Indirect CD4+ T cell protection against mouse gamma-herpesvirus infection via interferon gamma

J Virol. 2024 May 14;98(5):e0049324. doi: 10.1128/jvi.00493-24. Epub 2024 Apr 5.

Abstract

CD4+ T cells play a key role in γ-herpesvirus infection control. However, the mechanisms involved are unclear. Murine herpesvirus type 4 (MuHV-4) allows relevant immune pathways to be dissected experimentally in mice. In the lungs, it colonizes myeloid cells, which can express MHC class II (MHCII), and type 1 alveolar epithelial cells (AEC1), which lack it. Nevertheless, CD4+ T cells can control AEC1 infection, and this control depends on MHCII expression in myeloid cells. Interferon-gamma (IFNγ) is a major component of CD4+ T cell-dependent MuHV-4 control. Here, we show that the action of IFNγ is also indirect, as CD4+ T cell-mediated control of AEC1 infection depended on IFNγ receptor (IFNγR1) expression in CD11c+ cells. Indirect control also depended on natural killer (NK) cells. Together, the data suggest that the activation of MHCII+ CD11c+ antigen-presenting cells is key to the CD4+ T cell/NK cell protection axis. By contrast, CD8+ T cell control of AEC1 infection appeared to operate independently.

Importance: CD4+ T cells are critical for the control of gamma-herpesvirus infection; they act indirectly, by recruiting natural killer (NK) cells to attack infected target cells. Here, we report that the CD4+ T cell/NK cell axis of gamma-herpesvirus control requires interferon-γ engagement of CD11c+ dendritic cells. This mechanism of CD4+ T cell control releases the need for the direct engagement of CD4+ T cells with virus-infected cells and may be a common strategy for host control of immune-evasive pathogens.

Keywords: T cells; herpesvirus; interferon gamma; virus persistence.

MeSH terms

  • Alveolar Epithelial Cells / immunology
  • Alveolar Epithelial Cells / virology
  • Animals
  • CD11c Antigen / immunology
  • CD11c Antigen / metabolism
  • CD4-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Herpesviridae Infections* / immunology
  • Herpesviridae Infections* / virology
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Antigens Class II / metabolism
  • Interferon gamma Receptor
  • Interferon-gamma* / immunology
  • Interferon-gamma* / metabolism
  • Killer Cells, Natural* / immunology
  • Lung / immunology
  • Lung / virology
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Interferon* / genetics
  • Receptors, Interferon* / metabolism
  • Rhadinovirus* / immunology