PBLD inhibits angiogenesis via impeding VEGF/VEGFR2-mediated microenvironmental cross-talk between HCC cells and endothelial cells

Oncogene. 2022 Mar;41(13):1851-1865. doi: 10.1038/s41388-022-02197-x. Epub 2022 Feb 10.

Abstract

Sustained anti-angiogenesis therapy increases the level of tumor hypoxia, leading to increased expression of HIF-1a, thereby contributing to the resistance to anti-angiogenesis therapy in hepatocellular carcinoma (HCC). Here, we report that phenazine biosynthesis-like domain-containing protein (PBLD) inhibits hypoxia-induced angiogenesis via ERK/HIF-1a/VEGF axis in HCC cells. Bioinformatic analysis of the TCGA database and clinical samples validation also identify a negative correlation between PBLD and angiogenesis-related genes expression including HIF-1a. Apart from the downregulation of HIF-1a/VEGF expression in HCC cells, PBLD also blocks VEGF receptor 2 (VEGFR2) on endothelial cells via HCC-derived exosomal miR-940. PBLD also activates TCF4 transcriptional promotion effects on miR-940 by directly interacting with it. Together, PBLD exerts an inhibitory effect on angiogenesis not only via blocking the VEGFR2 expression in endothelial cells, but also through downregulating HIF-1a-induced VEGF expression and secretion in HCC cells. These explorations may provide a theoretical basis for exploring new targets and strategies to overcome resistance to anti-angiogenesis therapy.

MeSH terms

  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • Endothelial Cells / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Liver Neoplasms* / pathology
  • MicroRNAs* / genetics
  • MicroRNAs* / therapeutic use
  • Neovascularization, Pathologic / metabolism
  • Proteins
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism
  • Vascular Endothelial Growth Factor Receptor-2 / genetics
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism

Substances

  • Hypoxia-Inducible Factor 1, alpha Subunit
  • MicroRNAs
  • PBLD protein, human
  • Proteins
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factor Receptor-2