Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques

Prolonged infection and possible evolution of SARS-CoV-2 in patients living with uncontrolled HIV-1 infection highlight the importance of an effective vaccination regimen, yet the immunogenicity of COVID-19 vaccines and predictive immune biomarkers have not been well investigated. Herein, we report...

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Main Authors: Pingchao Li, Qian Wang, Yizi He, Chenchen Yang, Zhengyuan Zhang, Zijian Liu, Bo Liu, Li Yin, Yilan Cui, Peiyu Hu, Yichu Liu, Pingqian Zheng, Wei Wang, Linbing Qu, Caijun Sun, Suhua Guan, Liqiang Feng, Ling Chen
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2022.2136538
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author Pingchao Li
Qian Wang
Yizi He
Chenchen Yang
Zhengyuan Zhang
Zijian Liu
Bo Liu
Li Yin
Yilan Cui
Peiyu Hu
Yichu Liu
Pingqian Zheng
Wei Wang
Linbing Qu
Caijun Sun
Suhua Guan
Liqiang Feng
Ling Chen
author_facet Pingchao Li
Qian Wang
Yizi He
Chenchen Yang
Zhengyuan Zhang
Zijian Liu
Bo Liu
Li Yin
Yilan Cui
Peiyu Hu
Yichu Liu
Pingqian Zheng
Wei Wang
Linbing Qu
Caijun Sun
Suhua Guan
Liqiang Feng
Ling Chen
author_sort Pingchao Li
collection DOAJ
description Prolonged infection and possible evolution of SARS-CoV-2 in patients living with uncontrolled HIV-1 infection highlight the importance of an effective vaccination regimen, yet the immunogenicity of COVID-19 vaccines and predictive immune biomarkers have not been well investigated. Herein, we report that the magnitude and persistence of antibody and cell-mediated immunity (CMI) elicited by an Ad5-vectored COVID-19 vaccine are impaired in SIV-infected macaques with high viral loads (> 105 genome copies per ml plasma, SIVhi) but not in macaques with low viral loads (< 105, SIVlow). After a second vaccination, the immune responses are robustly enhanced in all uninfected and SIVlow macaques. These responses also show a moderate increase in 70% SIVhi macaques but decline sharply soon after. Further analysis reveals that decreased antibody and CMI responses are associated with reduced circulating follicular helper T cell (TFH) counts and aberrant CD4/CD8 ratios, respectively, indicating that dysregulation of CD4+ T cells by SIV infection impairs the COVID-19 vaccine-induced immunity. Ad5-vectored COVID-19 vaccine shows no impact on SIV loads or SIV-specific CMI responses. Our study underscores the necessity of frequent booster vaccinations in HIV-infected patients and provides indicative biomarkers for predicting vaccination effectiveness in these patients.
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spelling doaj-art-5e2cea3b05bc4148a9970b6665fd1f732025-08-20T02:30:45ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112110.1080/22221751.2022.2136538Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaquesPingchao Li0Qian Wang1Yizi He2Chenchen Yang3Zhengyuan Zhang4Zijian Liu5Bo Liu6Li Yin7Yilan Cui8Peiyu Hu9Yichu Liu10Pingqian Zheng11Wei Wang12Linbing Qu13Caijun Sun14Suhua Guan15Liqiang Feng16Ling Chen17State Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaGuangzhou nBiomed Ltd., Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaGuangzhou nBiomed Ltd., Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaGuangzhou Laboratory &amp; Bioland Laboratory, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaGuangzhou Laboratory &amp; Bioland Laboratory, Guangzhou, People’s Republic of ChinaGuangzhou Laboratory &amp; Bioland Laboratory, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaGuangzhou nBiomed Ltd., Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaState Key Laboratory of Respiratory Disease, Guangdong Laboratory of Computational Biomedicine, Guangzhou Institutes of Biomedicine and Health (GIBH), Chinese Academy of Sciences, Guangzhou, People’s Republic of ChinaProlonged infection and possible evolution of SARS-CoV-2 in patients living with uncontrolled HIV-1 infection highlight the importance of an effective vaccination regimen, yet the immunogenicity of COVID-19 vaccines and predictive immune biomarkers have not been well investigated. Herein, we report that the magnitude and persistence of antibody and cell-mediated immunity (CMI) elicited by an Ad5-vectored COVID-19 vaccine are impaired in SIV-infected macaques with high viral loads (> 105 genome copies per ml plasma, SIVhi) but not in macaques with low viral loads (< 105, SIVlow). After a second vaccination, the immune responses are robustly enhanced in all uninfected and SIVlow macaques. These responses also show a moderate increase in 70% SIVhi macaques but decline sharply soon after. Further analysis reveals that decreased antibody and CMI responses are associated with reduced circulating follicular helper T cell (TFH) counts and aberrant CD4/CD8 ratios, respectively, indicating that dysregulation of CD4+ T cells by SIV infection impairs the COVID-19 vaccine-induced immunity. Ad5-vectored COVID-19 vaccine shows no impact on SIV loads or SIV-specific CMI responses. Our study underscores the necessity of frequent booster vaccinations in HIV-infected patients and provides indicative biomarkers for predicting vaccination effectiveness in these patients.https://www.tandfonline.com/doi/10.1080/22221751.2022.2136538COVID-19 vaccineimmunogenicityimmunodeficiencyHIVSIV infectionrhesus macaques
spellingShingle Pingchao Li
Qian Wang
Yizi He
Chenchen Yang
Zhengyuan Zhang
Zijian Liu
Bo Liu
Li Yin
Yilan Cui
Peiyu Hu
Yichu Liu
Pingqian Zheng
Wei Wang
Linbing Qu
Caijun Sun
Suhua Guan
Liqiang Feng
Ling Chen
Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
Emerging Microbes and Infections
COVID-19 vaccine
immunogenicity
immunodeficiency
HIV
SIV infection
rhesus macaques
title Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
title_full Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
title_fullStr Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
title_full_unstemmed Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
title_short Booster vaccination is required to elicit and maintain COVID-19 vaccine-induced immunity in SIV-infected macaques
title_sort booster vaccination is required to elicit and maintain covid 19 vaccine induced immunity in siv infected macaques
topic COVID-19 vaccine
immunogenicity
immunodeficiency
HIV
SIV infection
rhesus macaques
url https://www.tandfonline.com/doi/10.1080/22221751.2022.2136538
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