Systemic immune profiling of Omicron-infected subjects inoculated with different doses of inactivated virus vaccine

Shanhe Yu; Yingni Lin; Yong Li; Shijun Chen; Lina Zhou; Hejie Song; Cuiping Yang; Haiqing Zhang; Jianping Zhou; Shunchang Sun; Yanan Li; Juan Chen; Ruixue Feng; Niu Qiao; Yinyin Xie; Ruihong Zhang; Tong Yin; Saijuan Chen; Qingyun Li; Jiang Zhu; Jieming Qu

doi:10.1016/j.cell.2023.08.033

Systemic immune profiling of Omicron-infected subjects inoculated with different doses of inactivated virus vaccine

Cell. 2023 Oct 12;186(21):4615-4631.e16. doi: 10.1016/j.cell.2023.08.033. Epub 2023 Sep 27.

Authors

Shanhe Yu¹, Yingni Lin², Yong Li², Shijun Chen³, Lina Zhou², Hejie Song², Cuiping Yang⁴, Haiqing Zhang², Jianping Zhou², Shunchang Sun⁵, Yanan Li², Juan Chen³, Ruixue Feng³, Niu Qiao³, Yinyin Xie³, Ruihong Zhang³, Tong Yin³, Saijuan Chen⁶, Qingyun Li⁷, Jiang Zhu⁸, Jieming Qu⁹

Affiliations

¹ Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Collaborative Innovation Center of Hematology, Ruijin Hospital Affiliated to Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China; Key Laboratory of Emergency Prevention, Diagnosis and Treatment of Respiratory Infectious Diseases, Shanghai 200025, China.
² Department of Pulmonary and Critical Care Medicine, Ruijin Hospital, Institute of Respiratory Diseases, Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China; Key Laboratory of Emergency Prevention, Diagnosis and Treatment of Respiratory Infectious Diseases, Shanghai 200025, China.
³ Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Collaborative Innovation Center of Hematology, Ruijin Hospital Affiliated to Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China.
⁴ Department of Gastroenterology, Ruijin Hospital, Shanghai Jiao-Tong University School of Medicine, Shanghai 201801, China.
⁵ Department of Laboratory Medicine, Ruijin Hospital, Shanghai Jiao-Tong University School of Medicine, Shanghai 201801, China.
⁶ Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Collaborative Innovation Center of Hematology, Ruijin Hospital Affiliated to Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China. Electronic address: sjchen@stn.sh.cn.
⁷ Department of Pulmonary and Critical Care Medicine, Ruijin Hospital, Institute of Respiratory Diseases, Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China; Key Laboratory of Emergency Prevention, Diagnosis and Treatment of Respiratory Infectious Diseases, Shanghai 200025, China. Electronic address: liqingyun68@hotmail.com.
⁸ Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Collaborative Innovation Center of Hematology, Ruijin Hospital Affiliated to Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China; Key Laboratory of Emergency Prevention, Diagnosis and Treatment of Respiratory Infectious Diseases, Shanghai 200025, China. Electronic address: zhujiang@shsmu.edu.cn.
⁹ Department of Pulmonary and Critical Care Medicine, Ruijin Hospital, Institute of Respiratory Diseases, Shanghai Jiao-Tong University School of Medicine, Shanghai 200025, China; Key Laboratory of Emergency Prevention, Diagnosis and Treatment of Respiratory Infectious Diseases, Shanghai 200025, China; National Research Center for Translational Medicine at Shanghai, Shanghai 200025, China. Electronic address: jmqu0906@163.com.

PMID: 37769658
DOI: 10.1016/j.cell.2023.08.033

Abstract

SARS-CoV-2 primary strain-based vaccination exerts a protective effect against Omicron variants-initiated infection, symptom occurrence, and disease severity in a booster-dependent manner. Yet, the underlying mechanisms remain unclear. During the 2022 Omicron outbreak in Shanghai, we enrolled 122 infected adults and 50 uninfected controls who had been unvaccinated or vaccinated with two or three doses of COVID-19 inactive vaccines and performed integrative analysis of 41-plex CyTOF, RNA-seq, and Olink on their peripheral blood samples. The frequencies of HLA-DR^hi classical monocytes, non-classical monocytes, and Th1-like Tem tended to increase, whereas the frequency of Treg was reduced by booster vaccine, and they influenced symptom occurrence in a vaccine dose-dependent manner. Intercorrelation and mechanistic analysis suggested that the booster vaccination induced monocytic training, which would prime monocytic activation and maturation rather than differentiating into myeloid-derived suppressive cells upon Omicron infections. Overall, our study provides insights into how booster vaccination elaborates protective immunity across SARS-CoV-2 variants.

Keywords: COVID-19 inactive vaccines; Omicron variants; Treg; booster vaccination; monocytic activation.