Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants

Yuan, Meng; Huang, Deli; Lee, Chang-Chun D.; Wu, Nicholas C.; Jackson, Abigail M.; Zhu, Xueyong; Liu, Hejun; Peng, Linghang; van Gils, Marit J.; Sanders, Rogier W.; Burton, Dennis R.; Reincke, S. Momsen; Pruss, Harald; Kreye, Jakob; Nemazee, David; Ward, Andrew B.; Wilson, Ian A.

doi:10.1126/science.abh1139

Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants

Journal Article · 01 August 2021 · Science

DOI:https://doi.org/10.1126/science.abh1139· OSTI ID:1831202

Yuan, Meng; Huang, Deli; Lee, Chang-Chun D.; Wu, Nicholas C.; Jackson, Abigail M.; Zhu, Xueyong; Liu, Hejun; Peng, Linghang; van Gils, Marit J.; Sanders, Rogier W.; Burton, Dennis R.; Reincke, S. Momsen; Pruss, Harald; Kreye, Jakob; Nemazee, David; Ward, Andrew B.; Wilson, Ian A.

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: DOE - Office Of Science; National Institutes of Health (NIH); OTHER

OSTI ID:: 1831202

Journal Information:: Science, Vol. 373

Country of Publication:: United States

Language:: ENGLISH

References (97)

