Antigen-Specific Adaptive Immunity to SARS-CoV-2 in Acute COVID-19 and Associations with Age and Disease Severity
Open accessAbstract
Limited knowledge is available on the relationship between antigen-specific immune responses and COVID-19 disease severity. We completed a combined examination of all three branches of adaptive immunity at the level of SARS-CoV-2-specific CD4 + and CD8 + T cell and neutralizing antibody responses in acute and convalescent subjects. SARS-CoV-2-specific CD4 + and CD8 + T cells were each associated with milder disease. Coordinated SARS-CoV-2-specific adaptive immune responses were associated with milder disease, suggesting roles for both CD4 + and CD8 + T cells in protective immunity in COVID-19. Notably, coordination of SARS-CoV-2 antigen-specific responses was disrupted in individuals ≥ 65 years old. Scarcity of naive T cells was also associated with aging and poor disease outcomes. A parsimonious explanation is that coordinated CD4 + T cell, CD8 + T cell, and antibody responses are protective, but uncoordinated responses frequently fail to control disease, with a connection between aging and impaired adaptive immune responses to SARS-CoV-2.
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There is a link between individual patient predisposition with respect to age and comorbidity.
“suggesting a link between individual patient predisposition with respect to age and comorbidity [127, 128].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [128]
There is some evidence linking robust T cell responses to mild COVID-19 disease outcome.
“there is some evidence linking robust T cell responses to mild disease outcome31.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [31]
CD4+ and CD8+ T cell responses play important roles in the resolution of SARS-CoV-2 infection and COVID-19, including modulating disease severity in humans and reducing viral loads in non-human primates.
“Several lines of evidence suggest that CD4+ and CD8+ T cell responses play important roles in the resolution of SARS-CoV-2 infection and COVID-19,33 including modulating disease severity in humans34,35 and reducing viral loads in non-human primates.36”
From Impact of SARS-CoV-2 variants on the total CD4+ and CD8+ T cell reactivity in infected or vaccinated individuals (2021) · cites this paper as [34]
SARS-CoV-2-specific T cell responses are significantly associated with milder COVID-19 disease.
“Studies of acute and convalescent COVID-19 patients have observed that SARS-CoV-2-specific T cell responses are significantly associated with milder disease (Liao et al., 2020; Rydyznski Moderbacher et al., 2020; Sekine et al., 2020; Zhou et al., 2020b), suggesting that T cell responses may be important for control and resolution of a primary SARS-CoV-2 infection.”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
An extended absence of SARS-CoV-2-specific CD4+ T cells is associated with severe or fatal COVID-19.
“In contrast, the strikingly extended absence of SARS-CoV-2-specific CD4+ T cells was associated with severe or fatal COVID-19 (>day 22 PSO in some cases) (Braun et al., 2020; Rydyznski Moderbacher et al., 2020; Tan et al., 2020a).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
SARS-CoV-2-specific CD4+ T cells have the strongest association with lessened COVID-19 disease severity compared with antibodies and CD8+ T cells.
“Notably, SARS-CoV-2-specific CD4+ T cells had the strongest association with lessened COVID-19 disease severity, compared with antibodies and CD8+ T cells (Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
IL-22 is robustly expressed by SARS-CoV-2-specific CD4+ T cells.
“In contrast, IL-22, which can also be made by mucosal CD4+ T cells, appears to be robustly expressed by SARS-CoV-2-specific CD4+ T cells (Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020; Weiskopf et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
T cell responses are detected after almost all SARS-CoV-2 infections.
“T cell responses are detected after almost all SARS-CoV-2 infections (Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020; Peng et al., 2020; Sekine et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
CD4+ T cell responses have been associated with control of primary SARS-CoV-2 infection.
“CD4+ T cell responses to SARS-CoV-2 are more prominent than CD8+ T cell responses (Grifoni et al., 2020; Sekine et al., 2020) and have been associated with control of primary SARS-CoV-2 infection (Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
Circulating SARS-CoV-2-specific CD8+ T cells are less consistently observed than CD4+ T cells.
“Overall, circulating SARS-CoV-2-specific CD8+ T cells are less consistently observed than CD4+ T cells (Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020; Sekine et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
SARS-CoV-2 cTfh cell frequencies are associated with reduced COVID-19 disease severity.
“Although neutralizing antibody titers have not correlated with reduced COVID-19 severity (Dan et al., 2021; Piccoli et al., 2020; Robbiani et al., 2020), SARS-CoV-2 cTfh cell frequencies have been associated with reduced disease severity (Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
The presence of virus-specific CD8+ T cells is associated with better COVID-19 outcomes.
“In SARS-CoV-2 infections, the presence of virus-specific CD8+ T cells has been associated with better COVID-19 outcomes (Rydyznski Moderbacher et al., 2020; Peng et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
The dominant cytokine produced by SARS-CoV-2-specific CD4+ T cells from COVID-19 patients is IFNγ, with a Th1 signature including TNF and IL-2.
