Deletion of the deISGylating enzyme USP18 enhances tumour cell antigenicity and radiosensitivity

Br J Cancer. 2021 Feb;124(4):817-830. doi: 10.1038/s41416-020-01167-y. Epub 2020 Nov 20.

Abstract

Background: Interferon (IFN) signalling pathways, a key element of the innate immune response, contribute to resistance to conventional chemotherapy, radiotherapy, and immunotherapy, and are often deregulated in cancer. The deubiquitylating enzyme USP18 is a major negative regulator of the IFN signalling cascade and is the predominant human protease that cleaves ISG15, a ubiquitin-like protein tightly regulated in the context of innate immunity, from its modified substrate proteins in vivo.

Methods: In this study, using advanced proteomic techniques, we have significantly expanded the USP18-dependent ISGylome and proteome in a chronic myeloid leukaemia (CML)-derived cell line. USP18-dependent effects were explored further in CML and colorectal carcinoma cellular models.

Results: Novel ISGylation targets were characterised that modulate the sensing of innate ligands, antigen presentation and secretion of cytokines. Consequently, CML USP18-deficient cells are more antigenic, driving increased activation of cytotoxic T lymphocytes (CTLs) and are more susceptible to irradiation.

Conclusions: Our results provide strong evidence for USP18 in regulating antigenicity and radiosensitivity, highlighting its potential as a cancer target.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigenic Variation
  • Cell Line, Tumor
  • Colorectal Neoplasms / enzymology*
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / radiotherapy
  • Cytokines / metabolism*
  • Gene Knockout Techniques
  • HCT116 Cells
  • Humans
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / enzymology*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / immunology*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / radiotherapy
  • Radiation Tolerance / genetics
  • Radiation Tolerance / immunology
  • Ubiquitin Thiolesterase / deficiency
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism*
  • Ubiquitins / metabolism*

Substances

  • Cytokines
  • Ubiquitins
  • ISG15 protein, human
  • USP18 protein, human
  • Ubiquitin Thiolesterase