Vaccination is one of the best ways to prevent severe COVID-19. Two doses of mRNA vaccine protect against serious illness caused by the coronavirus SARS-CoV-2. They do this, in part, by encouraging the immune system to make specialised proteins known as antibodies that recognise the virus. Most of the vaccine research so far has focussed on these antibodies, but they are only one part of the immune response. Vaccines also activate immune cells called T cells. These cells have two main roles, coordinating the immune response and killing cells infected with viruses. It is likely that they play a key role in preventing severe COVID-19.

There are many kinds of T cells, each with a different role. Currently, the identity and characteristics of the T cells that protect against COVID-19 is unclear. Different types of T cells have unique proteins on their surface. Examining these proteins can reveal details about how the T cells work, which part of the virus they recognise, and which part of the body they protect. A tool called cytometry by time of flight allows researchers to measure these proteins, one cell at a time.

Using this technique, Neidleman, Luo et al. investigated T cells from 11 people before vaccination and after their first and second doses. Five people had never had COVID-19 before, and six had already recovered from COVID-19. Neidleman, Luo et al. found that the T cells recognizing SARS-CoV-2 in the two groups differed. In people who had never had COVID-19 before, the second dose of vaccine improved the quality and quantity of the T cells. The same was not true for people who had already recovered from COVID-19. However, although their T cells did not improve further after a second vaccine dose, they did show signs that they might offer more protection overall. The proteins on the cells suggest that they might last longer, and that they might specifically protect the nose, throat and lungs. Neidleman, Luo et al. also found that, for both groups, T cells activated by vaccination responded in the same way to different variants of the virus.

This work highlights the importance of getting both vaccine doses for people who have never had COVID-19. It also suggests that vaccination in people who have had COVID-19 may generate better T cells. Larger studies could show whether these patterns remain true across the wider population. If so, it is possible that delivering vaccines to the nose or throat could boost immunity by mimicking natural infection. This might encourage T cells to make the surface proteins that allow them to home to these areas.

A year and a half since the December 2019 emergence of SARS-CoV-2, the novel betacoronavirus had already infected almost 200 million people and taken the lives of over 4 million, nearly collapsed worldwide health systems, disrupted the global economy, and perturbed society and public health on a scale not experienced within the past 100 years. Fortunately, multiple highly efficacious vaccines, including the two-dose mRNA-based ones developed by Pfizer/BioNTech and Moderna, which confer ~90 % protection against disease, were approved for emergency use before the end of 2020. Although the vaccines provide the most promising route for a rapid exit from the COVID-19 pandemic, concerns remain regarding the durability of the immunity elicited by these vaccines and the extent to which they will protect against the variants of SARS-CoV-2 now spreading rapidly around the world.

The first variant observed to display a survival advantage was the D614G, which was more transmissible than the original strain and quickly became the dominant variant throughout the world Korber et al., 2020. This variant, fortunately, did not evade immunity and in fact appeared to be more sensitive than the original strain to antibody neutralization by convalescent sera Weissman et al., 2021. More worrisome, however, was the emergence at the end of 2020 of rapidly spreading variants in multiple parts of the world, including B.1.1.7, B.1.351, P.1, and B.1.427/B.1.429 (originally identified in United Kingdom, South Africa, Brazil, and California, respectively) Plante et al., 2021, followed by additional highly transmissible variants in 2021 including the B.1.617.2 which was first detected in India Callaway, 2021. Some variants, including B.1.1.7, may be more virulent Davies et al., 2021. While antibodies against the original strain elicited by either vaccination or infection generally remain potent against B.1.1.7, their activity against B.1.351 and P.1 is compromised Wang et al., 2021; The CITIID-NIHR BioResource COVID-19 Collaboration et al., 2021; Muik et al., 2021; Garcia-Beltran et al., 2021; Stamatatos et al., 2021; Cele et al., 2021; Hoffmann et al., 2021; Planas et al., 2021; Edara et al., 2021; Kuzmina et al., 2021. Antibodies from vaccinees were 14-fold less effective against B.1.351 than against the ancestral strain, and a subset of individuals completely lacked neutralizing antibody activity against B.1.351 9 months or more after convalescence Planas et al., 2021.