“The dominant cytokine produced by SARS-CoV-2-specific CD4+ T cells from COVID-19 patients is IFNγ (Braun et al., 2020; Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020; Weiskopf et al., 2020), with a clear IFNγ, tumor necrosis factor (TNF), IL-2 protein signature of canonical Th1 cells (Braun et al., 2020; Rydyznski Moderbacher et al., 2020; Peng et al., 2020; Sekine et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
SARS-CoV-2-specific CD4+ T cells can be detected as early as days 2-4 post-symptom onset.
“SARS-CoV-2-specific CD4+ T cells can be detected as early as days 2–4 post-symptom onset (PSO) (Rydyznski Moderbacher et al., 2020; Tan et al., 2020a; Weiskopf et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
The vast majority of SARS-CoV-2 infected individuals seroconvert within 5-15 days post-symptom onset, with about 90% seroconversion by day 10.
“The vast majority of SARS-CoV-2 infected individuals seroconvert within 5–15 days PSO, with ∼90% seroconversion by day 10 PSO (Long et al., 2020; Rydyznski Moderbacher et al., 2020; Premkumar et al., 2020; Ripperger et al., 2020; Suthar et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
SARS-CoV-2-specific CD4+ T cells from patients consistently do not have Th2 characteristics.
“Last, there were initially great concerns about potential immune deviation to Th2 and immunopathogenesis (Peeples, 2020), but SARS-CoV-2-specific CD4+ T cells from patients consistently do not have Th2 characteristics (Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020; Sekine et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
Multiple reports describe healthy individuals controlling SARS-CoV-2 infection with little to no detectable neutralizing or RBD IgG antibodies while having significant SARS-CoV-2-specific T cell memory.
“Separately, there are multiple reports of healthy individuals successfully controlling a SARS-CoV-2 infection with little to no neutralizing (or RBD IgG) antibodies detectable post-infection, while having significant SARS-CoV-2-specific T cell memory (Rydyznski Moderbacher et al., 2020; Nelde et al., 2021; Schulien et al., 2020; Sekine et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
There is an approximately 1,000-fold range in the magnitude of antibody responses to SARS-CoV-2, as well as heterogeneity in the magnitude of SARS-CoV-2-specific CD4+ and CD8+ T cell responses.
“There is an ∼1,000-fold range in the magnitude of antibody responses to SARS-CoV-2, as well as heterogeneity in the magnitude of SARS-CoV-2-specific CD4+ T cell and CD8+ T cell responses (Grifoni et al., 2020; Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
T cell responses are important for prevention of severe COVID-19.
“data indicate that T cell responses are important for prevention of severe COVID-19 (Rydyznski Moderbacher et al., 2020)”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
Older individuals are less likely to make a coordinated adaptive immune response to SARS-CoV-2.
“Older individuals are less likely to make a coordinated adaptive immune response to SARS-CoV-2 (Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
COVID-19 disease severity was inversely correlated with the frequency of naive T cells.
“COVID-19 disease severity was inversely correlated with the frequency of naive T cells (Mathew et al., 2020; Rydyznski Moderbacher et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
One component of the higher risk in older individuals appears to be poor T cell responses due in part to a more limited naive T cell repertoire.
“it appears that one component of the risk is poor T cell responses due in part to a more limited naive T cell repertoire”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
Spike is a good target for CD4+ T cell, Tfh cell, and CD8+ T cell responses in people infected with SARS-CoV-2.
“the findings that Spike is a good target for CD4+ T cell responses, Tfh cell responses, and CD8+ T cell responses in SARS-CoV-2-infected people”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Rydyznski Moderbacher et al., 2020
Current evidence suggests that an early, robust and diverse T cell response against SARS-CoV-2 correlates with milder COVID-19 outcomes.
“Current evidence suggests an early, robust, and diverse T cell response directed against SARS-CoV-2 correlates with milder COVID-19 outcomes126,131,132”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
Adaptive responses to SARS-CoV-2 begin about one week after symptoms, and SARS-CoV-2-specific CD4+ and CD8+ T cells can be observed as early as four days after symptom onset.
“Adaptive responses to SARS-CoV-2 begin around one week after symptoms (Figure 2), with SARS-CoV-2 specific CD4+ and CD8+ T cells being observed as early as four days post-symptom onset126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
SARS-CoV-2 infection elicits a Th1 CD4+ T cell response, with IFNγ and IL-2 as the main cytokines produced and some TNFα as well.
“SARS-CoV-2 infection elicits a Th1 CD4+ T cell response, with IFNγ and IL-2 being the primary cytokines produced by these cells and some TNFα production as well112,126-129.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
Low frequencies of naive T cells correlate with severe COVID-19 outcomes.
“Low frequencies of naive T cells have also been correlated with severe COVID-19 outcomes126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
For CD8+ T cells, some studies report diminished cytotoxicity and cytokine production in severe COVID-19.