In vitro and in vivo functions of SARS-CoV-2 infection-enhancing and neutralizing antibodies No authors listed Cell https://doi.org/10.1016/j.cell.2021.06.021		August 2021
Serum Neutralizing Activity Elicited by mRNA-1273 Vaccine No authors listed New England Journal of Medicine https://doi.org/10.1056/NEJMc2102179		April 2021
mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants No authors listed Nature https://doi.org/10.1038/s41586-021-03324-6		February 2021
CoV-AbDab: the coronavirus antibody database No authors listed Bioinformatics https://doi.org/10.1093/bioinformatics/btaa739		August 2020
Cross-Reactive Neutralizing Antibody Responses Elicited by SARS-CoV-2 501Y.V2 (B.1.351) No authors listed New England Journal of Medicine https://doi.org/10.1056/NEJMc2104192		April 2021
Antibody evasion by the P.1 strain of SARS-CoV-2 No authors listed Cell https://doi.org/10.1016/j.cell.2021.03.055		March 2021
Structural analysis of full-length SARS-CoV-2 spike protein from an advanced vaccine candidate No authors listed Science https://doi.org/10.1126/science.abe1502		October 2020
Complete Mapping of Mutations to the SARS-CoV-2 Spike Receptor-Binding Domain that Escape Antibody Recognition No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2020.11.007		January 2021
Infection- and vaccine-induced antibody binding and neutralization of the B.1.351 SARS-CoV-2 variant No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2021.03.009		April 2021
SARS-CoV-2 variant B.1.1.7 is susceptible to neutralizing antibodies elicited by ancestral spike vaccines No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2021.03.002		April 2021
Cryo-electron microscopy structures of the N501Y SARS-CoV-2 spike protein in complex with ACE2 and 2 potent neutralizing antibodies No authors listed PLOS Biology https://doi.org/10.1371/journal.pbio.3001237		April 2021
SARS-CoV-2 neutralizing antibody structures inform therapeutic strategies No authors listed Nature https://doi.org/10.1038/s41586-020-2852-1		October 2020
Multi-clonal SARS-CoV-2 neutralization by antibodies isolated from severe COVID-19 convalescent donors No authors listed PLOS Pathogens https://doi.org/10.1371/journal.ppat.1009165		February 2021
Structural basis for accommodation of emerging B.1.351 and B.1.1.7 variants by two potent SARS-CoV-2 neutralizing antibodies No authors listed Structure https://doi.org/10.1016/j.str.2021.05.014		July 2021
New tools for automated high-resolution cryo-EM structure determination in RELION-3 No authors listed eLife https://doi.org/10.7554/eLife.42166		November 2018
A Highly Conserved Neutralizing Epitope on Group 2 Influenza A Viruses No authors listed Science https://doi.org/10.1126/science.1204839		July 2011
Cross-Neutralization of a SARS-CoV-2 Antibody to a Functionally Conserved Site Is Mediated by Avidity No authors listed Immunity https://doi.org/10.1016/j.immuni.2020.10.023		December 2020
Structures of Human Antibodies Bound to SARS-CoV-2 Spike Reveal Common Epitopes and Recurrent Features of Antibodies No authors listed Cell https://doi.org/10.1016/j.cell.2020.06.025		August 2020
Inference of Macromolecular Assemblies from Crystalline State No authors listed Journal of Molecular Biology https://doi.org/10.1016/j.jmb.2007.05.022		September 2007
UCSF Chimera?A visualization system for exploratory research and analysis No authors listed Journal of Computational Chemistry https://doi.org/10.1002/jcc.20084		January 2004
Deep Mutational Scanning of SARS-CoV-2 Receptor Binding Domain Reveals Constraints on Folding and ACE2 Binding No authors listed Cell https://doi.org/10.1016/j.cell.2020.08.012		September 2020
A panel of human neutralizing mAbs targeting SARS-CoV-2 spike at multiple epitopes No authors listed Nature Communications https://doi.org/10.1038/s41467-020-18159-4		August 2020
Rational development of a human antibody cocktail that deploys multiple functions to confer Pan-SARS-CoVs protection No authors listed Cell Research https://doi.org/10.1038/s41422-020-00444-y		December 2020
Recognition of the SARS-CoV-2 receptor binding domain by neutralizing antibodies No authors listed Biochemical and Biophysical Research Communications https://doi.org/10.1016/j.bbrc.2020.10.012		January 2021
SARS-CoV-2 RBD antibodies that maximize breadth and resistance to escape No authors listed Nature https://doi.org/10.1038/s41586-021-03807-6		July 2021
Enhancement versus neutralization by SARS-CoV-2 antibodies from a convalescent donor associates with distinct epitopes on the RBD No authors listed Cell Reports https://doi.org/10.1016/j.celrep.2021.108699		February 2021
Escape of SARS-CoV-2 501Y.V2 from neutralization by convalescent plasma No authors listed Nature https://doi.org/10.1038/s41586-021-03471-w		March 2021
GISAID: Global initiative on sharing all influenza data – from vision to reality No authors listed Eurosurveillance https://doi.org/10.2807/1560-7917.ES.2017.22.13.30494		March 2017
mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection No authors listed Science https://doi.org/10.1126/science.abg9175		March 2021
Individual Variation in the Germline Ig Gene Repertoire Inferred from Variable Region Gene Rearrangements No authors listed The Journal of Immunology https://doi.org/10.4049/jimmunol.1000445		May 2010
Cross-reactive coronavirus antibodies with diverse epitope specificities and Fc effector functions No authors listed Cell Reports Medicine https://doi.org/10.1016/j.xcrm.2021.100313		June 2021
Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen No authors listed Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1707304114		August 2017
