Antigenic cartography of SARS-CoV-2 reveals that Omicron BA.1 and BA.2 are antigenically distinct

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Abstract

The emergence and rapid spread of SARS-CoV-2 variants may impact vaccine efficacy significantly. The Omicron variant termed BA.2, which differs substantially from BA.1 based on genetic sequence, is currently replacing BA.1 in several countries, but its antigenic characteristics have not yet been assessed. Here, we used antigenic cartography to quantify and visualize antigenic differences between early SARS-CoV-2 variants (614G, Alpha, Beta, Gamma, Zeta, Delta and Mu) using hamster antisera obtained after primary infection. We first verified that the choice of the cell line for the neutralization assay did not affect the topology of the map substantially. Antigenic maps generated using pseudotyped SARS-CoV-2 on the widely used VeroE6 cell line and the human airway cell line Calu-3 generated similar maps. Maps made using authentic SARS-CoV-2 on Calu-3 cells also closely resembled those generated with pseudotyped viruses. The antigenic maps revealed a central cluster of SARS-CoV-2 variants, which grouped based on mutual spike mutations. Whereas these early variants are antigenically similar, clustering relatively close to each other in antigenic space, Omicron BA.1 and BA.2 have evolved as two distinct antigenic outliers. Our data show that BA.1 and BA.2 both escape vaccine-induced antibody responses as a result of different antigenic characteristics. Thus, antigenic cartography could be used to assess antigenic properties of future SARS-CoV-2 variants of concern that emerge and to decide on the composition of novel spike-based (booster) vaccines.

Abstract

Antigenic evolution by SARS-CoV-2 can be monitored by antigenic cartography, informing future coronavirus vaccine strain selections.

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Most cited references 36

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Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR

Victor M Corman, Olfert Landt, Marco Kaiser … (2020)

Background The ongoing outbreak of the recently emerged novel coronavirus (2019-nCoV) poses a challenge for public health laboratories as virus isolates are unavailable while there is growing evidence that the outbreak is more widespread than initially thought, and international spread through travellers does already occur. Aim We aimed to develop and deploy robust diagnostic methodology for use in public health laboratory settings without having virus material available. Methods Here we present a validated diagnostic workflow for 2019-nCoV, its design relying on close genetic relatedness of 2019-nCoV with SARS coronavirus, making use of synthetic nucleic acid technology. Results The workflow reliably detects 2019-nCoV, and further discriminates 2019-nCoV from SARS-CoV. Through coordination between academic and public laboratories, we confirmed assay exclusivity based on 297 original clinical specimens containing a full spectrum of human respiratory viruses. Control material is made available through European Virus Archive – Global (EVAg), a European Union infrastructure project. Conclusion The present study demonstrates the enormous response capacity achieved through coordination of academic and public laboratories in national and European research networks.

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Tracking changes in SARS-CoV-2 Spike: evidence that D614G increases infectivity of the COVID-19 virus

B Korber, W.M. Fischer, S. Gnanakaran … (2020)

Summary A SARS-CoV-2 variant carrying the Spike protein amino acid change D614G has become the most prevalent form in the global pandemic. Dynamic tracking of variant frequencies revealed a recurrent pattern of G614 increase at multiple geographic levels: national, regional and municipal. The shift occurred even in local epidemics where the original D614 form was well established prior to the introduction of the G614 variant. The consistency of this pattern was highly statistically significant, suggesting that the G614 variant may have a fitness advantage. We found that the G614 variant grows to higher titer as pseudotyped virions. In infected individuals G614 is associated with lower RT-PCR cycle thresholds, suggestive of higher upper respiratory tract viral loads, although not with increased disease severity. These findings illuminate changes important for a mechanistic understanding of the virus, and support continuing surveillance of Spike mutations to aid in the development of immunological interventions.

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Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization

Delphine Planas, David Veyer, Artem Baidaliuk … (2021)

The SARS-CoV-2 B.1.617 lineage was identified in October 2020 in India1-5. Since then, it has become dominant in some regions of India and in the UK, and has spread to many other countries6. The lineage includes three main subtypes (B1.617.1, B.1.617.2 and B.1.617.3), which contain diverse mutations in the N-terminal domain (NTD) and the receptor-binding domain (RBD) of the SARS-CoV-2 spike protein that may increase the immune evasion potential of these variants. B.1.617.2-also termed the Delta variant-is believed to spread faster than other variants. Here we isolated an infectious strain of the Delta variant from an individual with COVID-19 who had returned to France from India. We examined the sensitivity of this strain to monoclonal antibodies and to antibodies present in sera from individuals who had recovered from COVID-19 (hereafter referred to as convalescent individuals) or who had received a COVID-19 vaccine, and then compared this strain with other strains of SARS-CoV-2. The Delta variant was resistant to neutralization by some anti-NTD and anti-RBD monoclonal antibodies, including bamlanivimab, and these antibodies showed impaired binding to the spike protein. Sera collected from convalescent individuals up to 12 months after the onset of symptoms were fourfold less potent against the Delta variant relative to the Alpha variant (B.1.1.7). Sera from individuals who had received one dose of the Pfizer or the AstraZeneca vaccine had a barely discernible inhibitory effect on the Delta variant. Administration of two doses of the vaccine generated a neutralizing response in 95% of individuals, with titres three- to fivefold lower against the Delta variant than against the Alpha variant. Thus, the spread of the Delta variant is associated with an escape from antibodies that target non-RBD and RBD epitopes of the spike protein.