“For CD8+ T cells, there are reports of diminished CD8+ cytotoxicity and cytokine production in severe cases126,132, while others report the opposite141, and still others find no differences142.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
In one study, the presence of IFNγ-producing CD8+ T cells during acute COVID-19 was the strongest predictor of mild outcomes.
“Consistent with this hypothesis, one study identified the presence of IFNγ producing CD8+ T cells during the acute stages of disease as the strongest predictor of mild COVID-19 outcomes126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
Many studies report a correlation between higher IgG antibody titers and severe COVID-19.
“Many studies have reported a correlation between higher IgG antibody titers and severe disease, but others have seen either the opposite or no correlation between antibody production and disease severity126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
SARS-CoV-2-specific T Follicular Helper cells are detected concurrently with the antibody response, suggesting a role for T-dependent antibody production.
“This response occurs concurrently with the detection of circulating SARS-CoV-2 specific T Follicular Helper cells, suggesting a role for T-dependent antibody production126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
Other studies found either the opposite correlation or no correlation between antibody production and COVID-19 severity.
“Many studies have reported a correlation between higher IgG antibody titers and severe disease, but others have seen either the opposite or no correlation between antibody production and disease severity126.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [126]
In COVID-19 patients, a coordinated adaptive immunity of CD4+ T cells, CD8+ T cells, and antibody responses was correlated to milder disease, whereas an uncoordinated response frequently failed to control disease.
“In COVID-19 patients, a coordinated adaptive immunity of CD4+ T cells, CD8+ T cells, and antibody responses was correlated to milder disease, whereas an uncoordinated response frequently failed to control disease [68]”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [68]
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T follicular helper cell biology: a decade of discovery and diseases
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InfluentialSelf-citationMathew, D., Giles, J. R., Baxter, A. E., Oldridge, D. A., Greenplate, A. R., Wu, J. E., Alanio, C., Kuri-Cervantes, L., Pampena, M. B., D’Andrea, K., et al. (2020) · Science · doi:10.1126/science.abc8511 · Cited by 1,509 · cited 8× · see citing works
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InfluentialSARS-CoV-2 Reverse Genetics Reveals a Variable Infection Gradient in the Respiratory Tract
Hou, Y. J., Okuda, K., Edwards, C. E., Martinez, D. R., Asakura, T., Dinnon, K. H., Kato, T., Lee, R. E., Yount, B. L., Mascenik, T. M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.042 · Cited by 1,488 · see citing works
Self-citationDevelopment of an inactivated vaccine candidate for SARS-CoV-2
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“…titers were associated with protection against SARS-CoV-2 in non-human primate infection and rechallenge studies (Chandrashekar et al., 2020; Gao et al., 2020), as well as in three candidate COVID-19 vaccine studies in non-human primates (Gao et al., 2020; Wang et al., 2020c; Yu et al., 2020).”
SARS-CoV-2-reactive T cells in healthy donors and patients with COVID-19
Braun, J., Loyal, L., Frentsch, M., Wendisch, D., Georg, P., Kurth, F., Hippenstiel, S., Dingeldey, M., Kruse, B., Fauchere, F., et al. (2020) · Nature · doi:10.1038/s41586-020-2598-9 · Cited by 1,310 · see citing works
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“The RBD domain is the primary target of SARS-CoV-2-neutralizing antibodies (Ju et al., 2020; Rogers et al., 2020), much like what was found for SARS-CoV (Subbarao, 2020).”
Self-citationRobust neutralizing antibodies to SARS-CoV-2 infection persist for months
Wajnberg, A., Amanat, F., Firpo, A., Altman, D. R., Bailey, M. J., Mansour, M., McMahon, M., Meade, P., Mendu, D. R., Muellers, K., et al. (2020) · Science · doi:10.1126/science.abd7728 · Cited by 1,195 · see citing works
Robust neutralizing antibodies to SARS-CoV-2 infection persist for months
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Characteristics of Peripheral Lymphocyte Subset Alteration in COVID-19 Pneumonia
Wang, F., Nie, J., Wang, H., Zhao, Q., Xiong, Y., Deng, L., Song, S., Ma, Z., Mo, P., & Zhang, Y. (2020) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaa150 · Cited by 1,125 · see citing works
SARS-CoV-2 Vaccines: Status Report
Amanat, F., & Krammer, F. (2020) · Immunity · doi:10.1016/j.immuni.2020.03.007 · Cited by 1,120 · cited 1× · see citing works
“Thus, most COVID-19 vaccine efforts focus on the elicitation of neutralizing antibodies (Amanat and Krammer, 2020; Corey et al., 2020; Thanh Le et al., 2020), with additional interest in elicitation of CD4 or CD8 T cells (Corbett et al.”
Evaluation of the mRNA-1273 Vaccine against SARS-CoV-2 in Nonhuman Primates
Corbett, K. S., Flynn, B., Foulds, K. E., Francica, J. R., Boyoglu-Barnum, S., Werner, A. P., Flach, B., O’Connell, S., Bock, K. W., Minai, M., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2024671 · Cited by 1,066 · cited 1× · see citing works
“, 2020), with additional interest in elicitation of CD4 or CD8 T cells (Corbett et al., 2020; Folegatti et al., 2020; Jackson et al., 2020; Mercado et al., 2020; Sahin et al., 2020).”
