Lung influenza virus-specific memory CD4 T cell location and optimal cytokine production are dependent on interactions with lung antigen-presenting cells

Mucosal Immunol. 2024 Oct;17(5):843-857. doi: 10.1016/j.mucimm.2024.06.001. Epub 2024 Jun 6.

Abstract

Influenza A virus (IAV) infection leads to the formation of mucosal memory CD4 T cells that can protect the host. An in-depth understanding of the signals that shape memory cell development is required for more effective vaccine design. We have examined the formation of memory CD4 T cells in the lung following IAV infection of mice, characterizing changes to the lung landscape and immune cell composition. IAV-specific CD4 T cells were found throughout the lung at both primary and memory time points. These cells were found near lung airways and in close contact with a range of immune cells including macrophages, dendritic cells, and B cells. Interactions between lung IAV-specific CD4 T cells and major histocompatibility complex (MHC)II+ cells during the primary immune response were important in shaping the subsequent memory pool. Treatment with an anti-MHCII blocking antibody increased the proportion of memory CD4 T cells found in lung airways but reduced interferon-γ expression by IAV-specific immunodominant memory CD4 T cells. The immunodominant CD4 T cells expressed higher levels of programmed death ligand 1 (PD1) than other IAV-specific CD4 T cells and PD1+ memory CD4 T cells were located further away from MHCII+ cells than their PD1-low counterparts. This distinction in location was lost in mice treated with anti-MHCII antibodies. These data suggest that sustained antigen presentation in the lung impacts the formation of memory CD4 T cells by regulating their cytokine production and location.

MeSH terms

  • Animals
  • Antigen-Presenting Cells* / immunology
  • Antigen-Presenting Cells* / metabolism
  • CD4-Positive T-Lymphocytes* / immunology
  • Cell Communication / immunology
  • Cytokines* / metabolism
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Immunologic Memory*
  • Influenza A virus* / immunology
  • Lung* / immunology
  • Lung* / virology
  • Memory T Cells* / immunology
  • Memory T Cells* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Orthomyxoviridae Infections* / immunology
  • Programmed Cell Death 1 Receptor / metabolism

Substances

  • Cytokines
  • Histocompatibility Antigens Class II
  • Programmed Cell Death 1 Receptor