Correlates of Protection Against SARS-CoV-2 in Rhesus Macaques
Open accessAbstract
Recent studies have reported the protective efficacy of both natural 1 and vaccine-induced 2-7 immunity against challenge with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in rhesus macaques. However, the importance of humoral and cellular immunity for protection against infection with SARS-CoV-2 remains to be determined. Here we show that the adoptive transfer of purified IgG from convalescent rhesus macaques (Macaca mulatta) protects naive recipient macaques against challenge with SARS-CoV-2 in a dose-dependent fashion. Depletion of CD8+ T cells in convalescent macaques partially abrogated the protective efficacy of natural immunity against rechallenge with SARS-CoV-2, which suggests a role for cellular immunity in the context of waning or subprotective antibody titres. These data demonstrate that relatively low antibody titres are sufficient for protection against SARS-CoV-2 in rhesus macaques, and that cellular immune responses may contribute to protection if antibody responses are suboptimal. We also show that higher antibody titres are required for treatment of SARS-CoV-2 infection in macaques. These findings have implications for the development of SARS-CoV-2 vaccines and immune-based therapeutic agents.
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Binding and neutralizing antibody titres are important correlates of protection for these SARS-CoV-2 vaccines in non-human primates.
“Consistent with prior observations from our laboratory and others15,16,22, these findings suggest that binding and neutralizing antibody titres are important correlates of protection for these SARS-CoV-2 vaccines in non-human primates.”
From Optimization of non-coding regions for a non-modified mRNA COVID-19 vaccine (2022) · cites this paper as [22]
The IgG Adoptive Transfer Protection Study reports protection thresholds for neutralizing titres and binding-antibody ELISA titres in rhesus macaques. The Discussion also says neutralizing titres correlated with protection in earlier DNA and Ad26 vaccine studies. This paper’s direct binding-titre evidence comes from transfer of convalescent IgG, however, rather than from vaccinated animals, so it does not directly establish both as correlates for the vaccines. (LLM, conf=0.83)
Experimental — accuracy not yet measuredNeutralizing antibody titres elicited by CV2CoV to viral variants exceeded the values previously reported as threshold titres for protection (50-100).
“Although our challenge virus in this study was SARS-CoV-2 WA1/2020, the neutralizing antibody titres elicited by CV2CoV to viral variants exceeded the values we previously reported as threshold titres for protection (50–100)17,19,22.”
From Optimization of non-coding regions for a non-modified mRNA COVID-19 vaccine (2022) · cites this paper as [22]
The IgG Adoptive Transfer Protection Study (page unavailable) reports a pseudovirus neutralizing-antibody threshold of approximately 50 in rhesus macaques. Its approximately 100 threshold is for RBD ELISA binding titres, not neutralizing-antibody titres. The paper therefore supports the lower end of the cited 50–100 range, but not the full range as neutralizing-antibody thresholds; it does not assess CV2CoV variant titres. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCD8+ T cells contribute to virological control of SARS-CoV-2 infection when antibody titres are sub-optimal in non-human primates.
“CD8+ T cells have been shown to contribute to virological control of SARS-CoV-2 infection when antibodies titres were sub-optimal in non-human primates33,34.”
From Efficacy of an unmodified bivalent mRNA vaccine against SARS-CoV-2 variants in female small animal models (2023) · cites this paper as [33]
Depletion of CD8+ T cells partially abrogated protective efficacy against SARS-CoV-2 re-challenge in convalescent macaques.
“We previously reported that depletion of CD8+ T cells partially abrogated protective efficacy against SARS-CoV-2 re-challenge in convalescent macaques22.”
From Optimization of non-coding regions for a non-modified mRNA COVID-19 vaccine (2022) · cites this paper as [22]
Depletion of CD8+ T cells at 7 weeks after infection in macaques resulted in partial loss of protection from re-challenge.
“the depletion of CD8+ T cells at 7 weeks after infection in macaques resulted in a partial loss of protection from re-challenge48.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [48]
In the context of declining neutralizing antibody titres, cellular immunity is required to provide maximal protective immunity against SARS-CoV-2 re-exposure.
“These data suggest that, in the context of declining neutralizing antibody titres, cellular immunity is required to provide maximal protective immunity against SARS-CoV-2 re-exposure48.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [48]
Further studies provide evidence for a contribution of both IgG antibody and CD8+ T cells in protection against reinfection.
“Further studies have provided evidence for a contribution of both IgG antibody and CD8+ T cells in providing protection against reinfection48.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [48]
Transfer of high titres of purified IgG from convalescent animals is sufficient to protect against viral challenge, or at lower titres to reduce duration of viral replication.
“The transfer of high titres of purified IgG from convalescent animals is sufficient to protect against viral challenge or, at lower titres, to reduce the duration of viral replication.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [48]
In non-human primates, passive neutralizing antibody transfer was protective, while CD8+ T cell depletion reduced protection, indicating roles for both.
“The passive transfer of NAbs was also found to be protective in non-human primate models, whereas removal of CD8+ T cells in the same models impaired protection, suggesting a role for both components53.”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [53]
T-cell responses may contribute to protection from Covid-19 even when neutralizing antibody titers are lower.
