O-GlcNAc transferase promotes immune evasion and immunotherapy resistance in uterine corpus endometrial cancer by targeting the glucocorticoid receptor

J Immunother Cancer. 2025 Oct 5;13(10):e011479. doi: 10.1136/jitc-2025-011479.

Abstract

Background: Although some tumors respond to immune checkpoint blockade therapy, checkpoint inhibitors have been unsuccessful in treating uterine corpus endometrial cancer (UCEC), and the underlying molecular mechanisms remain unclear.

Methods: We investigated glucose flux regulation in UCEC cells with a focus on the hexosamine biosynthesis pathway (HBP). The role of O-linked N-acetylglucosamine (O-GlcNAc) transferase (OGT) and its interaction with the glucocorticoid receptor (GR) were examined using in vitro and in vivo models. A competitive peptide was designed to disrupt the interaction between OGT and GR.

Results: We found that UCEC cells direct glucose flux to the HBP. OGT, a critical enzyme for protein O-GlcNAcylation, increased programmed death ligand-1 (PD-L1) expression while decreasing major histocompatibility complex class I (MHC-I) expression, thereby promoting immune evasion and resistance to immunotherapy. Mechanistically, OGT interacted with GR, leading to O-GlcNAcylation of GR at serine 132, which required prior phosphorylation of GR. Disruptions of the OGT-GR interaction with the competitive peptide reduced GR O-GlcNAcylation, decreased PD-L1 expression, and increased MHC-I expression. This, in turn, activated CD8+ T cell-mediated immunity against tumor cells in vitro and in vivo.

Conclusions: Our findings reveal cross-talk between the HBP, steroid hormone pathway, and tumor immune evasion, and suggest potential strategies for sensitizing UCEC to immunotherapy.

Keywords: Immune Checkpoint Inhibitor; Immune modulatory; Immunotherapy; T cell; Tumor infiltrating lymphocyte - TIL.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm*
  • Endometrial Neoplasms* / drug therapy
  • Endometrial Neoplasms* / immunology
  • Endometrial Neoplasms* / metabolism
  • Endometrial Neoplasms* / pathology
  • Female
  • Humans
  • Immune Evasion*
  • Immunotherapy* / methods
  • Mice
  • N-Acetylglucosaminyltransferases* / metabolism
  • Receptors, Glucocorticoid* / metabolism

Substances

  • N-Acetylglucosaminyltransferases
  • Receptors, Glucocorticoid
  • O-GlcNAc transferase
  • OGT protein, human