Eva Lion
Paul G Thomas
Geert Mortier
Pierre Van Damme
Philippe Beutels
Kris Laukens
Viggo Van Tendeloo
Benson Ogunjimi
Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
eLife
CD4 T cell
T cell receptor
TCR repertoire
vaccination
title Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
title_full Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
title_fullStr Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
title_full_unstemmed Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
title_short Preexisting memory CD4 T cells in naïve individuals confer robust immunity upon hepatitis B vaccination
title_sort preexisting memory cd4 t cells in naive individuals confer robust immunity upon hepatitis b vaccination
topic CD4 T cell
T cell receptor
TCR repertoire
vaccination
url https://elifesciences.org/articles/68388
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