Self-citationDNA vaccine protection against SARS-CoV-2 in rhesus macaques
Yu, J., Tostanoski, L. H., Peter, L., Mercado, N. B., McMahan, K., Mahrokhian, S. H., Nkolola, J. P., Liu, J., Li, Z., Chandrashekar, A., et al. (2020) · Science · doi:10.1126/science.abc6284 · Cited by 997 · see citing works
Self-citationA dynamic COVID-19 immune signature includes associations with poor prognosis
Laing, A. G., Lorenc, A., del Molino del Barrio, I., Das, A., Fish, M., Monin, L., Muñoz-Ruiz, M., McKenzie, D. R., Hayday, T. S., Francos-Quijorna, I., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1038-6 · Cited by 946 · cited 5× · see citing works
“…(IP-10), IL-8, and IL-6 were elevated in acute COVID-19 (p < 0.0001, p < 0.05, p < 0.001; Figures S5A–S5C) and correlated with disease severity (Figure 5A), consistent with large cohort studies of plasma cytokines (Chen et al., 2020; Laing et al., 2020; Mathew et al., 2020; Yang et al., 2020).”
InfluentialGrifoni, A., Sidney, J., Zhang, Y., Scheuermann, R. H., Peters, B., & Sette, A. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.03.002 · Cited by 920 · see citing works
Self-citationWeiskopf, D., Schmitz, K. S., Raadsen, M. P., Grifoni, A., Okba, N. M. A., Endeman, H., van den Akker, J. P. C., Molenkamp, R., Koopmans, M. P. G., van Gorp, E. C. M., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abd2071 · Cited by 907 · see citing works
Self-citationComparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model
Rockx, B., Kuiken, T., Herfst, S., Bestebroer, T., Lamers, M. M., Oude Munnink, B. B., de Meulder, D., van Amerongen, G., van den Brand, J., Okba, N. M. A., et al. (2020) · Science · doi:10.1126/science.abb7314 · Cited by 901 · cited 2× · see citing works
“, 2020), similar to what was observed for SARS (Rockx et al., 2020).”
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“CXCL10 (IP-10), IL-8, and IL-6 were elevated in acute COVID19 (p < 0.0001, p < 0.05, p < 0.001; Figures S5A–S5C) and correlated with disease severity (Figure 5A), consistent with large cohort studies of plasma cytokines (Chen et al., 2020; Laing et al., 2020; Mathew et al., 2020; Yang et al., 2020).”
InfluentialPremkumar, L., Segovia-Chumbez, B., Jadi, R., Martinez, D. R., Raut, R., Markmann, A. J., Cornaby, C., Bartelt, L., Weiss, S., Park, Y., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abc8413 · Cited by 868 · cited 2× · see citing works
“This RBD sequence is 346 amino acids in length, corresponding to amino acids 319-591 of the Spike protein sequences in the Protein Data Bank (PDB) deposited by Premkumar et al., 2020 (PDB 6VSB) and for the reference strain Wuhan-Hu-1 (PDB 6XR8).”
Self-citationSARS-CoV-2 infection protects against rechallenge in rhesus macaques
Chandrashekar, A., Liu, J., Martinot, A. J., McMahan, K., Mercado, N. B., Peter, L., Tostanoski, L. H., Yu, J., Maliga, Z., Nekorchuk, M., et al. (2020) · Science · doi:10.1126/science.abc4776 · Cited by 816 · cited 2× · see citing works
“Neutralizing antibody titers were associated with protection against SARS-CoV-2 in non-human primate infection and rechallenge studies (Chandrashekar et al., 2020; Gao et al., 2020), as well as in three candidate COVID-19 vaccine studies in non-human primates (Gao et al.”
Self-citationSingle-Shot Ad26 Vaccine Protects Against SARS-CoV-2 in Rhesus Macaques
Mercado, N. B., Zahn, R., Wegmann, F., Loos, C., Chandrashekar, A., Yu, J., Liu, J., Peter, L., McMahan, K., Tostanoski, L. H., et al. (2020) · Nature · doi:10.1038/s41586-020-2607-z · Cited by 789 · cited 2× · see citing works
“Activation induced cell marker assay Assays were conducted as previously described (Grifoni et al., 2020a; Morou et al., 2019; Reiss et al., 2017).”
Self-citationDiversity and clonal selection in the human T-cell repertoire
Qi, Q., Liu, Y., Cheng, Y., Glanville, J., Zhang, D., Lee, J.-Y., Olshen, R. A., Weyand, C. M., Boyd, S. D., & Goronzy, J. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409155111 · Cited by 755 · cited 1× · see citing works
“A repertoire of fewer naive T cells in older individuals (Briceño et al., 2016; Qi et al., 2014) may be exacerbated as a risk factor specifically for severe COVID19, because early innate immune evasion by SARS-CoV-2 may limit T cell priming (Blanco-Melo et al.”
