Prior COVID-19 Immunization Does Not Cause IgA- or IgG-Dependent Enhancement of SARS-CoV-2 Infection
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cohorts
2.2. Cell Models
2.3. In Vitro Assay for Antibody-Dependent Enhancement (ADE)
2.4. SARS-CoV-2 RT-PCR for Viral Amplification
2.5. Live Virus Neutralization Experiments
2.6. Statistical Analysis
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Narayan, R.; Tripathi, S. Intrinsic ADE: The Dark Side of Antibody Dependent Enhancement During Dengue Infection. Front. Cell. Infect. Microbiol. 2020, 10, 580096. [Google Scholar] [CrossRef]
- Okuya, K.; Hattori, T.; Saito, T.; Takadate, Y.; Sasaki, M.; Furuyama, W.; Marzi, A.; Ohiro, Y.; Konno, S.; Hattori, T.; et al. Multiple Routes of Antibody-Dependent Enhancement of SARS-CoV-2 Infection. Microbiol. Spectr. 2022, 10, e01553-21. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Deng, T.; Zhang, Y.; Niu, W.; Nie, Q.; Yang, S.; Liu, P.; Pei, P.; Chen, L.; Li, H.; et al. ACE2 Can Act as the Secondary Receptor in the FcγR-Dependent ADE of SARS-CoV-2 Infection. iScience 2022, 25, 103720. [Google Scholar] [CrossRef]
- Shen, X.-R.; Li, Q.; Li, H.-L.; Wang, X.; Wang, Q.; Zheng, X.-S.; Geng, R.; Zhang, Y.-L.; Li, B.; Jiang, R.-D.; et al. Antibody-Dependent Enhancement of SARS-CoV-2 Infection of Human Immune Cells: In Vitro Assessment Provides Insight in COVID-19 Pathogenesis. Viruses 2021, 13, 2483. [Google Scholar] [CrossRef]
- Liu, Y.; Soh, W.T.; Kishikawa, J.-I.; Hirose, M.; Nakayama, E.E.; Li, S.; Sasai, M.; Suzuki, T.; Tada, A.; Arakawa, A.; et al. An infectivity-Enhancing Site on the SARS-CoV-2 Spike Protein Targeted by Antibodies. Cell 2021, 184, 3452–3466.e18. [Google Scholar] [CrossRef]
- Zhou, Y.; Liu, Z.; Li, S.; Xu, W.; Zhang, Q.; Silva, I.T.; Li, C.; Wu, Y.; Jiang, Q.; Liu, Z.; et al. Enhancement Versus Neutralization by SARS-CoV-2 Antibodies from a Convalescent Donor Associates with Distinct Epitopes on the RBD. Cell Rep. 2021, 34, 108699. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Edwards, R.J.; Manne, K.; Martinez, D.R.; Schäfer, A.; Alam, S.M.; Wiehe, K.; Lu, X.; Parks, R.; Sutherland, L.L.; et al. In Vitro and In Vivo Functions of SARS-CoV-2 Infection-Enhancing and Neutralizing Antibodies. Cell 2021, 184, 4203–4219.e32. [Google Scholar] [CrossRef]
- Li, D.; Luan, N.; Li, J.; Zhao, H.; Zhang, Y.; Long, R.; Jiang, G.; Fan, S.; Xu, X.; Cao, H.; et al. Waning Antibodies from Inactivated SARS-CoV-2 Vaccination Offer Protection against Infection without Antibody-Enhanced Immunopathology in Rhesus Macaque Pneumonia Models. Emerg. Microbes Infect. 2021, 10, 2194–2198. [Google Scholar] [CrossRef] [PubMed]
- Gao, Q.; Bao, L.; Mao, H.; Wang, L.; Xu, K.; Yang, M.; Li, Y.; Zhu, L.; Wang, N.; Lv, Z.; et al. Development of an Inactivated Vaccine Candidate for SARS-CoV-2. Science 2020, 369, 77–81. [Google Scholar] [CrossRef]
- Casadevall, A.; Pirofski, L.-A. The Convalescent Sera Option for Containing COVID-19. J. Clin. Investig. 2020, 130, 1545–1548. [Google Scholar] [CrossRef] [Green Version]