Reassuringly, early data suggest that relative to antibody responses, T-cell-mediated immunity appears to be less prone to evasion by the variants Skelly et al., 2021; Tarke et al., 2021; Redd et al., 2021; Geers et al., 2021; Woldemeskel et al., 2021; Stankov et al., 2021; Tauzin et al., 2021. Among 280 CD4+ and 523 CD8+ T cell epitopes from the original SARS-CoV-2, an average of 91.5 % (for CD4) and 98.1 % (for CD8) mapped to regions not mutated in the B.1.1.7, B1.351, P.1, and B.1.427/B.1.429 variants. Focusing on just the spike response, the sole SARS-CoV-2 antigen in the mRNA-based vaccines, then 89.7 % of the CD4+ epitopes and 96.4 % of the CD8+ epitopes are conserved Tarke et al., 2021. In line with this, the magnitude of the response of T cells from convalescent or vaccinated individuals was not markedly reduced when assessed against any of the variants Tarke et al., 2021. The relative resistance of T cells against SARS-CoV-2 immune evasion is important in light of the critical role these immune effectors play during COVID-19. T cell numbers display a strong, inverse association with disease severity Chen et al., 2020; Woodruff et al., 2020, and the frequency of SARS-CoV-2-specific T cells predicts recovery from severe disease Rydyznski Moderbacher et al., 2020; Neidleman et al., 2021. SARS-CoV-2-specific T cells can also provide long-term, self-renewing immunological memory: these cells are detected more than half a year into convalescence and can proliferate in response to homeostatic signals Dan et al., 2021; Neidleman et al., 2020b. Furthermore, the ability of individuals with inborn deficiencies in B cell responses to recover from COVID-19 without intensive care suggests that the combination of T cells and innate immune mechanisms is sufficient for recovery when antibodies are lacking Soresina et al., 2020.

Although T cells against the ancestral strain display a response of similar magnitude and breadth to the variants Tarke et al., 2021, to what extent these T cells’ phenotypes and effector functions differ during their response to variant detection is a different question. Small changes in the sequences of T cell epitopes, in the form of altered peptide ligands (APLs), can theoretically alter how the T cells respond to stimulation. Indeed, change of a single residue can convert a proliferative, IL4-secreting effector response into one that continues to produce IL4 in the absence of proliferation Evavold and Allen, 1991. Furthermore, APLs can activate Th1 cells without inducing either proliferation or cytokine production, shift Th1 responses into Th2-focused ones, and in some instances even render T cells anergic or immunoregulatory by eliciting TGFβ production Sloan-Lancaster and Allen, 1996.

Another important aspect that has not been explored is to what extent vaccine- vs. infection-induced T cell responses differ phenotypically and functionally, and to what extent convalescent individuals benefit from vaccination as they already harbor some form of immunity against the virus. Studies based on the antibody and B cell response suggest that for COVID-19 convalescents, a single dose of the mRNA vaccines is helpful while the additional booster is not necessary Stamatatos et al., 2021; Goel et al., 2021; Ebinger et al., 2021; how this translates in the context of vaccine-elicited T cell immunity is not clear.

To address these knowledge gaps, we conducted 39-parameter phenotyping by CyTOF on 33 longitudinal specimens from 11 mRNA-vaccinated individuals, six of whom had previously contracted and recovered from COVID-19. For each participant, blood specimens were obtained prior to vaccination, two weeks following the first dose, and two weeks following the second. For every specimen, we assessed in depth the phenotypes and effector functions of total CD4+ and CD8+ T cells, and of CD4+ and CD8+ T cells responding to the original SARS-CoV-2 spike, to spike from variants B.1.1.7 and B.1.351, and to nucleocapsid. By conducting analyses on the resulting 165 high-dimensional datasets generated, we find a reassuringly unaltered T cell response against the variants, an ability of the booster dose to alter the phenotypes of vaccine-elicited T cells, and a striking impact of prior infection on qualitative features of T cells elicited by vaccination.