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“S IgG and IgA responses were robust in most COVID-19 cases (25/28 acute, 15/15 convalescent S IgG; Figures 1E and S1E) (27/28 acute, 14/15 convalescent S IgA; Figures 1F and S1F), though (cid:1) 17% of cases had relatively low titers (within 3-fold of the LOD).”
InfluentialWang, H., Zhang, Y., Huang, B., Deng, W., Quan, Y., Wang, W., Xu, W., Zhao, Y., Li, N., Zhang, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.008 · Cited by 748 · cited 1× · see citing works
“…titers were associated with protection against SARS-CoV-2 in non-human primate infection and rechallenge studies (Chandra-shekar et al., 2020; Gao et al., 2020), as well as in three candidate COVID-19 vaccine studies in non-human primates (Gao et al., 2020; Wang et al., 2020c; Yu et al., 2020).”
Visualization of a Correlation Matrix [R package corrplot version 0.84]
Wei, T., & Šimko, V. (2017) · Cited by 737 · see citing works
Tissue-Resident T Cells and Other Resident Leukocytes
Masopust, D., & Soerens, A. G. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053214 · Cited by 608 · cited 2× · see citing works
“While blood sampling is a necessity for the vast majority of human immunology studies, it is established that certain cell types of ADIMs can be restricted to organs, such as the lungs, and not be detectable in the circulation (Masopust and Soerens, 2019).”
Molecular regulation of effector and memory T cell differentiation
Chang, J. T., Wherry, E. J., & Goldrath, A. W. (2014) · Nature Immunology · doi:10.1038/ni.3031 · Cited by 578 · see citing works
Imbalance of Regulatory and Cytotoxic SARS-CoV-2-Reactive CD4+ T Cells in COVID-19
Meckiff, B. J., Ramírez-Suástegui, C., Fajardo, V., Chee, S., Kusnadi, A., Simon, H. A., Eschweiler, S., Grifoni, A., Pelosi, E., Weiskopf, D., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.001 · Cited by 565 · cited 4× · see citing works
“…reported here do not assess the role of pre-existing cross-reactive T cells in response to SARS-CoV-2 (Braun et al., 2020; Grifoni et al., 2020a; Meckiff et al., 2020; Weiskopf et al., 2020), as the anti-gen-specific tools used in this study did not distinguish between T cell responses…”
InfluentialSelf-citationAcute SARS-CoV-2 Infection Impairs Dendritic Cell and T Cell Responses
Zhou, R., To, K. K.-W., Wong, Y.-C., Liu, L., Zhou, B., Li, X., Huang, H., Mo, Y., Luk, T.-Y., Lau, T. T.-K., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.026 · Cited by 531 · cited 1× · see citing works
“…2020) or neutralizing antibody data (Robbiani et al., 2020; Rogers et al., 2020; Wajnberg et al., 2020) are available, but combined assessments of antigen-specific CD4 + T cells, CD8 + T cells, and neutralizing antibodies in acute COVID-19 are still lacking (except 3 subjects in Zhou et al., 2020b).”
Rapid Generation of Neutralizing Antibody Responses in COVID-19 Patients
Suthar, M. S., Zimmerman, M. G., Kauffman, R. C., Mantus, G., Linderman, S. L., Hudson, W. H., Vanderheiden, A., Nyhoff, L., Davis, C. W., Adekunle, O., et al. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2020.100040 · Cited by 508 · cited 7× · see citing works
“Neutralizing antibodies and RBD IgG were detectable in the majority of patients in all time windows (Figures 1O and 1P) (Suthar et al., 2020).”
InfluentialA strategic approach to COVID-19 vaccine R&D
Corey, L., Mascola, J. R., Fauci, A. S., & Collins, F. S. (2020) · Science · doi:10.1126/science.abc5312 · Cited by 499 · cited 2× · see citing works
“Thus, most COVID-19 vaccine efforts focus on the elicitation of neutralizing antibodies (Amanat and Krammer, 2020; Corey et al., 2020; Thanh Le et al., 2020), with additional interest in elicitation of CD4 or CD8 T cells (Corbett et al.”
Airway Memory CD4+ T Cells Mediate Protective Immunity against Emerging Respiratory Coronaviruses
Zhao, J., Zhao, J., Mangalam, A. K., Channappanavar, R., Fett, C., Meyerholz, D. K., Agnihothram, S., Baric, R. S., David, C. S., & Perlman, S. (2016) · Immunity · doi:10.1016/j.immuni.2016.05.006 · Cited by 496 · cited 1× · see citing works
“In a mouse model of SARS, it was demonstrated that CD4+ T cells alone, in the absence of antibodies or CD8+ T cells, could provide protection against lethal challenge with SARS-CoV (Zhao et al., 2016).”
