The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age

PurposeCancer patients are at risk of severe COVID-19 infection, and vaccination is recommended. Nevertheless, we observe a failure of COVID-19 vaccines in this vulnerable population. We hypothesize that senescent peripheral T-cells alter COVID-19 vaccine-induced immunity.MethodsWe performed a monoc...

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Main Authors: E. Orillard, L. Spehner, L. Mansi, A. Bouard, A. Falcoz, Q. Lepiller, E. Renaude, JR. Pallandre, A. Vienot, M. Kroemer, C. Borg
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1160664/full
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author E. Orillard
E. Orillard
L. Spehner
L. Spehner
L. Mansi
L. Mansi
A. Bouard
A. Falcoz
A. Falcoz
Q. Lepiller
Q. Lepiller
E. Renaude
JR. Pallandre
JR. Pallandre
A. Vienot
A. Vienot
M. Kroemer
M. Kroemer
M. Kroemer
C. Borg
C. Borg
C. Borg
author_facet E. Orillard
E. Orillard
L. Spehner
L. Spehner
L. Mansi
L. Mansi
A. Bouard
A. Falcoz
A. Falcoz
Q. Lepiller
Q. Lepiller
E. Renaude
JR. Pallandre
JR. Pallandre
A. Vienot
A. Vienot
M. Kroemer
M. Kroemer
M. Kroemer
C. Borg
C. Borg
C. Borg
author_sort E. Orillard
collection DOAJ
description PurposeCancer patients are at risk of severe COVID-19 infection, and vaccination is recommended. Nevertheless, we observe a failure of COVID-19 vaccines in this vulnerable population. We hypothesize that senescent peripheral T-cells alter COVID-19 vaccine-induced immunity.MethodsWe performed a monocentric prospective study and enrolled cancer patients and healthy donors before the COVID-19 vaccination. The primary objective was to assess the association of peripheral senescent T-cells (CD28-CD57+KLRG1+) with COVID-19 vaccine-induced immunity.ResultsEighty cancer patients have been included, with serological and specific T-cell responses evaluated before and at 3 months post-vaccination. Age ≥ 70 years was the principal clinical factor negatively influencing the serological (p=0.035) and specific SARS-CoV-2 T-cell responses (p=0.047). The presence of senescent T-cells was correlated to lower serological (p=0.049) and specific T-cell responses (p=0.009). Our results sustained the definition of a specific cut-off for senescence immune phenotype (SIP) (≥ 5% of CD4 and ≥ 39.5% of CD8 T-cells), which was correlated to a lower serological response induced by COVID-19 vaccination for CD4 and CD8 SIPhigh (p=0.039 and p=0.049 respectively). While CD4 SIP level had no impact on COVID-19 vaccine efficacy in elderly patients, our results unraveled a possible predictive role for CD4 SIPhigh T-cell levels in younger cancer patients.ConclusionsElderly cancer patients have a poor serological response to vaccination; specific strategies are needed in this population. Also, the presence of a CD4 SIPhigh affects the serological response in younger patients and seems to be a potential biomarker of no vaccinal response.
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spelling doaj.art-0bc99df4bee547d4a5f1a4d48c6d81f22023-06-02T05:07:28ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-06-011410.3389/fimmu.2023.11606641160664The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of ageE. Orillard0E. Orillard1L. Spehner2L. Spehner3L. Mansi4L. Mansi5A. Bouard6A. Falcoz7A. Falcoz8Q. Lepiller9Q. Lepiller10E. Renaude11JR. Pallandre12JR. Pallandre13A. Vienot14A. Vienot15M. Kroemer16M. Kroemer17M. Kroemer18C. Borg19C. Borg20C. Borg21Department of Oncology, University Hospital of Besançon, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceDepartment of Oncology, University Hospital of Besançon, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceDepartment of Oncology, University Hospital of Besançon, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceITAC Platform, University of Bourgogne Franche-Comté, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceMethodology and Quality of Life Unit in Oncology, University Hospital of Besançon, Besançon, FranceDepartment of Virology, University Hospital of Besançon, Besançon, FranceResearch Unit EA3181, Université de Franche Comté, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceITAC Platform, University of Bourgogne Franche-Comté, Besançon, FranceDepartment of Oncology, University Hospital of Besançon, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceITAC Platform, University of Bourgogne Franche-Comté, Besançon, FranceDepartment of Pharmacy, University Hospital of Besançon, Besançon, FranceDepartment of Oncology, University Hospital of Besançon, Besançon, FranceBourgogne Franche-Comté University, INSERM, Etablissement Français du Sang Bourgogne Franche-Comté, UMR1098, Interactions Hôte-Greffon-Tumeur/Ingénierie cellulaire et Génique, Besançon, FranceITAC Platform, University of Bourgogne Franche-Comté, Besançon, FrancePurposeCancer patients are at risk of severe COVID-19 infection, and vaccination is recommended. Nevertheless, we observe a failure of COVID-19 vaccines in this vulnerable population. We hypothesize that senescent peripheral T-cells alter COVID-19 vaccine-induced immunity.MethodsWe performed a monocentric prospective study and enrolled cancer patients and healthy donors before the COVID-19 vaccination. The primary objective was to assess the association of peripheral senescent T-cells (CD28-CD57+KLRG1+) with COVID-19 vaccine-induced immunity.ResultsEighty cancer patients have been included, with serological and specific T-cell responses evaluated before and at 3 months post-vaccination. Age ≥ 70 years was the principal clinical factor negatively influencing the serological (p=0.035) and specific SARS-CoV-2 T-cell responses (p=0.047). The presence of senescent T-cells was correlated to lower serological (p=0.049) and specific T-cell responses (p=0.009). Our results sustained the definition of a specific cut-off for senescence immune phenotype (SIP) (≥ 5% of CD4 and ≥ 39.5% of CD8 T-cells), which was correlated to a lower serological response induced by COVID-19 vaccination for CD4 and CD8 SIPhigh (p=0.039 and p=0.049 respectively). While CD4 SIP level had no impact on COVID-19 vaccine efficacy in elderly patients, our results unraveled a possible predictive role for CD4 SIPhigh T-cell levels in younger cancer patients.ConclusionsElderly cancer patients have a poor serological response to vaccination; specific strategies are needed in this population. Also, the presence of a CD4 SIPhigh affects the serological response in younger patients and seems to be a potential biomarker of no vaccinal response.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1160664/fullCOVID-19, vaccinationpredictive biomarkercancer patientT lymphocyte (T-cell)senescence
spellingShingle E. Orillard
E. Orillard
L. Spehner
L. Spehner
L. Mansi
L. Mansi
A. Bouard
A. Falcoz
A. Falcoz
Q. Lepiller
Q. Lepiller
E. Renaude
JR. Pallandre
JR. Pallandre
A. Vienot
A. Vienot
M. Kroemer
M. Kroemer
M. Kroemer
C. Borg
C. Borg
C. Borg
The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
Frontiers in Immunology
COVID-19, vaccination
predictive biomarker
cancer patient
T lymphocyte (T-cell)
senescence
title The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
title_full The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
title_fullStr The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
title_full_unstemmed The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
title_short The presence of senescent peripheral T-cells is negatively correlated to COVID-19 vaccine-induced immunity in cancer patients under 70 years of age
title_sort presence of senescent peripheral t cells is negatively correlated to covid 19 vaccine induced immunity in cancer patients under 70 years of age
topic COVID-19, vaccination
predictive biomarker
cancer patient
T lymphocyte (T-cell)
senescence
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1160664/full
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