Different Neutralization Sensitivity of SARS-CoV-2 Cell-to-Cell and Cell-Free Modes of Infection to Convalescent Sera
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Abstract
The COVID-19 pandemic caused by SARS-CoV-2 has posed a global threat to human lives and economics. One of the best ways to determine protection against the infection is to quantify the neutralizing activity of serum antibodies. Multiple assays have been developed to validate SARS-CoV-2 neutralization; most of them utilized lentiviral or vesicular stomatitis virus-based particles pseudotyped with the spike (S) protein, making them safe and acceptable to work with in many labs. However, these systems are only capable of measuring infection with purified particles. This study has developed a pseudoviral assay with replication-dependent reporter vectors that can accurately quantify the level of infection directly from the virus producing cell to the permissive target cell. Comparative analysis of cell-free and cell-to-cell infection revealed that the neutralizing activity of convalescent sera was more than tenfold lower in cell cocultures than in the cell-free mode of infection. As the pseudoviral system could not properly model the mechanisms of SARS-CoV-2 transmission, similar experiments were performed with replication-competent coronavirus, which detected nearly complete SARS-CoV-2 cell-to-cell infection resistance to neutralization by convalescent sera. These findings suggest that the cell-to-cell mode of SARS-CoV-2 transmission, for which the mechanisms are largely unknown, could be of great importance for treatment and prevention of COVID-19.
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Differences in neutralization sensitivity were more pronounced when infection tests used replication-competent coronavirus.
“The observed differences were even more pronounced when infection tests were performed using replication-competent coronavirus [33].”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [33]
Cell-to-cell infection of SARS-CoV-2 pseudotyped HIV-1 was about one order of magnitude less sensitive to neutralization by convalescent sera than cell-free infection.
“Recently, we pseudotyped HIV-1 particles with SARS-CoV-2 protein S, and, using the HIV-1 replication-dependent reporter vector, inLuc, demonstrated that the cell-to-cell infection of SARS-CoV-2 was about one order of magnitude less sensitive to neutralization by convalescent sera than cell-free infection.”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [33]
Cell contact-mediated infection is resistant to neutralizing antibodies, demonstrated for HIV-1 and SARS-CoV-2.
“The importance of the cell-to-cell transmission mechanism for viral dissemination is evidenced by the resistance of cell contact-mediated infection to neutralizing antibodies, which has been demonstrated for HIV-1 [140] and SARS-CoV-2 [33,141].”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [33]
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HIV-1 cell-to-cell transmission and broadly neutralizing antibodies
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Topographic Changes in SARS Coronavirus–infected Cells at Late Stages of Infection
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Kinder, J. T., Moncman, C. L., Barrett, C. T., Jin, H., Kallewaard, N. L., & Dutch, R. (2020) · Journal of Virology · doi:10.1128/jvi.01068-20 · Cited by 39 · see citing works
Merwaiss, F., Czibener, C., & Alvarez, D. E. (2018) · Journal of Virology · doi:10.1128/jvi.01776-18 · Cited by 36 · see citing works
Shunaeva, A., Potashnikova, D. M., Av, P., Mishina, A., Filatov, A. V., Nikolaitchik, O. A., Hu, W.-S., & Mazurov, D. V. (2015) · Journal of Virology · doi:10.1128/jvi.01940-15 · Cited by 27 · see citing works
Self-citationFu, X., Tao, L., & Zhang, X. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.12.007 · Cited by 24 · see citing works
Establishment of Murine Hybridoma Cells Producing Antibodies against Spike Protein of SARS-CoV-2
Антипова, Н. В., Larionova, T. D., Siniavin, A. E., Nikiforova, M. A., Gushchin, V. А., Бабиченко, И. И., Volkov, A. V., Shakhparonov, M. I., & Pavlyukov, M. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239167 · Cited by 15 · see citing works
Self-citationSiniavin, A. E., Nikiforova, M. A., Grinkina, S. D., Gushchin, V. А., Starkov, V. G., Osipov, A. V., Tsetlin, V. I., & Utkin, Y. N. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.12.426042 · Cited by 6 · see citing works
Self-citation
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2 of the 92 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
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HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread
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“The importance of the cell-to-cell transmission mechanism for viral dissemination is evidenced by the resistance of cell contact-mediated infection to neutralizing antibodies, which has been demonstrated for HIV-1 [140] and SARS-CoV-2 [33,141].”