Self-citationHumoral and circulating follicular helper T cell responses in recovered patients with COVID-19
Juno, J. A., Tan, H.-X., Lee, W. S., Reynaldi, A., Kelly, H. G., Wragg, K., Esterbauer, R., Kent, H. E., Batten, C. J., Mordant, F. L., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0995-0 · Cited by 437 · see citing works
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“Activation induced cell marker assay Assays were conducted as previously described (Grifoni et al., 2020a; Morou et al., 2019; Reiss et al., 2017).”
Self-citationSevere immunosuppression and not a cytokine storm characterizes COVID-19 infections
Remy, K. E., Mazer, M. B., Striker, D. A., Ellebedy, A. H., Walton, A. H., Unsinger, J., Blood, T. M., Mudd, P. A., Yi, D. J., Mannion, D. A., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.140329 · Cited by 309 · cited 1× · see citing works
“, 2020), polyclonally stimulated T cells (Lucas et al., 2020; Remy et al., 2020), measurements of common leukocyte types, or inflammatory proteins in blood (Giamarellos-Bourboulis et al.”
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“…immune evasion by SARS-CoV-2 may limit T cell priming (Blanco-Melo et al., 2020; Vabret et al., 2020), and there is the possibility of fewer professional antigen presenting cells in the lungs with advanced age, as has been seen in small animal models of SARS (Chen et al., 2010; Zhao et al., 2011).”
Immunity and immunological memory following smallpox vaccination
Amanna, I. J., Slifka, M. K., & Crotty, S. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00392.x · Cited by 231 · cited 2× · see citing works
“For example, neutralizing antibodies, CD4 T cells, and CD8 T cells have each individually been shown to have protective roles against poxvirus infections in mice, and depletion of any one of the three components of the adaptive immune system can still result in protection from vaccinia virus infection (Amanna et al.,…”
Self-citationThe Innate Immune System: Fighting on the Front Lines or Fanning the Flames of COVID-19?
McKechnie, J. L., & Blish, C. A. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.05.009 · Cited by 218 · cited 1× · see citing works
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Immunization: vital progress, unfinished agenda
Piot, P., Larson, H. J., O’Brien, K. L., N’kengasong, J., Ng, E., Sow, S., & Kampmann, B. (2019) · Nature · doi:10.1038/s41586-019-1656-7 · Cited by 206 · cited 1× · see citing works
“The vast majority of licensed human vaccines work on the basis of protective antibody responses, with neutralizing antibodies being the most common mechanism of action (Piot et al., 2019; Plotkin, 2010; Plotkin et al., 2018).”
Reduced naïve <scp>CD</scp> 8 <sup>+</sup> <scp>T</scp> ‐cell priming efficacy in elderly adults
Briceño, O., Lissina, A., Wanke, K., Afonso, G., Braun, A., Ragon, K., Miquel, T., Gostick, E., Papagno, L., Stiasny, K., et al. (2016) · Aging Cell · doi:10.1111/acel.12384 · Cited by 151 · see citing works
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Altered differentiation is central to HIV-specific CD4+ T cell dysfunction in progressive disease
Morou, A., Brunet‐Ratnasingham, E., Dubé, M., Charlebois, R., Mercier, E., Darko, S. W., Brassard, N., Nganou‐Makamdop, K., Arumugam, S. A., Gendron‐Lepage, G., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0418-x · Cited by 101 · cited 2× · see citing works
“Activation induced cell marker assay Assays were conducted as previously described (Grifoni et al., 2020a; Morou et al., 2019; Reiss et al., 2017).”
OX40 Drives Protective Vaccinia Virus-Specific CD8 T Cells,
Salek‐Ardakani, S., Moutaftsi, M., Crotty, S., Sette, A., & Croft, M. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.11.7969 · Cited by 75 · cited 1× · see citing works
“…+ T cells have each individually been shown to have protective roles against poxvirus infections in mice, and depletion of any one of the three components of the adaptive immune system can still result in protection from vaccinia virus infection (Amanna et al., 2006; Salek-Ardakani et al., 2008).”
Self-citationAuthor Correction: A dynamic COVID-19 immune signature includes associations with poor prognosis
Laing, A. G., Lorenc, A., del Barrio, I. D. M., Das, A., Fish, M., Monin, L., Muñoz‐Ruiz, M., McKenzie, D. R., Hayday, T. S., Francos-Quijorna, I., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-01186-5 · Cited by 68 · cited 5× · see citing works
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InfluentialConcurrent human antibody and T H 1 type T-cell responses elicited by a COVID-19 RNA vaccinePreprint
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“…focus on the elicitation of neutralizing antibodies (Amanat and Krammer, 2020; Corey et al., 2020; Thanh Le et al., 2020), with additional interest in elicitation of CD4+ or CD8+ T cells (Corbett et al., 2020; Folegatti et al., 2020; Jackson et al., 2020; Mercado et al., 2020; Sahin et al., 2020).”
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“The different arms of adaptive immunity can compensate for each other in protective immunity in some contexts (Amanna et al., 2006; Plotkin et al., 2018).”