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Author and article information

Contributors

Anna Z. Mykytyn:

ORCID: https://orcid.org/0000-0001-7188-6871

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Melanie Rissmann:

ORCID: https://orcid.org/0000-0002-5298-5919

Role: Formal analysisRole: InvestigationRole: ResourcesRole: ValidationRole: Writing - review & editing

Adinda Kok:

ORCID: https://orcid.org/0000-0003-3635-7952

Role: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing - review & editing

Miruna E. Rosu:

ORCID: https://orcid.org/0000-0003-3469-7822

Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing - review & editing

Debby Schipper:

ORCID: https://orcid.org/0000-0001-6449-4765

Role: Investigation

Tim I. Breugem:

ORCID: https://orcid.org/0000-0002-5558-7043

Role: Investigation

Petra B. van den Doel:

ORCID: https://orcid.org/0000-0002-5735-5537

Role: Investigation

Felicity Chandler:

ORCID: https://orcid.org/0000-0002-3465-6409

Role: Resources

Theo Bestebroer: Role: InvestigationRole: MethodologyRole: ValidationRole: Writing - review & editing

Maurice de Wit:

ORCID: https://orcid.org/0000-0003-0449-8822

Role: Formal analysisRole: InvestigationRole: Resources

Martin E. van Royen:

ORCID: https://orcid.org/0000-0002-6814-0996

Role: Formal analysisRole: InvestigationRole: Resources

Richard Molenkamp:

ORCID: https://orcid.org/0000-0002-9004-3850

Role: InvestigationRole: ResourcesRole: Writing - review & editing

Bas B. Oude Munnink:

ORCID: https://orcid.org/0000-0002-9394-1189

Role: ConceptualizationRole: Resources

Rory D. de Vries:

ORCID: https://orcid.org/0000-0003-2817-0127

Role: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing - review & editing

Corine GeurtsvanKessel:

ORCID: https://orcid.org/0000-0002-7678-314X

Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ResourcesRole: Supervision

Derek J. Smith:

ORCID: https://orcid.org/0000-0002-2393-1890

Role: MethodologyRole: ResourcesRole: SoftwareRole: Writing - review & editing

Marion P. G. Koopmans:

ORCID: https://orcid.org/0000-0002-5204-2312

Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing - review & editing

Barry Rockx:

ORCID: https://orcid.org/0000-0003-2463-027X

Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing - review & editing

Mart M. Lamers:

ORCID: https://orcid.org/0000-0002-1431-4022

Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Ron Fouchier:

ORCID: https://orcid.org/0000-0001-8095-2869

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: Writing - review & editing

Bart L. Haagmans:

ORCID: https://orcid.org/0000-0001-6221-2015

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Immunol

Journal ID (iso-abbrev): Sci Immunol

Journal ID (publisher-id): sciimmunol

Journal ID (hwp): immunology

Title: Science Immunology

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2470-9468

Publication date (Electronic, pub): 23 June 2022

Publication date PMC-release: 23 June 2022

Electronic Location Identifier: eabq4450

Affiliations

[ ¹ ]Viroscience Department, Erasmus Medical Center, Rotterdam, Netherlands.

[ ² ]Department of Neurology, Erasmus University Medical Center, Rotterdam, Netherlands

[ ³ ]Department of Pathology, Erasmus University Medical Center, Rotterdam, Netherlands.

[ ⁴ ]Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

Author notes

[†]

These authors contributed equally to this work.

[* ]Corresponding author. Email: b.haagmans@ 123456erasmusmc.nl

Author information

Anna Z. Mykytyn https://orcid.org/0000-0001-7188-6871

Melanie Rissmann https://orcid.org/0000-0002-5298-5919

Adinda Kok https://orcid.org/0000-0003-3635-7952

Miruna E. Rosu https://orcid.org/0000-0003-3469-7822

Debby Schipper https://orcid.org/0000-0001-6449-4765

Tim I. Breugem https://orcid.org/0000-0002-5558-7043

Petra B. van den Doel https://orcid.org/0000-0002-5735-5537

Felicity Chandler https://orcid.org/0000-0002-3465-6409

Maurice de Wit https://orcid.org/0000-0003-0449-8822

Martin E. van Royen https://orcid.org/0000-0002-6814-0996

Richard Molenkamp https://orcid.org/0000-0002-9004-3850

Bas B. Oude Munnink https://orcid.org/0000-0002-9394-1189

Rory D. de Vries https://orcid.org/0000-0003-2817-0127

Corine GeurtsvanKessel https://orcid.org/0000-0002-7678-314X

Derek J. Smith https://orcid.org/0000-0002-2393-1890

Marion P. G. Koopmans https://orcid.org/0000-0002-5204-2312

Barry Rockx https://orcid.org/0000-0003-2463-027X

Mart M. Lamers https://orcid.org/0000-0002-1431-4022

Ron Fouchier https://orcid.org/0000-0001-8095-2869

Bart L. Haagmans https://orcid.org/0000-0001-6221-2015

Article

Publisher ID: abq4450

DOI: 10.1126/sciimmunol.abq4450

PMC ID: 9273038

PubMed ID: 35737747

SO-VID: 2de7ab45-5856-4f95-900c-ef3895abba88

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 08 April 2022

Date accepted : 14 June 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: 75N93021C00014

Funded by: FundRef http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;

Award ID: 101003589

Funded by: FundRef , Health Holland;

Award ID: EMCLHS20017

Funded by: FundRef , Health Holland;

Award ID: LSHM19136

Funded by: FundRef , Netherlands Organization for Health Research and Development ZONMW;

Award ID: 10150062010008

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Antigenic cartography of SARS-CoV-2 reveals that Omicron BA.1 and BA.2 are antigenically distinct

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Novel Coronavirus Disease COVID-19

Most cited references 36

Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR

Tracking changes in SARS-CoV-2 Spike: evidence that D614G increases infectivity of the COVID-19 virus

Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization

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Cited by 54

Most referenced authors 2,659