Detection of a SARS-CoV-2 variant of concern in South Africa No authors listed Nature https://doi.org/10.1038/s41586-021-03402-9		March 2021
Structural basis for potent neutralization of SARS-CoV-2 and role of antibody affinity maturation No authors listed Nature Communications https://doi.org/10.1038/s41467-020-19231-9		October 2020
PHENIX: a comprehensive Python-based system for macromolecular structure solution No authors listed Acta Crystallographica Section D Biological Crystallography https://doi.org/10.1107/S0907444909052925		January 2010
Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies No authors listed Nature Medicine https://doi.org/10.1038/s41591-021-01318-5		March 2021
Cross-neutralization of SARS-CoV-2 by a human monoclonal SARS-CoV antibody No authors listed Nature https://doi.org/10.1038/s41586-020-2349-y		May 2020
Ultrapotent antibodies against diverse and highly transmissible SARS-CoV-2 variants No authors listed Science https://doi.org/10.1126/science.abh1766		July 2021
Ultrapotent human antibodies protect against SARS-CoV-2 challenge via multiple mechanisms No authors listed Science https://doi.org/10.1126/science.abe3354		September 2020
[20] Processing of X-ray diffraction data collected in oscillation mode No authors listed Macromolecular Crystallography Part A https://doi.org/10.1016/S0076-6879(97)76066-X		January 1997
SARS-CoV-2 501Y.V2 escapes neutralization by South African COVID-19 donor plasma No authors listed Nature Medicine https://doi.org/10.1038/s41591-021-01285-x		March 2021
Potent neutralizing antibodies against multiple epitopes on SARS-CoV-2 spike No authors listed Nature https://doi.org/10.1038/s41586-020-2571-7		July 2020
An Alternative Binding Mode of IGHV3-53 Antibodies to the SARS-CoV-2 Receptor Binding Domain No authors listed Cell Reports https://doi.org/10.1016/j.celrep.2020.108274		October 2020
Neutralizing Activity of BNT162b2-Elicited Serum No authors listed New England Journal of Medicine https://doi.org/10.1056/NEJMc2102017		April 2021
Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants No authors listed eLife https://doi.org/10.7554/eLife.61312		October 2020
Modular basis for potent SARS-CoV-2 neutralization by a prevalent VH1-2-derived antibody class No authors listed Cell Reports https://doi.org/10.1016/j.celrep.2021.108950		April 2021
Human neutralizing antibodies elicited by SARS-CoV-2 infection No authors listed Nature https://doi.org/10.1038/s41586-020-2380-z		May 2020
Structurally Resolved SARS-CoV-2 Antibody Shows High Efficacy in Severely Infected Hamsters and Provides a Potent Cocktail Pairing Strategy No authors listed Cell https://doi.org/10.1016/j.cell.2020.09.035		November 2020
Mapping Neutralizing and Immunodominant Sites on the SARS-CoV-2 Spike Receptor-Binding Domain by Structure-Guided High-Resolution Serology No authors listed Cell https://doi.org/10.1016/j.cell.2020.09.037		November 2020
Comprehensive mapping of mutations in the SARS-CoV-2 receptor-binding domain that affect recognition by polyclonal human plasma antibodies No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2021.02.003		March 2021
A highly conserved cryptic epitope in the receptor binding domains of SARS-CoV-2 and SARS-CoV No authors listed Science https://doi.org/10.1126/science.abb7269		April 2020
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy No authors listed Journal of Structural Biology https://doi.org/10.1016/j.jsb.2009.01.004		May 2009
Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity No authors listed Cell https://doi.org/10.1016/j.cell.2021.03.013		April 2021
Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7 No authors listed Nature https://doi.org/10.1038/s41586-021-03398-2		March 2021
Appion: An integrated, database-driven pipeline to facilitate EM image processing No authors listed Journal of Structural Biology https://doi.org/10.1016/j.jsb.2009.01.002		April 2009
Emerging SARS-CoV-2 variants reduce neutralization sensitivity to convalescent sera and monoclonal antibodies No authors listed Cellular & Molecular Immunology https://doi.org/10.1038/s41423-021-00648-1		February 2021
Automated molecular microscopy: The new Leginon system No authors listed Journal of Structural Biology https://doi.org/10.1016/j.jsb.2005.03.010		July 2005
The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus No authors listed Nature Reviews Microbiology https://doi.org/10.1038/nrmicro1819		February 2008
Evidence of escape of SARS-CoV-2 variant B.1.351 from natural and vaccine-induced sera No authors listed Cell https://doi.org/10.1016/j.cell.2021.02.037		April 2021
Efficacy of ChAdOx1 nCoV-19 (AZD1222) vaccine against SARS-CoV-2 variant of concern 202012/01 (B.1.1.7): an exploratory analysis of a randomised controlled trial No authors listed The Lancet https://doi.org/10.1016/S0140-6736(21)00628-0		April 2021
The antigenic anatomy of SARS-CoV-2 receptor binding domain No authors listed Cell https://doi.org/10.1016/j.cell.2021.02.032		April 2021
Neutralization of Variant Under Investigation B.1.617.1 With Sera of BBV152 Vaccinees No authors listed Clinical Infectious Diseases https://doi.org/10.1093/cid/ciab411		May 2021
A Therapeutic Non-self-reactive SARS-CoV-2 Antibody Protects from Lung Pathology in a COVID-19 Hamster Model No authors listed Cell https://doi.org/10.1016/j.cell.2020.09.049		November 2020
Potent Neutralizing Antibodies against SARS-CoV-2 Identified by High-Throughput Single-Cell Sequencing of Convalescent Patients’ B Cells No authors listed Cell https://doi.org/10.1016/j.cell.2020.05.025		July 2020
