Rapid restoration of potent neutralization activity against the latest Omicron variant JN.1 via AI rational design and antibody engineering

Y Yunji Liao (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) H Hang Ma (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) Z Zhenyu Wang (Institute of Environmental Processes and Pollution Control, School of Environment and Ecology) S Shusheng Wang (Jecho Laboratories, Inc.) Y Yang He Y Yunsong Chang (Jecho Biopharmaceuticals Co., Ltd) H Huifang Zong (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) H Haoneng Tang (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) L Lei Wang Y Yong Ke (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) H Huiyu Cai (BioGeometry) P Ping Li J Jian Tang H Hua Chen (Department of Chemical Engineering, Delft University of Technology, Van der Maasweg 9, 2629 HZ Delft, The Netherlands) A Aleksandra Drelich (Department of Microbiology & Immunology Centers for Biodefense and Emerging Diseases, The University of Texas Medical Branch at Galveston, 301 University Boulevard, Galveston, Texas 77555, United States) B Bi-Hung Peng (Department of Neurosciences, Cell Biology, and Anatomy, University of Texas Medical Branch) J Jason Hsu (Department of Neurosciences, Cell Biology, and Anatomy, University of Texas Medical Branch) V Vivian Tat (Department of Pathology, University of Texas Medical Branch) C Chien-Te K. Tseng (Department of Microbiology and Immunology, University of Texas Medical Branch) J Jingjing Song (Jecho Biopharmaceuticals Co., Ltd) Y Yunsheng Yuan (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) M Mingyuan Wu (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) J Junjun Liu (Techshake Biotechnology Co., Ltd., Xi’an, Shaanxi, China.) Y Yali Yue (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) X Xiaoju Zhang (Department of Respiratory and Critical Care Medicine, Henan Provincial People’s Hospital, University People’s Hospital) Z Ziqi Wang (Division of Advanced Materials) L Li Yang J Jing Li X Xiaodan Ni (Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park) H Hongshi Li (Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park) Y Yuning Xiang (Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park) Y Yanlin Bian (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) B Baohong Zhang (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) H Haiyang Yin (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University) D Dimiter S. Dimitrov (Center for Antibody Therapeutics, University of Pittsburgh School of Medicine) J John Gilly (Jecho Biopharmaceuticals Co., Ltd) L Lei Han H Hua Jiang Y Yueqing Xie (Jecho Laboratories, Inc.) J Jianwei Zhu (Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University)

Abstract

The rapid evolution of the viral genome has led to the continual generation of new variants of SARS-CoV-2. Developing antibody drugs with broad-spectrum and high efficiency is a long-term task. It is promising but challenging to develop therapeutic neutralizing antibodies (nAbs) through in vitro evolution based on antigen–antibody binding interactions. From an early B cell antibody repertoire, we isolated antibody 8G3 that retains its nonregressive neutralizing activity against Omicron BA.1 and various other strains in vitro. 8G3 protected ACE2 transgenic mice from BA.1 and WA1/2020 virus infection without adverse clinical manifestations and completely cleared viral load in the lungs. Similar to most IGHV3–53 antibodies, the binding sites of 8G3 and ACE2 largely overlap, enabling competition with ACE2 for binding to RBD. By comprehensively considering the binding free energy changes of the antigen–antibody complexes, the biological environment of their interactions, and the evolutionary direction of the antibodies, we were able to select 50 mutants. Among them, 11 were validated by experiments showing better neutralizing activities. Further, a combination of four mutations were identified in 8G3 that increased its neutralization potency against JN.1, the latest Omicron mutant, by approximately 1,500-fold, and one of the mutations led to an improvement in activity against multiple variants to a certain extent. Together, we established a procedure of rapid selection of neutralizing antibodies with potent SARS-CoV-2 neutralization activity. Our results provide a reference for engineering neutralizing antibodies against future SARS-CoV-2 variants and even other pandemic viruses.

Article Details

Volume / Issue Vol. 122, Issue 6
Published February 11, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (40)

Y

Yunji Liao

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

H

Hang Ma

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

Z

Zhenyu Wang

Institute of Environmental Processes and Pollution Control, School of Environment and Ecology

S

Shusheng Wang

Jecho Laboratories, Inc.

Y

Yang He

Y

Yunsong Chang

Jecho Biopharmaceuticals Co., Ltd

H

Huifang Zong

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

H

Haoneng Tang

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

L

Lei Wang

Y

Yong Ke

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

H

Huiyu Cai

BioGeometry

P

Ping Li

J

Jian Tang

H

Hua Chen

Department of Chemical Engineering, Delft University of Technology, Van der Maasweg 9, 2629 HZ Delft, The Netherlands

A

Aleksandra Drelich

Department of Microbiology & Immunology Centers for Biodefense and Emerging Diseases, The University of Texas Medical Branch at Galveston, 301 University Boulevard, Galveston, Texas 77555, United States

B

Bi-Hung Peng

Department of Neurosciences, Cell Biology, and Anatomy, University of Texas Medical Branch

J

Jason Hsu

Department of Neurosciences, Cell Biology, and Anatomy, University of Texas Medical Branch

V

Vivian Tat

Department of Pathology, University of Texas Medical Branch

C

Chien-Te K. Tseng

Department of Microbiology and Immunology, University of Texas Medical Branch

J

Jingjing Song

Jecho Biopharmaceuticals Co., Ltd

Y

Yunsheng Yuan

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

M

Mingyuan Wu

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

J

Junjun Liu

Techshake Biotechnology Co., Ltd., Xi’an, Shaanxi, China.

Y

Yali Yue

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

X

Xiaoju Zhang

Department of Respiratory and Critical Care Medicine, Henan Provincial People’s Hospital, University People’s Hospital

Z

Ziqi Wang

Division of Advanced Materials

L

Li Yang

J

Jing Li

X

Xiaodan Ni

Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park

H

Hongshi Li

Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park

Y

Yuning Xiang

Shuimu BioSciences Ltd. F4, Bio² Innovation Center, Life Science Park

Y

Yanlin Bian

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

B

Baohong Zhang

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

H

Haiyang Yin

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University

D

Dimiter S. Dimitrov

Center for Antibody Therapeutics, University of Pittsburgh School of Medicine

J

John Gilly

Jecho Biopharmaceuticals Co., Ltd

L

Lei Han

H

Hua Jiang

Y

Yueqing Xie

Jecho Laboratories, Inc.

J

Jianwei Zhu

Engineering Research Center of Cell and Therapeutic Antibody, Ministry of Education, School of Pharmacy, Shanghai Jiao Tong University