T cells are important orchestrators and effectors during antiviral immunity. They may hold the key to long-term memory due to their ability to persist for decades, yet these cells have been disproportionately understudied relative to their humoral immune counterparts in the context of COVID-19. Here, we designed a longitudinal study assessing both the frequency and phenotypic characteristics of SARS-CoV-2-specific T cells in order to address the following questions: (1) Do SARS-CoV-2-specific T cells elicited by vaccination respond similarly to ancestral and variant strains?; (2) To what extent is the second dose needed for boosting T cell responses in infection-naïve and convalescent individuals?; and (3) Do vaccine-elicited memory T cells differ in infection-naïve vs. convalescent individuals?

To answer the first question, we compared post-vaccination SARS-CoV-2 spike-specific T cell responses against ancestral vs. the variant B.1.1.7 and B.1.351 strains. Consistent with recent studies Skelly et al., 2021; Tarke et al., 2021; Redd et al., 2021; Geers et al., 2021; Woldemeskel et al., 2021; Stankov et al., 2021; Tauzin et al., 2021, we find that vaccination-elicited T cells specific to the ancestral spike protein also recognize variant spike proteins. We further demonstrate that the phenotypic features of these cells are identical, whether they are stimulated by ancestral or variant spike proteins. This was important to establish because of prior reports that effector T cells can respond differently to APLs by altering their cytokine production or by mounting an immunoregulatory response Evavold and Allen, 1991; Sloan-Lancaster and Allen, 1996. APLs could theoretically arise when a variant infects an individual that was previously exposed to ancestral spike through vaccination or prior infection. That both the quantity and quality of T cell responses is maintained against the variants may provide an explanation for the real-world efficacy of the vaccines against variants. Although limited data are available, thus far all vaccines deployed in areas where the B.1.1.7 or B.1.351 strains dominate have protected vaccinees from severe and fatal COVID-19 Gupta, 2021. Given the potentially important role of SARS-CoV-2-specific T cells in protecting against severe and fatal COVID-19 Neidleman et al., 2021; Dan et al., 2021, we postulate that this protection may have been in large part mediated by vaccine-elicited T cells. In contrast, efficacy of the vaccines against mild or moderate disease in variant-dominated regions of the world is more variable. For example, in South Africa where B.1.351 is dominant, the AstraZeneca ChAdOx1 vaccine only prevented ~10 % of mild-to-moderate disease cases Madhi et al., 2021, while more recent data from Pfizer/BioNTech’s vaccine administered in Qatar, where both B.1.1.7 and B.1.351 are dominant, revealed that fully vaccinated individuals were 75 % less likely to develop COVID-19 Abu-Raddad et al., 2021. The overall diminished vaccine-mediated protection against milder disease in variant-dominated regions of the world might be explained by the likely important role of antibodies to prevent initial infection by blocking viral entry into host cells (manifesting as protection against asymptomatic and mildly symptomatic infection), and the observation that vaccine-elicited antibodies are generally less effective against the variant than against ancestral spike in lab assays Wang et al., 2021; The CITIID-NIHR BioResource COVID-19 Collaboration et al., 2021; Muik et al., 2021; Garcia-Beltran et al., 2021; Stamatatos et al., 2021; Cele et al., 2021; Hoffmann et al., 2021; Planas et al., 2021; Edara et al., 2021; Kuzmina et al., 2021. Reassuringly, there is no evidence that vaccinated individuals mount a weaker immune response to variants than do unvaccinated individuals, which could theoretically result through a phenomenon termed original antigenic sin (where the recall response is inappropriately diverted to the vaccination antigen at the expense of a protective response against the infecting variant strain) Klenerman and Zinkernagel, 1998.

To address the second question of whether a booster dose is needed, we compared the T cells after the first vs. second vaccination doses, among the infection-naïve and convalescent individuals. In infection-naïve individuals, spike-specific responses were observed after the first vaccination dose, and were further boosted after the second. This enhancement of the T cell response after the second dose is similar to the reported increase in anti-spike IgG levels after a second dose in infection-naïve individuals Goel et al., 2021; Ebinger et al., 2021. Interestingly, phenotypic changes were also observed after the second dose in that the B cells producing the anti-spike antibodies differentiated from IgM-dominant to IgG-dominant producers Goel et al., 2021. We also observed some phenotypic changes among spike-specific CD4+ T cells after the second dose, as reflected by an increase in the Ttm response at the expense of the Tcm response. Importantly, however, after either dose, spike-specific CD4+ T cells were still primarily Tcm and Tfh cells, the latter of which are important for providing helper function for B cells. The prominence of SARS-CoV-2-specific Tfh cells after just one dose of vaccination is consistent with prior reports that a single dose of SARS-CoV-2 mRNA in mice is sufficient to elicit potent B and Tfh cell responses in germinal centers Lederer et al., 2020. These results suggest that with regard to T cells, the booster dose is necessary for enhancing the magnitude and results in some phenotypic changes although a robust Tfh response is already established the first dose. Overall, our conclusions are in line with those drawn from serological studies Goel et al., 2021; Ebinger et al., 2021: that it is important to administer the second vaccine dose in infection-naïve individuals to boost spike-specific responses.