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Antibody-mediated spike activation promotes cell-cell transmission of SARS-CoV-2
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Metalloprotease-Dependent S2′-Activation Promotes Cell–Cell Fusion and Syncytiation of SARS-CoV-2
Harte, J. V., Wakerlin, S. L., Lindsay, A. J., McCarthy, J. V., & Coleman-Vaughan, C. (2022) · Viruses · doi:10.3390/v14102094 · Cited by 11 · see citing works
Kostin, N. N., Bobik, T. V., Skryabin, G. A., Simonova, M. A., Knorre, V. D., Abrikosova, V. A., Mokrushina, Y. A., Smirnov, I. V., Aleshenko, N. L., Kruglova, N. A., et al. (2022) · Acta Naturae · doi:10.32607/actanaturae.11776 · Cited by 10 · see citing works
Self-citationIn vitro high-content tissue models to address precision medicine challenges
Afewerki, S., Stocco, T. D., Silva, A. D. R., Furtado, A. S. A., de Sousa, G. F., Ruiz‐Esparza, G. U., Webster, T. J., Marciano, F. R., Strømme, M., Zhang, Y. S., et al. (2022) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2022.101108 · Cited by 8 · see citing works
Developing inhibitory peptides against SARS-CoV-2 envelope protein
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A Tiny Viral Protein, SARS-CoV-2-ORF7b: Functional Molecular Mechanisms
Mansueto, G., Fusco, G., & Colonna, G. (2024) · Biomolecules · doi:10.3390/biom14050541 · Cited by 8 · see citing works
SARS-CoV-2 Binding and Neutralization Properties of Peptides Derived from N-Terminus of Human ACE2
Astrakhantseva, I. V., Ershova, A. E., Chuvpilo, S. A., Kruglova, N. A., Ishmukhametov, A. A., Drutskaya, M. S., Kozlovskaya, L. I., & Nedospasov, S. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24098269 · Cited by 5 · see citing works
Self-citationMazurov, D. V., & Herschhorn, A. (2023) · mBio · doi:10.1128/mbio.02428-23 · Cited by 5 · see citing works
Self-citationCai, Y., Zhao, Z., & Zhuge, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1257953 · Cited by 4 · see citing works
Human ACE2 protein is a molecular switch controlling the mode of SARS-CoV-2 transmission
Yang, C. S., Liao, C., Hsu, H.-W., Liang, J., Chang, C.-S., Ko, H., Chang, R.-H., Tang, W., Chang, M.-H., Wang, I.-H., et al. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00980-w · Cited by 4 · see citing works
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Self-citationOn Immunological Studies at Sirius University of Science and Technology
Astrakhantseva, I. V., Krut’, V. G., Chuvpilo, S. A., Shevyrev, D., Shumeev, A. N., Александрович, Р. С., & Nedospasov, S. A. (2023) · Molecular Biology · doi:10.1134/s0026893323020036 · Cited by 3 · see citing works
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Immunoliposomes As a Promising Antiviral Agent against SARS-CoV-2
Bobik, T. V., Simonova, M. A., Rushkevich, N. Y., Kostin, N. N., Skryabin, G. A., Knorre, V. D., Schulga, A. A., Коновалова, Е. В., Proshkina, G. M., Gabibov, A. G., et al. (2024) · Doklady Biochemistry and Biophysics · doi:10.1134/s1607672923700618 · Cited by 1 · see citing works
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About Immunological Studies in “Sirius” University
Astrakhantseva, I. V., Krut’, V. G., Chuvpilo, S. A., Shevyrev, D., Shumeev, A. N., Александрович, Р. С., & Недоспасов, С. А. (2023) · Molecular Biology · doi:10.31857/s0026898423020039
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- Authors
- Kruglova, N., Siniavin, A., Gushchin, V., & Mazurov, D.
- Affiliations
- Institute of Gene Biology (RU)
- Russian Academy of Sciences (RU)
- Ministry of Health of the Russian Federation (RU)
- Corresponding author
- Mazurov, Dmitriy
- Venue
- Viruses
- Publisher
- MDPI AG
- Published
- 2021-06-12
- Volume
- 13
- Issue
- 6
- Pages
- 1133
- ISSN
- 1999-4915 (ISSN-L)
- PMC
- PMC8231521
- OpenAlex
- W3170524766
- Cited by
- 37
- References
- 92
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 10 · 2023: 8 · 2022: 8 · 2021: 6
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Viruses (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ministry of Science and Higher Education of Russian Federation (075-15-2019-1661)
- 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
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 detection and testing
- Keywords
- SARS-CoV-2, neutralizing antibodies, convalescent sera, cell-to-cell transmission, cell-free transmission, spike protein, COVID-19 pandemic
- MeSH terms
- SARS-CoV-2, Antibodies, Viral, Convalescence, Humans, Neutralization Tests, Genes, Reporter, Antibodies, Neutralizing, HEK293 Cells
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