“Although the correlation between antibody response and vaccine efficacy is high, which suggests that the neutralizing antibody response is important, T-cell responses may contribute to protection from Covid-19 even in the presence of lower neutralizing antibody titers.32”
From Efficacy of the ChAdOx1 nCoV-19 Covid-19 Vaccine against the B.1.351 Variant (2021) · cites this paper as [32]
Passive transfer of nAbs limits respiratory tract infection and protects against infection in animal models.
“passive transfer of nAbs limits respiratory tract infection and protects against infection in animal models (16–20)”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [18]
Studies in nonhuman primates indicate that even low titers of nAbs are sufficient to prevent experimental SARS-CoV-2 infection, particularly if CD8+ T cell responses are mounted.
“studies in nonhuman primates indicate that even low titers of nAbs are sufficient to prevent experimental SARS-CoV-2 infection, particularly if CD8+ T cell responses are mounted (18).”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [18]
E484K has been shown to impact neutralisation by monoclonal antibodies or convalescent sera, especially in combination with N501Y and K417N.
“E484K has been shown to impact neutralisation by monoclonal antibodies or convalescent sera, especially in combination with N501Y and K417N16,26,47–49.”
From Sensitivity of SARS-CoV-2 B.1.1.7 to mRNA vaccine-elicited antibodies (2021) · cites this paper as [16]
There are no studies to date that have specifically defined immune correlates of protection in upper and lower airways after vaccination with any COVID-19 vaccine approved for use in humans.
“Although immune responses associated with protection after primary infection have been assessed in NHPs (15), there are no studies to date that have specifically defined immune correlates of protection in upper and lower airways after vaccination with any COVID-19 vaccine approved for use in humans.”
From Immune correlates of protection by mRNA-1273 vaccine against SARS-CoV-2 in nonhuman primates (2021) · cites this paper as [15]
T cells might limit disease progression when neutralizing antibody titres are low.
“Although it is increasingly recognized that neutralizing antibodies dominate protection against initial infection 4,13 , T cells might limit disease progression 5 when neutralizing antibody titres are low 14 .”
From Age-related immune response heterogeneity to SARS-CoV-2 vaccine BNT162b2 (2021) · cites this paper as [14]
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Self-citation
- Authors
- McMahan, K., Yu, J., Mercado, N. B., Loos, C., Tostanoski, L. H., Chandrashekar, A., Liu, J., Peter, L., Atyeo, C., Zhu, A., Bondzie, E. A., Dagotto, G., Gebre, M. S., Jacob-Dolan, C., Li, Z., Nampanya, F., Patel, S., Pessaint, L., Van Ry, A., Blade, K., Yalley-Ogunro, J., Cabus, M., Brown, R., Cook, A., Teow, E., Andersen, H., Lewis, M. G., Lauffenburger, D. A., Alter, G., & Barouch, D. H.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Ragon Institute of MGH, MIT and Harvard (US)
- Harvard University (US)
- Bioqual (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Barouch, Dan H.
- ORCID
- McMahan, Katherine
- Yu, Jingyou
- Mercado, Noe B.
- Loos, Carolin
- Tostanoski, Lisa H.
- Chandrashekar, Abishek
- Liu, Jinyan
- Peter, Lauren
- Atyeo, Caroline
- Zhu, Alex
- Bondzie, Esther A.
- Dagotto, Gabriel
- Gebre, Makda S.
- Jacob-Dolan, Catherine
- Li, Zhenfeng
- Nampanya, Felix
- Patel, Shivani
- Pessaint, Laurent
- Van Ry, Alex
- Blade, Kelvin
- Brown, Renita
- Cook, Anthony
- Andersen, Hanne
- Lewis, Mark G.
- Lauffenburger, Douglas A.
- Alter, Galit
- Barouch, Dan H.
- Venue
- Nature
- Published
- 2020-12-04
- Volume
- 590
- Issue
- 7847
- Pages
- 630-634
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7906955
- OpenAlex
- W3108193091
- Cited by
- 1,068
- References
- 17
- Citations by year
- 2026: 32 · 2025: 60 · 2024: 115 · 2023: 177 · 2022: 360 · 2021: 317 · 2020: 7
- FWCI
- 28.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- RePEc: Research Papers in Economics (submittedVersion)
- PMC
- ImmPort
- Funders
- Bill and Melinda Gates Foundation (INV-006131)
- Massachusetts Consortium on Pathogen Readiness
- National Institutes of Health (R01OD024917, CA260476, AI128751, U42OD021458, P40OD012217)
- National Cancer Institute (U01CA260476)
- National Institute of Allergy and Infectious Diseases (R01AI129797, UM1AI124377, UM1AI126603, U19AI128751, T32AI007387)
- 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 › COVID-19 Clinical Research Studies
- Keywords
- SARS-CoV-2, COVID-19 pandemic, rhesus monkeys, humoral immunity, cell-mediated immunity, CD8+ T cells, antibody titers, waning immunity, drug rechallenge, passive immunotherapy, vaccine development
- MeSH terms
- COVID-19, SARS-CoV-2, COVID-19 Serotherapy, Animals, Disease Models, Animal, Female, Immunoglobulin G, Immunization, Passive, Macaca mulatta, Male, Regression Analysis, CD8-Positive T-Lymphocytes, Adoptive Transfer, Viral Load
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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