The authors declare no competing interests. Neutralising responses in NHPs exceeded levels observed in convalescent individuals upon boosting with SARS-CoV-2 immunogens. S-specific TFH targeting either non-RBD or RBD peptides were detected in all animals; interestingly, RBD-derived peptides tended to be more frequently recognised by GC TFH than non-RBD epitopes (2.4% non-RBD, S-specific versus 6.2% RBD-specific; Fig. Nat. S-specific memory B cells were highest in S-S immunised animals (0.37%, range 0.32–0.49), and approximately equivalent frequencies in R-R (0.1925%, range 0.192–0.193), and S-R (0.12%, range 0.11–0.23) immunised animals. Safety and immunogenicity of two RNA-based COVID-19 vaccine candidates. bioRxiv https://doi.org/10.1101/2020.08.27.270975 (2020). Our results suggest that primary SARS-CoV-2 exposure protects against subsequent reinfection in rhesus macaques. Circulating follicular T helper cells and cytokine profile in humans following vaccination with the rVSV-ZEBOV Ebola vaccine. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. C Neutralisation activity in the plasma (human, macaques) or serum (mouse) was assessed using a microneutralisation assay. SARS-CoV-2 mRNA vaccines foster potent antigen-specific germinal center responses associated with neutralizing antibody generation. Comparing the humoral and cellular immunity between primary infection and rechallenge revealed notably enhanced neutralizing antibody and immune responses. J. Med. Secondary PCR products were sequenced using the secondary reverse constant chain primer using standard sanger sequencing (Macrogen). et al. Harper, D. M. et al. Deng W, Bao L, Liu J, et al. P values were derived by two-tailed Mann–Whitney U tests. Juno, J. Tiller, T., Busse, C. E. & Wardemann, H. Cloning and expression of murine Ig genes from single B cells. This study shows that previous infection with SARS-CoV-2 induces effective immunity to future infections in most individuals. Serum from mice (n = 10 per group), and plasma from macaques (n = 2 for RBD/RBD group, n = 3 for Spike/RBD and Spike/Spike groups) and human convalescent donors (n = 72) were assessed for endpoint total IgG titres measured by ELISA against A S or B RBD. Reference: [1] Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. Liu, L. et al. Any CellTrace Blue+ cells were excluded from flow cytometric analysis of B or T cell populations. Source data are provided as a source data file. Statistical significance was assessed by Mann–Whitney U tests. 2F). S6B, C), one of which was substantially more immunogenic than the others (P99, sequence TNVYADSFVIRGDEV). GC B-cell specificity was also assessed by S- or RBD-probe binding (Fig. Walls, A. C. et al. Cycling conditions for secondary PCRs were one cycle of 94 °C, 5 min; 50 cycles of 94 °C, 30 s; 57 °C, 20 s; 72 °C, 55 s; one cycle of 72 °C, 10 min; 4 °C. Tan, HX., Juno, J.A., Lee, W.S. In contrast, a single immunisation of RBD elicited minimal serum antibody in line with other reports of sub-optimal immunogenicity of RBD in mice16 and recent Phase I trials comparing RBD or S encoded by RNA-based vaccines15. In contrast, enhanced neutralisation activity was not seen in S-R immunised macaques, where titres were equivalent to S-S animals. Cells were washed twice with PBS containing 1% FCS and fixed with 1% formaldehyde (Polysciences). To assess the relative merits of RBD-focussed antibody responses versus more holistically targeting the entire S, we primed C57BL/6 mice with S or RBD, and then boosted 21 days later with either homologous or heterologous immunogens. In contrast, RBD-specific memory B cells were less frequently detected overall, with S-S (0.12%, range 0.04–0.18) animals displaying the highest level, followed by the S-R (0.04%, range 0.02–0.14) and R-R (0.04%, range 0.02–0.06) groups. Plates were developed with TMB substrate (Sigma), stopped with 0.15 M sulphuric acid and read at 450 nm. Seow, J. et al. Self-assembling influenza nanoparticle vaccines drive extended germinal center activity and memory B cell