Lysine acetylation of NKG2D ligand Rae-1 stabilizes the protein and sensitizes tumor cells to NKG2D immune surveillance

Cancer Lett. 2021 Apr 1:502:143-153. doi: 10.1016/j.canlet.2020.12.002. Epub 2020 Dec 3.

Abstract

Shedding, loss of expression, or internalization of natural killer group 2, member D (NKG2D) ligands from the tumor cell surface leads to immune evasion, which is associated with poor prognosis in patients with cancer. In many cancers, matrix metalloproteinases cause the proteolytic shedding of NKG2D ligands. However, it remained unclear how to protect NKG2D ligands from shedding. Here, we showed that the shedding of the mouse NKG2D ligand Rae-1 can be prevented by two critical acetyltransferases, GCN5 and PCAF, which acetylate the lysine residues of Rae-1 to avoid shedding both in vitro and in vivo. In contrast, mutations at lysines 80 and 87 of Rae-1 abrogated this acetylation and thereby desensitized tumor cells to NKG2D-dependent immune surveillance. Notably, the protein levels of GCN5 correlated with the expression levels of the human NKG2D ligand ULPB1 in a human tumor tissue microarray and, more importantly, with prolonged overall survival in many cancers. Our results suggest that the acetylation of Rae-1 protein at lysines 80 and 87 by GCN5 and PCAF protects Rae-1 from shedding so as to activate NKG2D-dependent immune surveillance. This discovery may shed light on new targets for NKG2D immunotherapy in cancer treatment.

Keywords: Acetylation; GCN5; NKG2D ligand stabilization; PCAF.

Publication types

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

MeSH terms

  • Acetylation
  • Cell Line, Tumor
  • GPI-Linked Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lysine / genetics
  • Lysine / metabolism*
  • Mutation*
  • NK Cell Lectin-Like Receptor Subfamily K / metabolism*
  • Neoplasm Transplantation
  • Neoplasms / genetics
  • Neoplasms / metabolism*
  • Nuclear Matrix-Associated Proteins / chemistry*
  • Nuclear Matrix-Associated Proteins / genetics
  • Nuclear Matrix-Associated Proteins / metabolism*
  • Nucleocytoplasmic Transport Proteins / chemistry*
  • Nucleocytoplasmic Transport Proteins / genetics
  • Nucleocytoplasmic Transport Proteins / metabolism*
  • Protein Stability
  • Survival Analysis
  • Tissue Array Analysis
  • Tumor Escape
  • p300-CBP Transcription Factors / metabolism

Substances

  • GPI-Linked Proteins
  • Intracellular Signaling Peptides and Proteins
  • KLRK1 protein, human
  • NK Cell Lectin-Like Receptor Subfamily K
  • Nuclear Matrix-Associated Proteins
  • Nucleocytoplasmic Transport Proteins
  • RAE1 protein, human
  • ULBP1 protein, human
  • p300-CBP Transcription Factors
  • p300-CBP-associated factor
  • Lysine