- Arvin, A.M.; Fink, K.; Schmid, M.A.; Cathcart, A.; Spreafico, R.; Havenar-Daughton, C.; Lanzavecchia, A.; Corti, D.; Virgin, H.W. A Perspective on Potential Antibody-Dependent Enhancement of SARS-CoV-2. Nature 2020, 584, 353–363. [Google Scholar] [CrossRef]
- Cele, S.; Jackson, L.; Khoury, D.S.; Khan, K.; Moyo-Gwete, T.; Tegally, H.; San, J.E.; Cromer, D.; Scheepers, C.; Amoako, D.G.; et al. Omicron Extensively but Incompletely Escapes Pfizer BNT162b2 Neutralization. Nature 2021, 602, 654–656. [Google Scholar] [CrossRef]
- Reynolds, C.J.; Gibbons, J.M.; Pade, C.; Lin, K.M.; Sandoval, D.M.; Pieper, F.; Butler, D.K.; Liu, S.; Otter, A.D.; Joy, G.; et al. Heterologous Infection and Vaccination Shapes Immunity against SARS-CoV-2 Variants. Science 2022, 375, 183–192. [Google Scholar] [CrossRef]
- Junqueira, C.; Crespo, Â.; Ranjbar, S.; De Lacerda, L.B.; Lewandrowski, M.; Ingber, J.; Parry, B.; Ravid, S.; Clark, S.; Schrimpf, M.R.; et al. FcγR-Mediated SARS-CoV-2 Infection of Monocytes Activates Inflammation. Nature 2022, 606, 576–584. [Google Scholar] [CrossRef] [PubMed]
- Lempp, F.A.; Soriaga, L.B.; Montiel-Ruiz, M.; Benigni, F.; Noack, J.; Park, Y.-J.; Bianchi, S.; Walls, A.C.; Bowen, J.E.; Zhou, J.; et al. Lectins Enhance SARS-CoV-2 Infection and Influence Neutralizing Antibodies. Nature 2021, 598, 342–347. [Google Scholar] [CrossRef] [PubMed]
- Clark, N.M.; Janaka, S.K.; Hartman, W.; Stramer, S.; Goodhue, E.; Weiss, J.; Evans, D.T.; Connor, J.P. Anti-SARS-CoV-2 IgG and IgA Antibodies in COVID-19 Convalescent Plasma Do Not Enhance Viral Infection. PLoS ONE 2022, 17, e0257930. [Google Scholar] [CrossRef] [PubMed]
- García-Nicolás, O.; V’kovski, P.; Zettl, F.; Zimmer, G.; Thiel, V.; Summerfield, A. No Evidence for Human Monocyte-Derived Macrophage Infection and Antibody-Mediated Enhancement of SARS-CoV-2 Infection. Front. Cell Infect. Microbiol. 2021, 11, 644574. [Google Scholar] [CrossRef]
- Noailly, B.; Yaugel-Novoa, M.; Werquin, J.; Jospin, F.; Drocourt, D.; Bourlet, T.; Rochereau, N.; Paul, S. Antiviral Activities of HIV-1-Specific Human Broadly Neutralizing Antibodies Are Isotype-Dependent. Vaccines 2022, 10, 903. [Google Scholar] [CrossRef]
- Pezzi, L.; Charrel, R.N.; Ninove, L.; Nougairede, A.; Molle, G.; Coutard, B.; Durand, G.; Leparc-Goffart, I.; De Lamballerie, X.; Thirion, L. Development and Evaluation of a Duo SARS-CoV-2 RT-QPCR Assay Combining Two Assays Approved by the World Health Organization Targeting the Envelope and the RNA-Dependant RNA Polymerase (RdRp) Coding Regions. Viruses 2020, 12, 686. [Google Scholar] [CrossRef]
- Corman, V.M.; Landt, O.; Kaiser, M.; Molenkamp, R.; Meijer, A.; Chu, D.K.W.; Bleicker, T.; Brünink, S.; Schneider, J.; Schmidt, M.L.; et al. Detection of 2019 Novel Coronavirus (2019-NCoV) by Real-Time RT-PCR. Eurosurveillance 2020, 25, 2000045. [Google Scholar] [CrossRef] [Green Version]
