TGF-β1 facilitates gallbladder carcinoma metastasis by regulating FOXA1 translation efficiency through m6A modification

Cell Death Dis. 2024 Jun 17;15(6):422. doi: 10.1038/s41419-024-06800-9.

Abstract

TGF-β1 plays a pivotal role in the metastatic cascade of malignant neoplasms. N6-methyladenosine (m6A) stands as one of the most abundant modifications on the mRNA transcriptome. However, in the metastasis of gallbladder carcinoma (GBC), the effect of TGF-β1 with mRNA m6A modification, especially the effect of mRNA translation efficiency associated with m6A modification, remains poorly elucidated. Here we demonstrated a negative correlation between FOXA1 and TGF-β1 expression in GBC. Overexpression of FOXA1 inhibited TGF-β1-induced migration and epithelial-mesenchymal transition (EMT) in GBC cells. Mechanistically, we confirmed that TGF-β1 suppressed the translation efficiency of FOXA1 mRNA through polysome profiling analysis. Importantly, both in vivo and in vitro experiments showed that TGF-β1 promoted m6A modification on the coding sequence (CDS) region of FOXA1 mRNA, which was responsible for the inhibition of FOXA1 mRNA translation by TGF-β1. We demonstrated through MeRIP and RIP assays, dual-luciferase reporter assays and site-directed mutagenesis that ALKBH5 promoted FOXA1 protein expression by inhibiting m6A modification on the CDS region of FOXA1 mRNA. Moreover, TGF-β1 inhibited the binding capacity of ALKBH5 to the FOXA1 CDS region. Lastly, our study confirmed that overexpression of FOXA1 suppressed lung metastasis and EMT in a nude mice lung metastasis model. In summary, our research findings underscore the role of TGF-β1 in regulating TGF-β1/FOXA1-induced GBC EMT and metastasis by inhibiting FOXA1 translation efficiency through m6A modification.

MeSH terms

  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • Animals
  • Cell Line, Tumor
  • Cell Movement
  • Epithelial-Mesenchymal Transition* / genetics
  • Gallbladder Neoplasms* / genetics
  • Gallbladder Neoplasms* / metabolism
  • Gallbladder Neoplasms* / pathology
  • Gene Expression Regulation, Neoplastic
  • Hepatocyte Nuclear Factor 3-alpha* / genetics
  • Hepatocyte Nuclear Factor 3-alpha* / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude*
  • Neoplasm Metastasis
  • Protein Biosynthesis*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transforming Growth Factor beta1* / metabolism

Substances

  • Hepatocyte Nuclear Factor 3-alpha
  • Transforming Growth Factor beta1
  • FOXA1 protein, human
  • Adenosine
  • N-methyladenosine
  • TGFB1 protein, human
  • RNA, Messenger