maturation. Briefly, plates containing single sorted cells were thawed and cDNA prepared using Superscript III reverse transcriptase (Invitrogen) with incubation conditions of 42 °C, 5 min; 25 °C, 5 min; 50 °C, 60 min; 94 °C, 5 min; 4 °C. Immunogenicity of prime-boost protein subunit vaccine strategies against SARS-CoV-2 in mice and macaques. In contrast, priming of mice with S resulted in consistently higher serum titres and neutralising activity, irrespective of the subsequent boosting immunogen, highlighting the impact of a broader TFH repertoire in modulating the magnitude of immune responses after boosting. Similarly, immunisation of NHP with one or two doses of SARS-CoV-2 immunogens, elicited binding antibodies at levels above the median observed in convalescent individuals. Sci. Chi, X. et al. Privacy Policy Terms and Conditions, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. The distribution of GC B and TFH responses after prime-boost immunisation were consistent in BALB/c mice (Fig. Induction of ICOS+CXCR3+CXCR5+ TH cells correlates with antibody responses to influenza vaccination. By submitting a comment you agree to abide by our Terms and Community Guidelines. Cell entry is mediated by engagement of the enzyme ACE2 on the target cell surface by the viral receptor-binding domain (RBD), localised within the C-terminal domain of S16,7. doi: 10.1126/science.abc5343. Dynamic changes in circulating T follicular helper cell composition predict neutralising antibody responses after yellow fever vaccination. Mason, R. D. et al. Reinfection rates among patients who previously tested positive for COVID-19: a retrospective cohort study. Barber-Axthelm, I. M. et al. Multiple factors likely contribute to the differential responses between species including size, microbiome and the fact that macaques are an outbred population with diverse MHC and immunoglobulin alleles. As a reference, S- and RBD-specific antibody and serum neutralisation titres were assessed in a panel of 72 convalescent donors recovered from COVID-19 (participant details in Table 1). Deng W, Bao L, Liu J, et al. In a separate study that included many of the same researchers, titled “DNA vaccine protection against SARS-CoV-2 in rhesus macaques,” the team developed a … A Reciprocal endpoint titres of S- or RBD-specific IgG were measured in longitudinal plasma samples by ELISA. For macaques, a single-cell suspension was prepared from the draining iliac lymph node of a single animal 14 days after a second immunisation with S. Single S- (S+RBD−) and RBD-specific (S+RBD+) IgG+ B cells were stained as above and sorted using a BD Aria II into 96-well plates. Neutralizing antibodies correlate with protection from SARS-CoV-2 in humans during a fishery vessel outbreak with high attack rate. Selective RBD focussing translated into increased serum neutralisation, with S-R eliciting 2.5-fold higher activity (median 361; IQR 226–706) compared to S-S (143; IQR 96–254) (p = 0.0055) (Fig. 2056689), and all associated procedures were carried out in accordance with approved guidelines. S is a type 1 viral fusion protein, expressed as a single polypeptide and cleaved into S1 and S2 subunits, with a heterotrimeric quaternary structure common to many respiratory viruses reviewed in5. SARS-CoV-2 protein subunit vaccination elicits potent neutralizing antibody responses. However, the comparative performance of each immunogen in pre-clinical animal models, and the potential for combinatorial use in heterologous prime-boost strategies, is unclear. Cells were then surface stained with S/RBD probes and the following antibodies: B220 BUV737 (RA3-6B2; BD; 1:300), IgD BUV395 (11–26 c.2a; BD; 1:300), CD45 APC-Cy7 (30-F11; BD; 1:300), SA BV786 (BD; 1:300), GL7 AF488 (GL7; Biolegend; 1:300), CD38 PE-Cy7 (90; Biolegend; 1:750), CD3 BV786 (145-2C11; Biolegend; 1:750) and F4/80 BV786 (BM; Biolegend; 1:150). Kelly, H. G. et al. Data is generally presented as median +/− interquartile range or range. Stephen J. Kent or Adam K. Wheatley. We find in mice that RBD is relatively poorly immunogenic compared to S, with primary immunisation compromised by a reduced capacity to efficiently induce germinal centre B cells and recruit effective T follicular helper cells. SARS-CoV-2, which is the prime target of neutralising antibody responses. Nat Commun 12, 1403 (2021). Phase 1-2 trial of a SARS-CoV-2 recombinant spike protein nanoparticle vaccine. Transl. The primary immunogenicity of SARS-CoV-2 S and RBD was assessed in groups of C57BL/6 mice vaccinated with S, RBD or control ovalbumin (OVA) proteins. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Boosting S-primed mice with either S or RBD significantly augments neutralising titres, with RBD-focussing driving moderate improvement in serum neutralisation. Data is presented as median ± IQR. Rapid decay of anti–SARS-CoV-2 antibodies in persons with mild COVID-19. Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. We have previously observed differences in vaccine antigen immunogenicity between small and large animal models35, highlighting the value of NHP models in clarifying the translational pathway of prototypic vaccines to humans. Or alternatively, do additional epitopes across the larger S protein make additive contributions to immunogenicity or neutralisation that counteract any off-target immune distraction? Published online July 2, 2020 . https://doi.org/10.1038/s41467-021-21665-8, DOI: https://doi.org/10.1038/s41467-021-21665-8. Macaque studies and related experimental procedures were approved by the Monash University Animal Ethics Committee (no. Science 369, 818–823 (2020). B The capacity of plasma antibodies to inhibit the interaction of RBD and human ACE2 was assessed by ELISA. Overall, these data suggest differences in both the magnitude, and qualitative aspects of the humoral response, exist between S-specific antibody elicited by infection versus by immunisation with pre-fusion stabilised S immunogens. 7. Our results suggest that primary SARS-CoV-2 exposure protects against subsequent reinfection in rhesus macaques. Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial. After initial viral clearance, upon rechallenge, the animals showed a 5 log 10 reduction in median viral loads compared with primary infection and an anamnestic humoral and cellular immune response. Plasma was heat inactivated at 56 °C for 30 min. These studies confirm recombinant S proteins as promising vaccine candidates and highlight multiple pathways to achieving potent serological neutralisation. and K.S. Immunity 53, 1281–1295.e5 (2020). The SIREN study does have several limitations. Antibodies capable of preventing RBD binding to ACE2 can therefore prevent infection and constitute an efficient pathway to neutralisation. The profile of B and T cell immunity was assessed in draining lymph nodes 2 weeks after the boost immunisation. Consistent with GC B-cell frequencies, immunisation with S induced high frequencies of T follicular helper (TFH) cells (CXCR5++BCL-6+; median 0.7%; 0.3–1.1) relative to OVA (median 0.4%; 0.2–0.8) or RBD (median 0.13%; 0.1–0.2) (Fig. Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. ADS and S.J.K. Science 367, 1260–1263 (2020). 1D). Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques, Science (2020). Reinfection with a SARS-CoV-2 variant virus has been reported in Brazil, (69,70,71) the U.K., (72) and South Africa. The spike (S) glycoprotein of SARS-CoV-2 is a clear target for vaccines designed to elicit neutralising antibodies to prevent infection. Med. S12A) were also detected in all draining lymph nodes (11.4% of total LN CD4+ T cells), with a median of 13% exhibiting recent proliferation as measured by Ki-67 expression (Fig. Nevertheless, the limited recognition of the RBD by B and cTFH cells following SARS-CoV-2 infection17 suggests that at a population level, RBD-based immunogens might be less reliable vaccine antigens than S, which was robustly immunogenic in all species. All statistical analyses were performed using Prism (GraphPad). Caly, L. et al. Responses in macaques were notably more variable than mice. 0 × 10 11 viral particles by the intramuscular route without adjuvant) induces strong neutralising antibody responses and provides protection against SARS-CoV-2 challenge in rhesus macaques aged 6–12 years. However, we find RBD boosting of S-primed animals (S-R) markedly increased RBD-specific serum antibody titres 4.2-fold relative to S-S (p = 0.0055). 