- Pozzetto, B.; Legros, V.; Djebali, S.; Barateau, V.; Guibert, N.; Villard, M.; Peyrot, L.; Allatif, O.; Fassier, J.-B.; Massardier-Pilonchéry, A.; et al. Immunogenicity and Efficacy of Heterologous ChAdOx1–BNT162b2 Vaccination. Nature 2021, 600, 701–706. [Google Scholar] [CrossRef]
- Crooks, C.M.; Weiler, A.M.; Rybarczyk, S.L.; Bliss, M.I.; Jaeger, A.S.; Murphy, M.E.; Simmons, H.A.; Mejia, A.; Fritsch, M.K.; Hayes, J.M.; et al. Previous Exposure to Dengue Virus is Associated with Increased Zika Virus Burden at the Maternal-Fetal Interface in Rhesus Macaques. PLoS Negl. Trop. Dis. 2021, 15, e0009641. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, J.; Sasaki, T.; Yamanaka, A.; Ichihara, Y.; Koketsu, R.; Samune, Y.; Cruz, P.; Sato, K.; Tanga, N.; Yoshimura, Y.; et al. The Potential of COVID-19 Patients’ Sera to Cause Antibody-Dependent Enhancement of Infection and IL-6 Production. Sci. Rep. 2021, 11, 23713. [Google Scholar] [CrossRef]
- Shimizu, J.; Sasaki, T.; Koketsu, R.; Morita, R.; Yoshimura, Y.; Murakami, A.; Saito, Y.; Kusunoki, T.; Samune, Y.; Nakayama, E.E.; et al. Reevaluation of Antibody-Dependent Enhancement of Infection in Anti-SARS-CoV-2 Therapeutic Antibodies and mRNA-Vaccine Antisera Using FcR- and ACE2-Positive Cells. Sci. Rep. 2022, 12, 15612. [Google Scholar] [CrossRef] [PubMed]
- Joyner, M.J.; Bruno, K.A.; Klassen, S.A.; Kunze, K.L.; Johnson, P.W.; Lesser, E.R.; Wiggins, C.C.; Senefeld, J.W.; Klompas, A.M.; Hodge, D.O.; et al. Safety Update: COVID-19 Convalescent Plasma in 20,000 Hospitalized Patients. Mayo Clin. Proc. 2020, 95, 1888–1897. [Google Scholar] [CrossRef] [PubMed]
Characteristics | Groups | ||
---|---|---|---|
Severe Disease (n = 19) | Mild/Asymptomatic Disease (n = 36) | Vaccinated (n = 26) | |
M/F sex ratio | 3.75 | 0.29 | 0.30 |
Age (years), median (IQR) | 70 (61.5–71.5) | 34 (29–40.3) | 85 (29–86) |
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Yaugel-Novoa, M.; Noailly, B.; Jospin, F.; Berger, A.-E.; Waeckel, L.; Botelho-Nevers, E.; Longet, S.; Bourlet, T.; Paul, S. Prior COVID-19 Immunization Does Not Cause IgA- or IgG-Dependent Enhancement of SARS-CoV-2 Infection. Vaccines 2023, 11, 773. https://doi.org/10.3390/vaccines11040773
Yaugel-Novoa M, Noailly B, Jospin F, Berger A-E, Waeckel L, Botelho-Nevers E, Longet S, Bourlet T, Paul S. Prior COVID-19 Immunization Does Not Cause IgA- or IgG-Dependent Enhancement of SARS-CoV-2 Infection. Vaccines. 2023; 11(4):773. https://doi.org/10.3390/vaccines11040773
Chicago/Turabian StyleYaugel-Novoa, Melyssa, Blandine Noailly, Fabienne Jospin, Anne-Emmanuelle Berger, Louis Waeckel, Elisabeth Botelho-Nevers, Stéphanie Longet, Thomas Bourlet, and Stéphane Paul. 2023. "Prior COVID-19 Immunization Does Not Cause IgA- or IgG-Dependent Enhancement of SARS-CoV-2 Infection" Vaccines 11, no. 4: 773. https://doi.org/10.3390/vaccines11040773
APA StyleYaugel-Novoa, M., Noailly, B., Jospin, F., Berger, A. -E., Waeckel, L., Botelho-Nevers, E., Longet, S., Bourlet, T., & Paul, S. (2023). Prior COVID-19 Immunization Does Not Cause IgA- or IgG-Dependent Enhancement of SARS-CoV-2 Infection. Vaccines, 11(4), 773. https://doi.org/10.3390/vaccines11040773