SARS-CoV-2 infection enhances vaccine-induced immunological memory against spike protein

In a recent study published in the journal Science Translational Medicine, researchers in France perform a longitudinal follow-up assessment of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike (S) glycoprotein-specific immunological memory among unvaccinated and vaccinated coronavirus disease 2019 (COVID-19) convalescents, as well as COVID-19-naïve vaccinees.

Study: Prior SARS-CoV-2 infection enhances and reshapes spike protein–specific memory induced by vaccination. Image Credit: Andrus Ciprian / Shutterstock.com

Study: Prior SARS-CoV-2 infection enhances and reshapes spike protein–specific memory induced by vaccination. Image Credit: Andrus Ciprian / Shutterstock.com

Hybrid immunity against COVID-19

Hybrid immune protection against SARS-CoV-2 results from COVID-19 vaccine- and prior SARS-CoV-2 infection-induced antibodies. This hybrid immunity is associated with more robust memory B- and T- lymphocyte responses, stronger neutralizing antibodies, and a lower risk of reinfections and associated outcomes.

Evaluating immune responses induced by prior COVID-19 and subsequent vaccinations could improve the understanding of how this hybrid immunity contributes to immunological memory. Furthermore, this information could aid in identifying high-risk individuals to be prioritized for booster vaccinations against COVID-19.

About the study

In the present study, researchers compare cellular (memory lymphocytes) and serological (antibodies) immunological memory among vaccinated or unvaccinated individuals with a history of COVID-19 and SARS-CoV-2 infection-naïve vaccinated individuals.

The study comprised 613 COVID-19 patients, from the Covid-Ser and Immunonosocor cohorts. These individuals were categorized as mild or severe COVID-19 convalescents, mild COVID-19 convalescents who received single or double Pfizer’s BNT162b2 messenger ribonucleic acid (mRNA) vaccination or a single adenovirus vector-based ChAdOx1 vaccination, and SARS-CoV-2 infection-naïve individuals who received two homologous BNT162b2 doses, or heterologous ChAdOx1/BNT162b2 vaccination.

The occurrence of breakthrough infections was monitored based on the rebound of SARS-CoV-2 S receptor-binding domain (RBD) immunoglobulin G (IgG) titers using SARS-CoV-2 IgG assays. The researchers also examined serological memory B lymphocyte parameters such as avidity, neutralization potential, and titers of antibodies against the S protein subunit 1 (S1) and S RBD proteins.

The capability of serological samples to protect Vero E6 cells from infection with SARS-CoV-2 19A, Delta, or Omicron strains was assessed using 50% plaque reduction neutralization test (PRNT50) assays. In addition, human airway epithelium (HAE) cells with anti-RBD IgG titers were tested for their ability to neutralize 19A. Anti-RBD antibody avidity was determined using biolayer interferometry.

Anti-RBD memory T lymphocyte responses were assessed using interferon-gamma (IFN-γ) release assays. Comparative phenotypical analyses were performed using the cluster of differentiation (CD-137) and OX-40 as surface activation-induced markers (AIMs).

Flow cytometry was performed to analyze the anti-RBD memory B lymphocyte compartment. Anti-RBD memory B lymphocyte trafficking and expression patterns were assessed based on α4β1, α4β7, β1/β7 integrins, cutaneous lymphocyte antigen (CLA), C-C chemokine receptor (CCR)-4,7, 9, and CD62L. Matrix analysis was performed to determine the correlation between cellular and serological anti-S memory B lymphocyte markers.

Results

Vaccinated convalescents with hybrid immune protection had the highest anti-S titers at six months following vaccination. In comparison to SARS-CoV-2 infection-naïve vaccinees, vaccinated convalescents also exhibited greater frequencies of atypical (IgDCD27) mucosa-targeted subset of DN2 (double-negative type 2) CD21CD11c+ memory B lymphocytes, with an exclusive mucosal homing potential. These individuals also exhibited elevated helper T 1 (TH1) lymphocyte polarization of the anti-SARS-CoV-2 S follicular helper T lymphocyte (TFH) pool.

Cellular anti-S B lymphocyte memory was less subject to quantitative variations than its serological counterpart but more susceptible to qualitative changes instructed by prior COVID-19 history. These findings indicate that vaccinating individuals who have previously been infected with SARS-CoV-2 reinforced the serological component of memory B lymphocytes and reshaped memory B lymphocyte compartment’s composition and tracking patterns. No reinfections were reported during the six months between SARS-CoV-2 infection/vaccination and the collection of blood samples.

Median antibody titers, which are expressed as binding antibody unit (BAU)/mL, among vaccinated COVID-19 convalescents for single BNT162b2 vaccination, double BNT162b2 vaccination, and single ChAdOx vaccination were 1,214, 1,193, and 851 BAU/mL, respectively.

Unvaccinated convalescents exhibited the least anti-RBD IgG titers, particularly for mildly symptomatic COVID-19, with median values of 206 and 81 and for severe and mild SARS-CoV-2 infections, respectively. The median anti-RBD IgG titers among COVID-19 vaccinees without a history of infection were 180 and 249 for double homologous BNT162b2 and ChAdOx/BNT162b2 heterologous vaccinations, respectively.

Similar trends were observed for anti-S IgA titers. Serological samples from convalescent vaccinees displayed five- to 10-fold greater serum-neutralizing antibody titers against SARS-CoV-2 19A and Delta strains as compared to those from the convalescent or naïve vaccinated individuals. Concerning Omicron, neutralizing antibody titers were four- to 19-fold lower than those for 19A.

Similar findings were observed in the HAE model, irrespective of anti-RBD IgG titers. Anti-RBD antibodies had higher avidity among vaccinees than among unvaccinated COVID-19 convalescents, irrespective of prior COVID-19 history.

IFN-γ secretion was two- to four-fold greater in response to RBD peptides among convalescent vaccinees than unvaccinated COVID-19 convalescents or naïve homologous double BNT162b2 vaccinees. ChAdOx/ BNT162b2 vaccinees expressed IFN-γ at levels similar to that among individuals with hybrid immunity.

Significantly greater TFH1 and lower TFH2 lymphocyte frequencies were observed among convalescent COVID-19 vaccinees than among naïve vaccinees. Cellular and serological markers of anti-S memory B lymphocytes correlated with each other.

Conclusions

The study findings showed that a history of COVID-19 increased anti-S titers induced by subsequent COVID-19 vaccinations. Furthermore, hybrid immunity was characterized by anti-S memory B lymphocyte pool remodeling that is compatible with improved functional protection at mucosal sites.

Prior SARS-CoV-2 infection and vaccination conferred greater immune protection than either of them alone in terms of serological anti-S titers and neutralizing antibodies.

Journal reference:
  • Barateau, V., Peyrot, L., Saade, C., et al. (2023). Prior SARS-CoV-2 infection enhances and reshapes spike protein–specific memory induced by vaccination. Science Translational Medicine 15. doi:10.1126/scitranslmed.ade0550
Pooja Toshniwal Paharia

Written by

Pooja Toshniwal Paharia

Pooja Toshniwal Paharia is an oral and maxillofacial physician and radiologist based in Pune, India. Her academic background is in Oral Medicine and Radiology. She has extensive experience in research and evidence-based clinical-radiological diagnosis and management of oral lesions and conditions and associated maxillofacial disorders.

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