Staggered immunization with mRNA vaccines encoding SARS-CoV-2 polymerase or spike antigens broadens the T cell epitope repertoire

Proc Natl Acad Sci U S A. 2024 Dec 3;121(49):e2406332121. doi: 10.1073/pnas.2406332121. Epub 2024 Nov 26.

Abstract

Combining a T cell-targeting mRNA vaccine encoding the conserved SARS-CoV-2 RNA-dependent RNA polymerase, RdRp, with a Spike-encoding mRNA vaccine may offer an additional pathway toward COVID-19 protection. Here, we show that a nucleoside-modified RdRp mRNA vaccine raises robust and durable CD8+ T cell responses in mice. Immunization drives a CD8+ T cell response enriched toward a specific RdRp epitope. Unexpectedly, coadministration of mRNA vaccines encoding RdRp or the Spike Receptor Binding Domain (RBD) dampens RBD-specific immune responses. Contralateral administration reduces the suppression of RBD-specific T cell responses while type I interferon signaling blockade restores RBD-specific antibodies. A staggered immunization strategy maintains both RBD vaccine-mediated antibody and T cell responses as well as protection against lethal SARS-CoV-2 challenge in human ACE2 transgenic mice. In HLA-A2.1 transgenic mice, the RdRp vaccine elicits CD8+ T cell responses against HLA-A*02:01-restricted epitopes recognized by human donor T cells. These results highlight RdRp as a candidate antigen for COVID-19 vaccines. The findings also offer insights into crafting effective multivalent mRNA vaccines to broaden CD8+ T cell responses against SARS-CoV-2 and potentially other viruses with pandemic potential.

Keywords: SARS-CoV-2; T cell receptor specificity; anti-pathogen T cell response; interferon signaling; mRNA vaccines.

MeSH terms

  • Angiotensin-Converting Enzyme 2 / genetics
  • Angiotensin-Converting Enzyme 2 / immunology
  • Angiotensin-Converting Enzyme 2 / metabolism
  • Animals
  • Antibodies, Viral / immunology
  • CD8-Positive T-Lymphocytes* / immunology
  • COVID-19 Vaccines* / administration & dosage
  • COVID-19 Vaccines* / immunology
  • COVID-19* / immunology
  • COVID-19* / prevention & control
  • Epitopes, T-Lymphocyte* / immunology
  • Female
  • HLA-A2 Antigen / genetics
  • HLA-A2 Antigen / immunology
  • Humans
  • Immunization
  • Mice
  • Mice, Transgenic*
  • SARS-CoV-2* / immunology
  • Spike Glycoprotein, Coronavirus* / genetics
  • Spike Glycoprotein, Coronavirus* / immunology
  • Vaccines, Synthetic / administration & dosage
  • Vaccines, Synthetic / immunology
  • mRNA Vaccines* / immunology

Substances

  • Spike Glycoprotein, Coronavirus
  • Epitopes, T-Lymphocyte
  • mRNA Vaccines
  • COVID-19 Vaccines
  • spike protein, SARS-CoV-2
  • Vaccines, Synthetic
  • HLA-A2 Antigen
  • Angiotensin-Converting Enzyme 2
  • Antibodies, Viral