A targeted single mutation in influenza A virus universal epitope transforms immunogenicity and protective immunity via CD4+ T cell activation

Cell Rep. 2024 Jun 25;43(6):114259. doi: 10.1016/j.celrep.2024.114259. Epub 2024 May 30.

Abstract

CD4+ T cells are central to adaptive immunity. Their role in cross-protection in viral infections such as influenza and severe acute respiratory syndrome (SARS) is well documented; however, molecular rules governing T cell receptor (TCR) engagement of peptide-human leukocyte antigen (pHLA) class II are less understood. Here, we exploit an aspect of HLA class II presentation, the peptide-flanking residues (PFRs), to "tune" CD4+ T cell responses within an in vivo model system of influenza. Using a recombinant virus containing targeted substitutions at immunodominant HLA-DR1 epitopes, we demonstrate limited weight loss and improved clinical scores after heterosubtypic re-challenge. We observe enhanced protection linked to lung-derived influenza-specific CD4+ and CD8+ T cells prior to re-infection. Structural analysis of the ternary TCR:pHLA complex identifies that flanking amino acids influence side chains in the core 9-mer peptide, increasing TCR affinity. Augmentation of CD4+ T cell immunity is achievable with a single mutation, representing a strategy to enhance adaptive immunity that is decoupled from vaccine modality.

Keywords: CD4(+) T cell; CP: Immunology; HLA-DR1; influenza A virus; lung CD8(+) tissue-resident memory T cell; peptide-flanking residues; vaccine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Epitopes / immunology
  • Female
  • Humans
  • Influenza A virus* / genetics
  • Influenza A virus* / immunology
  • Influenza, Human / immunology
  • Influenza, Human / prevention & control
  • Influenza, Human / virology
  • Lymphocyte Activation / immunology
  • Mice
  • Mutation*
  • Orthomyxoviridae Infections / immunology
  • Orthomyxoviridae Infections / virology
  • Receptors, Antigen, T-Cell* / genetics
  • Receptors, Antigen, T-Cell* / immunology
  • Receptors, Antigen, T-Cell* / metabolism

Substances

  • Epitopes
  • Receptors, Antigen, T-Cell