Syntaxin-6 mediated autophagy confers lenvatinib resistance in hepatocellular carcinoma

Oncogene. 2025 Jul;44(25):2025-2039. doi: 10.1038/s41388-025-03371-7. Epub 2025 Apr 3.

Abstract

Lenvatinib is the first-line therapy for inoperable HCC. However, intrinsic and acquired drug resistance occurs during the treatment period. Autophagy is an adaptive response that favors tumor survival under stress. In the present study, we aim to reveal the unknown autophagic engagement in lenvatinib resistance. Lenvatinib-resistant HCC cell lines and xenograft mouse HCC models were established to identify the key regulator of lenvatinib resistance in HCC. By in vitro functional restoration assays and autophagic flux detection, we demonstrated that the Syntaxin-6 (STX6) -mediated autophagy induced lenvatinib resistance of HCC cells. Mechanistically, Co-immunoprecipitation assay and mass spectrometry indicated that the interactions of STX6 with Beclin1, VTI1A, and VAMP3 facilitated autophagy, leading to the lenvatinib resistance. Additionally, STX6 enhanced the ability of proliferation, migration, and invasion of HCC in vitro and in vivo. Clinically, STX6 expression was significantly elevated in HCC tissues compared to it in para-tumor tissues. High STX6 expression predicted poor outcomes for patients following resection. Moreover, high expression of STX6 displayed low preventive efficacy of lenvatinib as a postoperative adjuvant treatment for HCC patients with a high risk of recurrence. Collectively, we identified that STX6-mediated autophagy plays a crucial role in lenvatinib resistance in HCC, providing a potential therapeutic target to overcome lenvatinib resistance for HCC patients.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Autophagy* / drug effects
  • Carcinoma, Hepatocellular* / drug therapy
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Female
  • Humans
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Male
  • Mice
  • Mice, Nude
  • Phenylurea Compounds* / pharmacology
  • Phenylurea Compounds* / therapeutic use
  • Qa-SNARE Proteins* / genetics
  • Qa-SNARE Proteins* / metabolism
  • Quinolines* / pharmacology
  • Quinolines* / therapeutic use
  • Xenograft Model Antitumor Assays

Substances

  • lenvatinib
  • Quinolines
  • Phenylurea Compounds
  • Qa-SNARE Proteins
  • Antineoplastic Agents