TNF and IFNγ-induced cell death requires IRF1 and ELAVL1 to promote CASP8 expression

J Cell Biol. 2024 Mar 4;223(3):e202305026. doi: 10.1083/jcb.202305026. Epub 2024 Feb 6.

Abstract

TNFα and IFNγ (TNF/IFNγ) synergistically induce caspase-8 activation and cancer cell death. However, the mechanism of IFNγ in promoting TNF-initiated caspase-8 activation in cancer cells is poorly understood. Here, we found that in addition to CASP8, CYLD is transcriptionally upregulated by IFNγ-induced transcription factor IRF1. IRF1-mediated CASP8 and CYLD upregulation additively mediates TNF/IFNγ-induced cancer cell death. Clinically, the expression levels of TNF, IFNγ, CYLD, and CASP8 in melanoma tumors are increased in patients responsive to immune checkpoint blockade (ICB) therapy after anti-PD-1 treatment. Accordingly, our genetic screen revealed that ELAVL1 (HuR) is required for TNF/IFNγ-induced caspase-8 activation. Mechanistically, ELAVL1 binds CASP8 mRNA and extends its stability to sustain caspase-8 expression both in IFNγ-stimulated and in basal conditions. Consequently, ELAVL1 determines death receptors-initiated caspase-8-dependent cell death triggered from stimuli including TNF and TRAIL by regulating basal/stimulated caspase-8 levels. As caspase-8 is a master regulator in cell death and inflammation, these results provide valuable clues for tumor immunotherapy and inflammatory diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caspase 8 / genetics
  • Cell Death
  • Deubiquitinating Enzyme CYLD / genetics
  • ELAV-Like Protein 1 / genetics
  • Humans
  • Immunotherapy*
  • Inflammation
  • Interferon Regulatory Factor-1* / genetics
  • Interferon-gamma* / genetics
  • Melanoma* / genetics
  • Mice
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • CASP8 protein, human
  • Caspase 8
  • ELAV-Like Protein 1
  • ELAVL1 protein, human
  • Interferon Regulatory Factor-1
  • IRF1 protein, human
  • IFNG protein, human
  • Interferon-gamma
  • Tumor Necrosis Factor-alpha
  • CYLD protein, human
  • Deubiquitinating Enzyme CYLD