A different situation appears to be the case for convalescent individuals. Longitudinal serological studies suggest that the spike-specific antibody response in convalescent individuals after the first mRNA dose is already equivalent to that of infection-naïve individuals after their second mRNA dose Goel et al., 2021; Ebinger et al., 2021, suggesting that convalescent individuals may only need a single dose of vaccination. We found no evidence of increased numbers of spike-specific CD4+ T cells after the second dose, and minimal phenotypic changes between the cells at the two post-vaccination timepoints. Spike-specific CD4+ T cells from these individuals did however exhibit marked phenotypic changes as they transitioned from the pre- to the post-vaccination timepoints. This was expected since the cells from the pre-vaccination timepoint are resting memory CD4+ T cells that were primed months prior, while the post-vaccination timepoints were more recently-reactivated memory cells. Interestingly, unlike for the infection-naïve individuals where all individuals responded similarly to each dose of vaccination, the magnitude of the CD4+ T cell response differed markedly between different convalescent individuals. PID4112 had a large pool of spike-specific CD4+ T cells prior to vaccination, and their numbers increased to extremely high levels after the first vaccination dose. Surprisingly, this large peak in the spike-specific response was accompanied by an increase in the nucleocapsid-specific CD4+ T cells, which was unexpected since the vaccine does not contain nucleocapsid. We suspect this high response to nucleocapsid was due to inflammation-mediated bystander activation of T cells in an antigen-independent manner. Consistent with this hypothesis, the participant reported severe side effects (severe headache, chills, myalgia, nausea, and diarrhea) after the first dose. The remaining five convalescent donors, by contrast, never exhibited a robust T cell response, and in fact after full vaccination actually exhibited a highly significantly lower CD4+ T cell response than the infection-naïve vaccinees. We speculate on an explanation further below. Overall, our results suggest that a second SARS-CoV-2 vaccine dose in individuals who have recovered from COVID-19 may provide less benefit than in individuals who have not previously been exposed to SARS-CoV-2; these findings are in line with recommendations from previously published serological studies Stamatatos et al., 2021; Goel et al., 2021; Ebinger et al., 2021.

One of the most striking observations from this study, and the third and final question we set out to answer, was the remarkably distinct phenotypes of spike-specific CD4+ T cells from infection-naïve vs. convalescent individuals who were fully vaccinated. The spike-specific CD4+ T cells from the convalescent individuals harbored features suggesting increased potential for long-term persistence: they were enriched for Tcm cells, which are have longer in vivo half-lives than their Tem and Ttm counterparts Bacchus-Souffan et al., 2021, and express elevated levels of CD127, a marker of long-lived memory T cells Kaech et al., 2003. Interestingly, CD127 expression on SARS-CoV-2-specific T cells has been implicated in COVID-19 disease amelioration and in these cells’ long-term persistence. CD127 expression was more frequent on spike-specific CD4+ T cells from ICU patients who eventually survived severe COVID-19 than in those that did not Neidleman et al., 2021. IL7, the ligand for CD127, can drive homeostatic proliferation and expansion of spike-specific CD4+ T cells Neidleman et al., 2020b, and CD127 is not only expressed on SARS-CoV-2-specific memory CD4+ and CD8+ T cells, but its levels increase further over the course of convalescence Neidleman et al., 2020b; Ma et al., 2021. Together, these findings suggest that after vaccination, spike-specific CD4+ T cells in convalescent individuals may persist longer than those from infection-naïve individuals, but additional long-term follow-up studies will be required to directly test whether this indeed is the case.