Single-Cell Transcriptomic Analysis of SARS-CoV-2 Reactive CD4 + T CellsPreprint
Meckiff, B. J., Ramírez-Suástegui, C., Fajardo, V., Chee, S., Kusnadi, A., Simon, H. A., Grifoni, A., Pelosi, E., Weiskopf, D., Sette, A., et al. (2020) · SSRN Electronic Journal · doi:10.2139/ssrn.3641939 · Cited by 41 · cited 4× · see citing works
“…reported here do not assess the role of pre-existing cross-reactive T cells in response to SARS-CoV-2 (Braun et al., 2020; Grifoni et al., 2020a; Meckiff et al., 2020; Weiskopf et al., 2020), as the anti-gen-specific tools used in this study did not distinguish between T cell responses…”
InfluentialSelf-citationSARS-CoV-2: A New Song Recalls an Old Melody
Subbarao, K. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.04.019 · Cited by 20 · cited 2× · see citing works
“The RBD domain is the primary target of SARS-CoV-2-neutralizing antibodies (Ju et al., 2020; Rogers et al., 2020), much like what was found for SARS-CoV (Subbarao, 2020).”
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Khoury, D. S., Cromer, D., Reynaldi, A., Schlub, T. E., Wheatley, A. K., Juno, J. A., Subbarao, K., Kent, S. J., Triccas, J. A., & Davenport, M. P. (2021) · Nature Medicine · doi:10.1038/s41591-021-01377-8 · Cited by 3,742 · see citing works
Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection.
Dan, J. M., Mateus, J., Kato, Y., Hastie, K. M., Yu, E. D., Faliti, C. E., Grifoni, A., Ramirez, S. I., Haupt, S., Frazier, A., et al. (2021) · Science · doi:10.1126/science.abf4063 · Cited by 2,656 · see citing works
“Neutralizing antibodies have generally not correlated with lessenedCOVID-19disease severity (5, 19,20), which was also observed for Middle Eastern respiratory syndrome (MERS), causedbyMERSCoV (21).”
BackgroundMethodResultInfluentialSelf-citationAdaptive immunity to SARS-CoV-2 and COVID-19
Sette, A., & Crotty, S. (2021) · Cell · doi:10.1016/j.cell.2021.01.007 · Cited by 1,860 · see citing works
“Notably, frequencies of RBD (and Spike) memory B cells increased over time, with more RBDmemory B cells at 6 months PSO than at 1 month PSO (Dan et al., 2021; Gaebler et al., 2020), consistent with observations at 3 months PSO (Rodda et al., 2021).”
InfluentialSelf-citationThe T cell immune response against SARS-CoV-2
Moss, P. A. H. (2022) · Nature Immunology · doi:10.1038/s41590-021-01122-w · Cited by 1,205 · see citing works
Tarke, A., Coelho, C. H., Zhang, Z., Dan, J. M., Yu, E. D., Methot, N., Bloom, N. I., Goodwin, B., Phillips, E., Mallal, S., et al. (2022) · Cell · doi:10.1016/j.cell.2022.01.015 · Cited by 858 · see citing works
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Self-citationSingle-cell multi-omics analysis of the immune response in COVID-19
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Self-citationT cell response to SARS-CoV-2 infection in humans: A systematic review
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BackgroundHighly functional virus-specific cellular immune response in asymptomatic SARS-CoV-2 infection
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Self-citationThe germinal centre B cell response to SARS-CoV-2
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“This immune response fights intracellular infections, including viruses (38), some bacteria, fungi (39), and protozoans (40).”
BackgroundBNT162b2 vaccination induces durable SARS-CoV-2–specific T cells with a stem cell memory phenotype
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Complement activation induces excessive T cell cytotoxicity in severe COVID-19
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Targeting immune dysfunction in aging
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Time-resolved systems immunology reveals a late juncture linked to fatal COVID-19
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“While mechanistic studies are still being conducted, emerging evidence has suggested that SRAS-CoV-2-specific CD4 and CD8 T cells in coordination with neutralizing antibodies are required for generating protective immunity against SARS-CoV-2 (33).”
BackgroundResultInfluentialLeukocyte trafficking to the lungs and beyond: lessons from influenza for COVID-19
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BackgroundAge-associated remodeling of T cell immunity and metabolism
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Adaptive immune determinants of viral clearance and protection in mouse models of SARS-CoV-2
Israelow, B., Mao, T., Klein, J., Song, E., Menasche, B., Omer, S. B., & Iwasaki, A. (2021) · doi:10.1101/2021.05.19.444825 · Cited by 189 · see citing works
T Cell Responses to SARS-CoV-2
Sette, A., Sidney, J., & Crotty, S. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101721-061120 · Cited by 181 · see citing works
Self-citationRiou, C., Bruyn, E. D., Stek, C. J., Daroowala, R., Goliath, R. T., Abrahams, F., Said-Hartley, Q., Allwood, B., Hsiao, M., Wilkinson, K. A., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci149125 · Cited by 204 · see citing works
“61; Supplemental Figure 2A), as previously reported (8, 15, 42, 43).”
