Background: Long-term immunity to SARS-CoV-2 infection, including neutralizing antibodies (nAb) and T cell-mediated immunity, is required to reduce ongoing disease burden. We investigated the association between variability of memory CD4 and CD8 T cells and levels of neutralizing antibodies in convalescent COVID-19 subjects.
Methods: Participants (n=49) were recruited in the ADAPT observational study at St Vincent’s Hospital, Sydney. SARS-CoV-2 specific CD4 T cells in PBMC, collected at 3 and 8 months post-infection, were measured by upregulation of CD25/CD134 at 48 hrs and by cell trace violet proliferation assay at day 7. Antibodies to SARS-CoV-2 spike protein were measured by a flow-based assay of binding to cells expressing variant spike proteins, and by live virus neutralization assays. Single cell RNA-seq of antigen-specific CD4 T cells was done using 10x Genomics 5’v2 Gene expression and immune profiling kit.
Results: Higher titres of nAb were associated with significantly higher levels of receptor binding domain (RBD)-specific CD4 T cells, including specific memory cells that proliferated vigorously in vitro. Conversely, low nAb titres in about half of convalescent individuals were found together with a lack of RBD-specific memory CD4 T cells. These low nAb subjects had other, non-RBD, spike-specific CD4 T cells, but they had more of an inhibitory Foxp3+ and CTLA-4+ cell phenotype. In contrast, high nAb subjects had effector T-bet+/granzymes+/perforin+ cytotoxic RBD-specific proliferative memory CD4 T cells. Single cell transcriptomics of RBD-specific CD4+ T cells from high nAb subjects revealed heterogeneity that included central and transitional memory, Tregs, and cytotoxic cell clusters containing diverse TCR repertoires. Nevertheless, vaccination of low nAb individuals led to slight but significant improvements in RBD-specific memory CD4 T cells and nAb titres.
Conclusions: Our results suggest that targeting CD4 T cell epitopes proximal to and within the RBD-region should be considered in booster vaccines.