TRIM65/NF2/YAP1 Signaling Coordinately Orchestrates Metabolic and Immune Advantages in Hepatocellular Carcinoma

Adv Sci (Weinh). 2024 Sep;11(35):e2402578. doi: 10.1002/advs.202402578. Epub 2024 Jul 15.

Abstract

Hepatocellular carcinoma (HCC) is one of the leading causes of cancer deaths worldwide. Significantly activated uridine nucleotide and fatty acid metabolism in HCC cells promote malignant proliferation and immune evasion. Herein, it is demonstrated that the tripartite motif 65 (TRIM65) E3 ubiquitin-protein ligase, O-GlcNAcylated via O-GlcNAcylation transferase, is highly expressed in HCC and facilitated metabolic remodeling to promote the accumulation of products related to uracil metabolism and palmitic acid, driving the progression of HCC. Mechanistically, it is showed that TRIM65 mediates ubiquitylation at the K44 residue of neurofibromatosis type 2 (NF2), the key protein upstream of classical Hippo signaling. Accelerated NF2 degradation inhibits yes-associated protein 1 phosphorylation, inducing aberrant activation of related metabolic enzyme transcription, and orchestrating metabolic and immune advantages. In conclusion, these results reveal a critical role for the TRIM family molecule TRIM65 in supporting HCC cell survival and highlight the therapeutic potential of targeting its E3 ligase activity to alter the regulation of proteasomal degradation.

Keywords: TRIM65; hepatocellular carcinoma; immune evasion; palmitic acid; uracil metabolism.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / metabolism
  • Cell Line, Tumor
  • Disease Models, Animal
  • Humans
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Signal Transduction* / genetics
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Tripartite Motif Proteins* / genetics
  • Tripartite Motif Proteins* / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism
  • YAP-Signaling Proteins* / genetics
  • YAP-Signaling Proteins* / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Transcription Factors
  • TRIM65 protein, human
  • Tripartite Motif Proteins
  • Ubiquitin-Protein Ligases
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • NF2 protein, human