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Kinetics and correlates of the neutralizing antibody response to SARS-CoV-2 infection in humans
Vanshylla, K., Di Cristanziano, V., Kleipass, F., Dewald, F., Schommers, P., Gieselmann, L., Gruell, H., Schlotz, M., Ercanoglu, M. S., Stumpf, R., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.04.015 · Cited by 153 · see citing works
T cell apoptosis characterizes severe Covid-19 disease
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Immunogenicity of Pfizer-BioNTech COVID-19 vaccine in patients with inborn errors of immunity
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Immune signatures underlying post-acute COVID-19 lung sequelae
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“Detected as early as 2 to 4 days after onset of COVID-19 symptoms (33), CD4+ T cells play an important role in assisting the development of CD8+ cells and B cells.”
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“A lower level of memory CD4 T-cells contributed to poorer T cell responses in SARS patients [105].”
COVID-19 vaccination for people with severe mental illness: why, what, and how?
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The impact of pre-existing cross-reactive immunity on SARS-CoV-2 infection and vaccine responses
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The known unknowns of T cell immunity to COVID-19
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Peripheral and lung resident memory T cell responses against SARS-CoV-2
Grau-Expósito, J., Sánchez-Gaona, N., Massana, N., Suppi, M., Astorga-Gamaza, A., Perea, D., Rosado, J., Falcó-Roget, A., Kirkegaard-Biosca, C., Torrella, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23333-3 · Cited by 161 · see citing works
Alterations in T and B cell function persist in convalescent COVID-19 patients
Shuwa, H. A., Shaw, T. N., Knight, S., Wemyss, K., McClure, F. A., Pearmain, L., Prise, I. E., Jagger, C. P., Morgan, D. J., Khan, S., et al. (2020) · Med · doi:10.1016/j.medj.2021.03.013 · Cited by 170 · see citing works
SARS-CoV-2-specific T cells in infection and vaccination
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“Differences in both humoral and cellular responses in females versus males or in subjects of different ages or with concomitant pathologies are present and have been attentively studied [3, 80].”
Background
- Authors
- Rydyznski Moderbacher, C., Ramirez, S. I., Dan, J. M., Grifoni, A., Hastie, K. M., Weiskopf, D., Belanger, S., Abbott, R. K., Kim, C., Choi, J., Kato, Y., Crotty, E. G., Kim, C., Rawlings, S. A., Mateus, J., Tse, L. P. V., Frazier, A., Baric, R., Peters, B., Greenbaum, J., Saphire, E. O., Smith, D. M., Sette, A., & Crotty, S.
- Affiliations
- La Jolla Institute for Immunology (US)
- University of California San Diego (US)
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Sette, Alessandro
- Crotty, Shane
- ORCID
- Ramirez, Sydney I.
- Dan, Jennifer M.
- Grifoni, Alba
- Hastie, Kathryn M.
- Weiskopf, Daniela
- Abbott, Robert K.
- Kim, Christina
- Choi, Jinyong
- Kato, Yu
- Kim, Cheryl
- Rawlings, Stephen A.
- Mateus, Jose
- Tse, Long Ping Victor
- Frazier, April
- Baric, Ralph
- Peters, Bjoern
- Greenbaum, Jason
- Saphire, Erica Ollmann
- Smith, Davey M.
- Sette, Alessandro
- Crotty, Shane
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-11
- Volume
- 183
- Issue
- 4
- Pages
- 996-1012.e19
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7494270
- OpenAlex
- W3084879098
- Cited by
- 1,790
- References
- 77
- Citations by year
- 2026: 54 · 2025: 144 · 2024: 180 · 2023: 288 · 2022: 543 · 2021: 517 · 2020: 62
- FWCI
- 46.45
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Bill and Melinda Gates Foundation (INV-006133)
- National Institute of Allergy and Infectious Diseases (U19 AI118626, AI100625, 75N9301900065, AI142742, AI145762, AI135078)
- National Institutes of Health
- Pontificia Universidad Javeriana
- University of California, San Diego
- Departamento Administrativo de Ciencia, Tecnología e Innovación
- Wellcome
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- SARS-CoV-2, COVID-19 pandemic, CD4+ T cells, CD8+ T cells, neutralizing antibodies, disease severity, age, naive T cells, immunosenescence
- MeSH terms
- Betacoronavirus, COVID-19, SARS-CoV-2, Acute Disease, Adult, Aged, Aged, 80 and over, Antibodies, Viral, Antigens, Viral, Female, Humans, Male, Middle Aged, Pneumonia, Viral, Severity of Illness Index, CD4-Positive T-Lymphocytes, Cytokines, Coronavirus Infections, CD8-Positive T-Lymphocytes, Young Adult, Adaptive Immunity, Antibodies, Neutralizing, Pandemics
About these checks
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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