KCTD17-mediated Ras stabilization promotes hepatocellular carcinoma progression

Clin Mol Hepatol. 2024 Oct;30(4):895-913. doi: 10.3350/cmh.2024.0364. Epub 2024 Aug 5.

Abstract

Background/aims: Potassium channel tetramerization domain containing 17 (KCTD17) protein, an adaptor for the cullin3 (Cul3) ubiquitin ligase complex, has been implicated in various human diseases; however, its role in hepatocellular carcinoma (HCC) remains elusive. Here, we aimed to elucidate the clinical features of KCTD17, and investigate the mechanisms by which KCTD17 affects HCC progression.

Methods: We analyzed transcriptomic data from patients with HCC. Hepatocyte-specific KCTD17 deficient mice were treated with diethylnitrosamine (DEN) to assess its effect on HCC progression. Additionally, we tested KCTD17-directed antisense oligonucleotides for their therapeutic potential in vivo.

Results: Our investigation revealed the upregulation of KCTD17 expression in both tumors from patients with HCC and mouse models of HCC, in comparison to non-tumor controls. We identified the leucine zipper-like transcriptional regulator 1 (Lztr1) protein, a previously identified Ras destabilizer, as a substrate for KCTD17-Cul3 complex. KCTD17-mediated Lztr1 degradation led to Ras stabilization, resulting in increased proliferation, migration, and wound healing in liver cancer cells. Hepatocyte-specific KCTD17 deficient mice or liver cancer xenograft models were less susceptible to carcinogenesis or tumor growth. Similarly, treatment with KCTD17-directed antisense oligonucleotides (ASO) in a mouse model of HCC markedly lowered tumor volume as well as Ras protein levels, compared to those in control ASO-treated mice.

Conclusion: KCTD17 induces the stabilization of Ras and downstream signaling pathways and HCC progression and may represent a novel therapeutic target for HCC.

Keywords: Antisense oligonucleotides; HCC; KCTD17; Lztr1; Ras.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • Cell Proliferation
  • Cullin Proteins / genetics
  • Cullin Proteins / metabolism
  • Diethylnitrosamine / toxicity
  • Disease Progression*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Male
  • Mice
  • Oligonucleotides, Antisense / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • ras Proteins / genetics
  • ras Proteins / metabolism

Substances

  • Cullin Proteins
  • ras Proteins
  • Transcription Factors
  • CUL3 protein, human
  • Diethylnitrosamine
  • Oligonucleotides, Antisense