TNF Signaling Dictates Myeloid and Non-Myeloid Cell Crosstalk to Execute MCMV-Induced Extrinsic Apoptosis

Viruses. 2020 Oct 28;12(11):1221. doi: 10.3390/v12111221.

Abstract

Cytomegaloviruses all encode the viral inhibitor of caspase-8-induced apoptosis (vICA). After binding to this initiator caspase, vICA blocks caspase-8 proteolytic activity and ability to activate caspase-3 and/or caspase-7. In this manner, vICA has long been known to prevent apoptosis triggered via tumor necrosis factor (TNF) family death receptor-dependent extrinsic signaling. Here, we employ fully wild-type murine cytomegalovirus (MCMV) and vICA-deficient MCMV (∆M36) to investigate the contribution of TNF signaling to apoptosis during infection of different cell types. ∆M36 shows the expected ability to kill mouse splenic hematopoietic cells, bone marrow-derived macrophages (BMDM), and dendritic cells (BMDC). Antibody blockade or genetic elimination of TNF protects myeloid cells from death, and caspase-8 activation accompanies cell death. Interferons, necroptosis, and pyroptotic gasdermin D (GSDMD) do not contribute to myeloid cell death. Human and murine fibroblasts or murine endothelial cells (SVEC4-10) normally insensitive to TNF become sensitized to ∆M36-induced apoptosis when treated with TNF or TNF-containing BMDM-conditioned medium. We demonstrate that myeloid cells are the natural source of TNF that triggers apoptosis in either myeloid (autocrine) or non-myeloid cells (paracrine) during ∆M36 infection of mice. Caspase-8 suppression by vICA emerges as key to subverting innate immune elimination of a wide variety of infected cell types.

Keywords: Caspase-8; DNA virus; HCMV; IFN; M36; MCMV; TNF; UL36; apoptosis; cell death; cytomegalovirus; extrinsic apoptosis; inflammation; intrinsic apoptosis; myeloid cells; necroptosis; pyroptosis; replication; vICA.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Apoptosis / genetics*
  • Caspase 8 / genetics
  • Caspase 8 / metabolism*
  • Cell Survival
  • Dendritic Cells / immunology
  • Dendritic Cells / virology
  • Endothelial Cells / immunology
  • Endothelial Cells / virology
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Macrophages / immunology
  • Macrophages / virology
  • Mice
  • Mice, Knockout
  • Muromegalovirus / immunology
  • Muromegalovirus / pathogenicity*
  • Myeloid Cells / immunology
  • Myeloid Cells / virology
  • NIH 3T3 Cells
  • Signal Transduction*
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology*
  • Viral Proteins / genetics*

Substances

  • Intracellular Signaling Peptides and Proteins
  • Tumor Necrosis Factor-alpha
  • Viral Proteins
  • Casp8 protein, mouse
  • Caspase 8