3G). 2020 Jul 2. Lancet 364, 1757–1765 (2004). [Published online ahead of print]. Cell https://doi.org/10.1016/j.cell.2020.07.012 (2020). 78, 3572–3577 (2004). ICOS + PD-1 + CXCR3 + T follicular helper cells contribute to the generation of high-avidity antibodies following influenza vaccination. S1). 23. Genomic evidence for reinfection with SARS-CoV-2: a case study. More information: Wei Deng et al. Peer review information Nature Communications thanks Smita Iyer, Karin Lore and Monica Vaccari for their contribution to the peer review of this work. Inhibition of ACE2-RBD interaction by serum antibodies was similarly enhanced in the S-R group compared to the S-S group (Figs. All authors reviewed the manuscript. Mice were serially immunised intramuscularly at a 21-day interval with S, RBD or OVA proteins and immune responses assessed 14 days post boost (n = 10 animals across two independent experiments). doi: 10.1126/science.abc5343 OpenUrl Abstract / FREE Full Text In contrast, high frequencies of S-specific GC B cells were elicited in S-S (4.81%, range 3.41–7.71) and S-R (9.11%, range 0.82–13.6) immunised, but not R-R immunised animals. Coronavirus disease 2019 (COVID-19), which is caused by infection with the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has become a global pandemic. After blocking with 1% FCS in PBS, duplicate wells of serially diluted plasma were added and incubated for 2 h at room temperature. [1] Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. Source data are provided as a source data file. J. Clin. Samples were acquired on a BD LSR Fortessa using BD FACS Diva. J. Med. S6A). doi: 10.1126/science.abc5343 PubMed Google Scholar Crossref The SARS-CoV-2 NTD (residues 1–290) was synthesised with a C-terminal Avitag and His-tag, cloned into mammalian expression vectors and expressed in Expi293 cells. JCI Insight 5, e136653 (2020). S6B, C). Keech, C. et al. These differences might explain the comparatively high serological binding titres required in mice for neutralisation activity compared to humans and immunised primates. DNA vaccine protection against SARS-CoV-2 in rhesus macaques. Structure and immunogenicity of a stabilized HIV-1 envelope trimer based on a group-M consensus sequence. Serially diluted sera (mouse) or plasma (non-human primate, convalescent COVID-19 donors) was pre-incubated with 10 mg/ml of recombinant BSA, S, RBD or NTD proteins in 1% FCS/PBS for 2 h, before addition to S-coated plates for 15 min. Different serological assay platforms were used to determine seropositivity and not all of them have the same sensitivity over time or focus on the spike of SARS-CoV-2, which is the prime target of neutralising antibody responses. Cell https://doi.org/10.1016/j.cell.2020.02.058 (2020). By the end of this year, we should have better answers. Deng W, Bao L, Liu J et al. The SARS-CoV-2 RBD expression plasmids were kindly provided by Florian Krammer, Mt. Blue+ cells were stained with Aqua viability dye ( Thermofisher ) and South.! For 30 min primary exposure to sars-cov-2 protects against reinfection in rhesus macaques assays17 coronavirus spike proteins the Declaration of Helsinki spike protein nanoparticle drive. H Frequency of circulating memory B cell immunity was assessed by ELISA the lowest B-cell. Than the others ( P99, sequence TNVYADSFVIRGDEV ) patient primary exposure to sars-cov-2 protects against reinfection in rhesus macaques with COVID‐19 in.. 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( CXCR5++BCL-6+CD4+CD3+B220− ) and circulating follicular T helper cells contribute to the peer review of this license, http.
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