Human-IgG-Neutralizing Monoclonal Antibodies Block the SARS-CoV-2 Infection No authors listed Cell Reports https://doi.org/10.1016/j.celrep.2020.107918		July 2020
Sensitivity of SARS-CoV-2 B.1.1.7 to mRNA vaccine-elicited antibodies No authors listed Nature https://doi.org/10.1038/s41586-021-03412-7		March 2021
Analysis of SARS-CoV-2 variant mutations reveals neutralization escape mechanisms and the ability to use ACE2 receptors from additional species No authors listed Immunity https://doi.org/10.1016/j.immuni.2021.06.003		July 2021
A noncompeting pair of human neutralizing antibodies block COVID-19 virus binding to its receptor ACE2 No authors listed Science https://doi.org/10.1126/science.abc2241		May 2020
Cross-Reactive SARS-CoV-2 Neutralizing Antibodies From Deep Mining of Early Patient Responses No authors listed Frontiers in Immunology https://doi.org/10.3389/fimmu.2021.678570		June 2021
Structural basis of a shared antibody response to SARS-CoV-2 No authors listed Science https://doi.org/10.1126/science.abd2321		July 2020
A human neutralizing antibody targets the receptor-binding site of SARS-CoV-2 No authors listed Nature https://doi.org/10.1038/s41586-020-2381-y		May 2020
Acquisition of the L452R Mutation in the ACE2-Binding Interface of Spike Protein Triggers Recent Massive Expansion of SARS-CoV-2 Variants No authors listed Journal of Clinical Microbiology https://doi.org/10.1128/JCM.00921-21		October 2021
Structure-based design of prefusion-stabilized SARS-CoV-2 spikes No authors listed Science https://doi.org/10.1126/science.abd0826		July 2020
Studies in humanized mice and convalescent humans yield a SARS-CoV-2 antibody cocktail No authors listed Science https://doi.org/10.1126/science.abd0827		June 2020
SARS-CoV-2 evolution in an immunocompromised host reveals shared neutralization escape mechanisms No authors listed Cell https://doi.org/10.1016/j.cell.2021.03.027		May 2021
Neutralization of SARS-CoV-2 spike 69/70 deletion, E484K and N501Y variants by BNT162b2 vaccine-elicited sera No authors listed Nature Medicine https://doi.org/10.1038/s41591-021-01270-4		February 2021
Resistance of SARS-CoV-2 variants to neutralization by monoclonal and serum-derived polyclonal antibodies No authors listed Nature Medicine https://doi.org/10.1038/s41591-021-01294-w		March 2021
Features and development of Coot No authors listed Acta Crystallographica Section D Biological Crystallography https://doi.org/10.1107/S0907444910007493		March 2010
Antibody neutralization of SARS-CoV-2 through ACE2 receptor mimicry No authors listed Nature Communications https://doi.org/10.1038/s41467-020-20501-9		January 2021
Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor No authors listed Nature https://doi.org/10.1038/s41586-020-2180-5		March 2020
Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein No authors listed Cell https://doi.org/10.1016/j.cell.2020.02.058		April 2020
Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model No authors listed Science https://doi.org/10.1126/science.abc7520		June 2020
Convergent antibody responses to SARS-CoV-2 in convalescent individuals No authors listed Nature https://doi.org/10.1038/s41586-020-2456-9		June 2020
A Rapid and Efficient Screening System for Neutralizing Antibodies and Its Application for SARS-CoV-2 No authors listed Frontiers in Immunology https://doi.org/10.3389/fimmu.2021.653189		March 2021
A neutralizing human antibody binds to the N-terminal domain of the Spike protein of SARS-CoV-2 No authors listed Science https://doi.org/10.1126/science.abc6952		June 2020
Structurally resolved SARS-CoV-2 antibody shows high efficacy in severely infected hamsters and provides a potent cocktail pairing strategy. Du et al No authors listed Mendeley https://doi.org/10.17632/ssxn5c6k59.1		January 2020
Increased resistance of SARS-CoV-2 variant P.1 to antibody neutralization No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2021.04.007		May 2021
SARS-CoV-2 variants B.1.351 and P.1 escape from neutralizing antibodies No authors listed Cell https://doi.org/10.1016/j.cell.2021.03.036		April 2021
Rapid isolation and profiling of a diverse panel of human monoclonal antibodies targeting the SARS-CoV-2 spike protein No authors listed Nature Medicine https://doi.org/10.1038/s41591-020-0998-x		July 2020
A combination of cross-neutralizing antibodies synergizes to prevent SARS-CoV-2 and SARS-CoV pseudovirus infection No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2021.04.005		May 2021
Persistence and Evolution of SARS-CoV-2 in an Immunocompromised Host No authors listed New England Journal of Medicine https://doi.org/10.1056/NEJMc2031364		December 2020
Analysis of a SARS-CoV-2-Infected Individual Reveals Development of Potent Neutralizing Antibodies with Limited Somatic Mutation No authors listed Immunity https://doi.org/10.1016/j.immuni.2020.06.001		July 2020
Longitudinal Isolation of Potent Near-Germline SARS-CoV-2-Neutralizing Antibodies from COVID-19 Patients No authors listed Cell https://doi.org/10.1016/j.cell.2020.06.044		August 2020
Projecting the transmission dynamics of SARS-CoV-2 through the postpandemic period No authors listed Science https://doi.org/10.1126/science.abb5793		April 2020
Phaser crystallographic software No authors listed Journal of Applied Crystallography https://doi.org/10.1107/S0021889807021206		July 2007
Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability No authors listed Science https://doi.org/10.1126/science.abc5902		June 2020
Paired heavy- and light-chain signatures contribute to potent SARS-CoV-2 neutralization in public antibody responses No authors listed Cell Reports https://doi.org/10.1016/j.celrep.2021.109771		October 2021

