Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity

The origins of preexisting SARS-CoV-2 cross-reactive antibodies and their potential impacts on vaccine efficacy have not been fully clarified. In this study, we demonstrated that S2 was the prevailing target of the preexisting S protein cross-reactive antibodies in both healthy human and SPF mice. A...

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Main Authors: Liqiu Jia, Shufeng Weng, Jing Wu, Xiangxiang Tian, Yifan Zhang, Xuyang Wang, Jing Wang, Dongmei Yan, Wanhai Wang, Fang Fang, Zhaoqin Zhu, Chao Qiu, Wenhong Zhang, Ying Xu, Yanmin Wan
Format: Article
Language:English
Published: Taylor & Francis Group 2022-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2022.2117503
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author Liqiu Jia
Shufeng Weng
Jing Wu
Xiangxiang Tian
Yifan Zhang
Xuyang Wang
Jing Wang
Dongmei Yan
Wanhai Wang
Fang Fang
Zhaoqin Zhu
Chao Qiu
Wenhong Zhang
Ying Xu
Yanmin Wan
author_facet Liqiu Jia
Shufeng Weng
Jing Wu
Xiangxiang Tian
Yifan Zhang
Xuyang Wang
Jing Wang
Dongmei Yan
Wanhai Wang
Fang Fang
Zhaoqin Zhu
Chao Qiu
Wenhong Zhang
Ying Xu
Yanmin Wan
author_sort Liqiu Jia
collection DOAJ
description The origins of preexisting SARS-CoV-2 cross-reactive antibodies and their potential impacts on vaccine efficacy have not been fully clarified. In this study, we demonstrated that S2 was the prevailing target of the preexisting S protein cross-reactive antibodies in both healthy human and SPF mice. A dominant antibody epitope was identified on the connector domain of S2 (1147-SFKEELDKYFKNHT-1160, P144), which could be recognized by preexisting antibodies in both human and mouse. Through metagenomic sequencing and fecal bacteria transplant, we demonstrated that the generation of S2 cross-reactive antibodies was associated with commensal gut bacteria. Furthermore, six P144 reactive monoclonal antibodies were isolated from naïve SPF mice and were proven to cross-react with commensal gut bacteria collected from both human and mouse. A variety of cross-reactive microbial proteins were identified using LC-MS, of which E. coli derived HSP60 and HSP70 proteins were confirmed to be able to bind to one of the isolated monoclonal antibodies. Mice with high levels of preexisting S2 cross-reactive antibodies mounted higher S protein specific binding antibodies, especially against S2, after being immunized with a SARS-CoV-2 S DNA vaccine. Similarly, we found that levels of preexisting S2 and P144-specific antibodies correlated positively with RBD binding antibody titers after two doses of inactivated SARS-CoV-2 vaccination in human. Collectively, our study revealed an alternative origin of preexisting S2-targeted antibodies and disclosed a previously neglected aspect of the impact of gut microbiota on host anti-SARS-CoV-2 immunity.
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spelling doaj-art-cfda007d165d495f8e99736f2cdbb6642025-08-20T02:29:56ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2117503Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunityLiqiu Jia0Shufeng Weng1Jing Wu2Xiangxiang Tian3Yifan Zhang4Xuyang Wang5Jing Wang6Dongmei Yan7Wanhai Wang8Fang Fang9Zhaoqin Zhu10Chao Qiu11Wenhong Zhang12Ying Xu13Yanmin Wan14Department of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, ChinaState Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Science, Fudan University, Shanghai, ChinaDepartment of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, ChinaDepartment of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, ChinaDepartment of Immunology, School of Basic Medical, Jiamusi University, Jiamusi, ChinaClinical Laboratory, the First Affiliated Hospital of Zhengzhou University, Key Laboratory of Laboratory Medicine of Henan Province, Zhengzhou, ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, ChinaShanghai Public Health Clinical Center, Fudan University, Shanghai, ChinaInstitutes of Biomedical Sciences & Shanghai Key Laboratory of Medical Epigenetics, Fudan University, Shanghai, ChinaDepartment of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, ChinaState Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Science, Fudan University, Shanghai, ChinaDepartment of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, ChinaThe origins of preexisting SARS-CoV-2 cross-reactive antibodies and their potential impacts on vaccine efficacy have not been fully clarified. In this study, we demonstrated that S2 was the prevailing target of the preexisting S protein cross-reactive antibodies in both healthy human and SPF mice. A dominant antibody epitope was identified on the connector domain of S2 (1147-SFKEELDKYFKNHT-1160, P144), which could be recognized by preexisting antibodies in both human and mouse. Through metagenomic sequencing and fecal bacteria transplant, we demonstrated that the generation of S2 cross-reactive antibodies was associated with commensal gut bacteria. Furthermore, six P144 reactive monoclonal antibodies were isolated from naïve SPF mice and were proven to cross-react with commensal gut bacteria collected from both human and mouse. A variety of cross-reactive microbial proteins were identified using LC-MS, of which E. coli derived HSP60 and HSP70 proteins were confirmed to be able to bind to one of the isolated monoclonal antibodies. Mice with high levels of preexisting S2 cross-reactive antibodies mounted higher S protein specific binding antibodies, especially against S2, after being immunized with a SARS-CoV-2 S DNA vaccine. Similarly, we found that levels of preexisting S2 and P144-specific antibodies correlated positively with RBD binding antibody titers after two doses of inactivated SARS-CoV-2 vaccination in human. Collectively, our study revealed an alternative origin of preexisting S2-targeted antibodies and disclosed a previously neglected aspect of the impact of gut microbiota on host anti-SARS-CoV-2 immunity.https://www.tandfonline.com/doi/10.1080/19490976.2022.2117503Cross-reactive antibodySARS-CoV-2spike proteincommensal gut bacteriavaccine immunogenicity
spellingShingle Liqiu Jia
Shufeng Weng
Jing Wu
Xiangxiang Tian
Yifan Zhang
Xuyang Wang
Jing Wang
Dongmei Yan
Wanhai Wang
Fang Fang
Zhaoqin Zhu
Chao Qiu
Wenhong Zhang
Ying Xu
Yanmin Wan
Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
Gut Microbes
Cross-reactive antibody
SARS-CoV-2
spike protein
commensal gut bacteria
vaccine immunogenicity
title Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
title_full Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
title_fullStr Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
title_full_unstemmed Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
title_short Preexisting antibodies targeting SARS-CoV-2 S2 cross-react with commensal gut bacteria and impact COVID-19 vaccine induced immunity
title_sort preexisting antibodies targeting sars cov 2 s2 cross react with commensal gut bacteria and impact covid 19 vaccine induced immunity
topic Cross-reactive antibody
SARS-CoV-2
spike protein
commensal gut bacteria
vaccine immunogenicity
url https://www.tandfonline.com/doi/10.1080/19490976.2022.2117503
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