Importance of Neutralizing Monoclonal Antibodies Targeting Multiple Antigenic Sites on the Middle East Respiratory Syndrome Coronavirus Spike Glycoprotein To Avoid Neutralization Escape
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Middle East respiratory syndrome coronavirus (MERS-CoV) causes a highly lethal pulmonary infection with ∼35% mortality. The potential for a future pandemic originating from animal reservoirs or health care-associated events is a major public health concern. There are no vaccines or therapeutic agents currently available for MERS-CoV. Using a probe-based single B cell cloning strategy, we have identified and characterized multiple neutralizing monoclonal antibodies (MAbs) specifically binding to the receptor-binding domain (RBD) or S1 (non-RBD) regions from a convalescent MERS-CoV-infected patient and from immunized rhesus macaques. RBD-specific MAbs tended to have greater neutralizing potency than non-RBD S1-specific MAbs. Six RBD-specific and five S1-specific MAbs could be sorted into four RBD and three non-RBD distinct binding patterns, based on competition assays, mapping neutralization escape variants, and structural analysis. We determined cocrystal structures for two MAbs targeting the RBD from different angles and show they can bind the RBD only in the “out” position. We then showed that selected RBD-specific, non-RBD S1-specific, and S2-specific MAbs given prophylactically prevented MERS-CoV replication in lungs and protected mice from lethal challenge. Importantly, combining RBD- and non-RBD MAbs delayed the emergence of escape mutations in a cell-based virus escape assay. These studies identify MAbs targeting different antigenic sites on S that will be useful for defining mechanisms of MERS-CoV neutralization and for developing more effective interventions to prevent or treat MERS-CoV infections. IMPORTANCE MERS-CoV causes a highly lethal respiratory infection for which no vaccines or antiviral therapeutic options are currently available. Based on continuing exposure from established reservoirs in dromedary camels and bats, transmission of MERS-CoV into humans and future outbreaks are expected. Using structurally defined probes for the MERS-CoV spike glycoprotein (S), the target for neutralizing antibodies, single B cells were sorted from a convalescent human and immunized nonhuman primates (NHPs). MAbs produced from paired immunoglobulin gene sequences were mapped to multiple epitopes within and outside the receptor-binding domain (RBD) and protected against lethal MERS infection in a murine model following passive immunization. Importantly, combining MAbs targeting distinct epitopes prevented viral neutralization escape from RBD-directed MAbs. These data suggest that antibody responses to multiple domains on CoV spike protein may improve immunity and will guide future vaccine and therapeutic development efforts.
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Polyclonal antibodies against multiple non-RBD spike epitopes might block viral attachment, add neutralizing activity, or prevent post-attachment fusion.
“A polyclonal antibody against multiple epitopes of the S protein beyond the RBD might, for example, inhibit viral attachment156–160, provide additional neutralizing activity161 and/or prevent post-attachment fusion162.”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [156]
A vaccine targeting multiple epitopes would reduce the chance of immune escape by mutation.
“A vaccine targeting multiple epitopes would also mitigate the possibility of immune escape by mutation156.”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [156]
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Self-citation
- Authors
- Wang, L., Shi, W., Chappell, J. D., Joyce, M. G., Zhang, Y., Kanekiyo, M., Becker, M. M., van Doremalen, N., Fischer, R., Wang, N., Corbett, K. S., Choe, M., Mason, R. D., Van Galen, J. G., Zhou, T., Saunders, K. O., Tatti, K. M., Haynes, L. M., Kwong, P. D., Modjarrad, K., Kong, W.-P., McLellan, J. S., Denison, M. R., Munster, V. J., Mascola, J. R., & Graham, B. S.
- Affiliations
- National Institutes of Health (US)
- Vanderbilt University Medical Center (US)
- Virus Ecology Unit, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA
- Dartmouth College (US)
- Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
- Centers for Disease Control and Prevention (US)
- ORCID
- Wang, Lingshu
- Shi, Wei
- Chappell, James D.
- Joyce, M. Gordon
- Zhang, Yi
- Kanekiyo, Masaru
- Fischer, Robert
- Wang, Nianshuang
- Corbett, Kizzmekia S.
- Choe, Misook
- Mason, Rosemarie D.
- Zhou, Tongqing
- Saunders, Kevin O.
- Tatti, Kathleen M.
- Kwong, Peter D.
- Modjarrad, Kayvon
- Kong, Wing-Pui
- McLellan, Jason S.
- Denison, Mark R.
- Munster, Vincent J.
- Mascola, John R.
- Graham, Barney S.
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2018-05-15
- Volume
- 92
- Issue
- 10
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC5923077
- OpenAlex
- W2790876064
- Cited by
- 169
- References
- 62
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 9 · 2023: 12 · 2022: 17 · 2021: 37 · 2020: 59 · 2019: 17 · 2018: 7
- FWCI
- 22.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- HHS | National Institutes of Health (Intramural funding, HHSN261200800001E Agreement No. 16x142)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
- Keywords
- MERS-CoV, neutralizing monoclonal antibodies, spike protein, receptor binding domain, neutralization escape, antibody epitopes, passive immunization, prophylaxis, rhesus monkeys, co-crystal structure, lung viral replication, Camelus dromedarius, bats
- MeSH terms
- Animals, Antibodies, Monoclonal, Antibodies, Viral, Humans, Macaca mulatta, Vaccination, Coronavirus Infections, Crystallography, X-Ray, Mice, Antibodies, Neutralizing, Spike Glycoprotein, Coronavirus, Middle East Respiratory Syndrome Coronavirus
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