Cited By (5)

Additional file 2 of Characterization of SARS-CoV-2 worldwide transmission based on evolutionary dynamics and specific viral mutations in the spike protein No authors listed figshare https://doi.org/10.6084/m9.figshare.16305775.v1		January 2021
Additional file 4 of Characterization of SARS-CoV-2 worldwide transmission based on evolutionary dynamics and specific viral mutations in the spike protein No authors listed figshare https://doi.org/10.6084/m9.figshare.16305781.v1		January 2021
Additional file 3 of Characterization of SARS-CoV-2 worldwide transmission based on evolutionary dynamics and specific viral mutations in the spike protein No authors listed figshare https://doi.org/10.6084/m9.figshare.16305778.v1		January 2021
Additional file 5 of Characterization of SARS-CoV-2 worldwide transmission based on evolutionary dynamics and specific viral mutations in the spike protein No authors listed figshare https://doi.org/10.6084/m9.figshare.16305784.v1		January 2021
Additional file 6 of Characterization of SARS-CoV-2 worldwide transmission based on evolutionary dynamics and specific viral mutations in the spike protein No authors listed figshare https://doi.org/10.6084/m9.figshare.16305787		January 2021

Similar Records

Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants

Journal Article · 2021 · Science · OSTI ID:1832585

Yuan, Meng; Huang, Deli; Lee, Chang-Chun D.; +14 more

Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants

Journal Article · 2021 · Science · OSTI ID:1784370

Yuan, Meng; Huang, Deli; Lee, Chang-Chun D.; +14 more

Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants

Citation Formats

References (97)

Cited By (5)

Similar Records

Related Subjects