Another interesting characteristic of post-vaccination spike-specific CD4+ T cells from convalescent individuals relative to infection-naïve individuals was their expression of multiple tissue-homing receptors. In particular, these cells were preferentially CCR7+ CD62L + and CXCR4+ CD69+. CCR7 and CD62L mediate homing to lymph nodes, while CXCR4 is a chemokine receptor important in migration of hematopoietic stem cells to bone marrow, but also able to direct immune cells to the lung during inflammation Mamazhakypov et al., 2021. Interestingly, we recently observed co-expression of CXCR4 with CD69 (an activation marker that also identifies T resident memory cells) in pulmonary T cells from COVID-19 patients Neidleman et al., 2021. Many of these cells were bystander (non-SARS-CoV-2-specific) CXCR4+ CD69+ T cells whose numbers in blood increased prior to death from COVID-19. We therefore proposed a model whereby recruitment of non-SARS-CoV-2-specific T cells into the lungs of severe patients may exacerbate the cytokine storm and thereby contribute to death Neidleman et al., 2021. In the case of the vaccinated convalescent individuals, however, expression of CXCR4 and CD69 on SARS-CoV-2-specific T cells is expected to be beneficial as it would direct the T cells capable of recognizing infected cells into the lung. CCR7 and CD62L co-expression would further enable these cells to enter draining lymph nodes and participate in germinal center reactions. Supporting the hypothesis that the post-vaccination spike-specific CD4+ T cells from convalescent individuals may better home to lymphoid tissues is our observation that frequencies of these cells in blood correlated negatively with the extent to which they co-expressed CCR7 and CD62L. This was further supported by our finding that CD4+ T cells from the nasopharynx of the upper respiratory tract were preferentially CCR7+ CD62L + and CXCR4+ CD69+ relative to their blood counterparts. All together, these results imply that compared to infection-naïve individuals, convalescents’ spike-specific CD4+ T cells may be superior in surviving and migrating to the respiratory tract. Directly testing this hypothesis will require obtaining large numbers of respiratory tract cells from vaccinated, infection-naïve vs. convalescent individuals (e.g. via bronchoalveolar lavages or endotracheal aspirates), or from animal models of SARS-CoV-2 infection, for quantitation and characterization of SARS-CoV-2-specific T cells. Of note, vaccination of infection-naïve individuals might not induce a strong humoral immunity in the respiratory mucosa either, as neutralizing antibodies against SARS-CoV-2 are rarely detected in nasal swabs from vaccinees Planas et al., 2021. If it turns out that current vaccination strategies do not ensure robust humoral and cell-mediated immune responses in the respiratory tract, then strategies that better elicit mucosal-homing SARS-CoV-2-specific B and T cells in infection-naïve individuals – for example by implementing an intranasal route of mRNA immunization – may hold a greater chance of achieving sterilizing immunity.

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Author details

1. Jason Neidleman

   1. Department or Urology, University of California, San Francisco, San Francisco, United States
   2. Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Data curation, Formal analysis, Investigation, Methodology, Writing - review and editing

   Contributed equally with

   Xiaoyu Luo

   Competing interests

   No competing interests declared

2. Xiaoyu Luo

   Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Data curation, Formal analysis, Methodology, Visualization, Writing - review and editing

   Contributed equally with

   Jason Neidleman

   Competing interests

   No competing interests declared

3. Matthew McGregor

   1. Department or Urology, University of California, San Francisco, San Francisco, United States
   2. Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

4. Guorui Xie

   1. Department or Urology, University of California, San Francisco, San Francisco, United States
   2. Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

5. Victoria Murray

   University of California, San Francisco, San Francisco, United States

   Contribution

   Resources

   Competing interests

   No competing interests declared

6. Warner C Greene

   Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Funding acquisition, Supervision, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9896-8615

7. Sulggi A Lee

   Medicine, University of California, San Francisco, San Francisco, United States

   Contribution

   Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Writing - review and editing

   For correspondence

   Sulggi.lee@ucsf.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1560-2250

8. Nadia R Roan

   1. Department or Urology, University of California, San Francisco, San Francisco, United States
   2. Gladstone Institute of Virology, San Francisco, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing - original draft

   For correspondence

   nadia.roan@gladstone.ucsf.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5464-1976

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