Cytomegalovirus inhibition of extrinsic apoptosis determines fitness and resistance to cytotoxic CD8 T cells

Proc Natl Acad Sci U S A. 2020 Jun 9;117(23):12961-12968. doi: 10.1073/pnas.1914667117. Epub 2020 May 22.

Abstract

Viral immune evasion is currently understood to focus on deflecting CD8 T cell recognition of infected cells by disrupting antigen presentation pathways. We evaluated viral interference with the ultimate step in cytotoxic T cell function, the death of infected cells. The viral inhibitor of caspase-8 activation (vICA) conserved in human cytomegalovirus (HCMV) and murine CMV (MCMV) prevents the activation of caspase-8 and proapoptotic signaling. We demonstrate the key role of vICA from either virus, in deflecting antigen-specific CD8 T cell-killing of infected cells. vICA-deficient mutants, lacking either UL36 or M36, exhibit greater susceptibility to CD8 T cell control than mutants lacking the set of immunoevasins known to disrupt antigen presentation via MHC class I. This difference is evident during infection in the natural mouse host infected with MCMV, in settings where virus-specific CD8 T cells are adoptively transferred. Finally, we identify the molecular mechanism through which vICA acts, demonstrating the central contribution of caspase-8 signaling at a point of convergence of death receptor-induced apoptosis and perforin/granzyme-dependent cytotoxicity.

Keywords: CD8 T cells; apoptosis; apoptosis inhibition; cytomegalovirus; immune evasion.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Animals
  • Apoptosis / immunology
  • Caspase 8 / genetics
  • Caspase 8 / metabolism
  • Cell Line
  • Coculture Techniques
  • Cytomegalovirus / immunology*
  • Cytomegalovirus / pathogenicity
  • Cytomegalovirus Infections / immunology*
  • Cytomegalovirus Infections / virology
  • Disease Models, Animal
  • Fibroblasts
  • Granzymes / metabolism
  • Histocompatibility Antigens Class I / immunology
  • Histocompatibility Antigens Class I / metabolism
  • Host Microbial Interactions / immunology*
  • Humans
  • Immune Evasion*
  • Mice
  • Mice, Knockout
  • Muromegalovirus / genetics
  • Muromegalovirus / immunology
  • Muromegalovirus / metabolism
  • Mutagenesis
  • Perforin / genetics
  • Perforin / metabolism
  • Receptors, Death Domain / metabolism
  • Signal Transduction / immunology
  • T-Lymphocytes, Cytotoxic / immunology*
  • T-Lymphocytes, Cytotoxic / metabolism
  • Time-Lapse Imaging
  • Viral Proteins / genetics
  • Viral Proteins / immunology
  • Viral Proteins / metabolism

Substances

  • Histocompatibility Antigens Class I
  • M36 protein, mouse cytomegalovirus
  • Receptors, Death Domain
  • UL36 protein, Human herpesvirus 1
  • Viral Proteins
  • perforin 1, mouse
  • Perforin
  • Granzymes
  • CASP8 protein, human
  • Casp8 protein, mouse
  • Caspase 8