Circ-RAPGEF5 promotes intrahepatic cholangiocarcinoma progression by stabilizing SAE1 to facilitate SUMOylation

J Exp Clin Cancer Res. 2023 Sep 13;42(1):239. doi: 10.1186/s13046-023-02813-y.

Abstract

Background: Intrahepatic cholangiocarcinoma (ICC) is an aggressive malignancy with a poor prognosis. The underlying functions and mechanisms of circular RNA and SUMOylation in the development of ICC remain poorly understood.

Methods: Circular RNA hsa_circ_0001681 (termed Circ-RAPGEF5 hereafter) was identified by circular RNA sequencing from 19 pairs of ICC and adjacent tissue samples. The biological function of Circ-RAPGEF5 in tumor proliferation and metastasis was examined by a series of in vitro assays. A preclinical model was used to validate the therapeutic effect of targeting Circ-RAPGEF5. RNA pull-down and dual-luciferase reporter assays were used to access the RNA interactions. Western blot and Co-IP assays were used to detect SUMOylation levels.

Results: Circ-RAPGEF5, which is generated from exons 2 to 6 of the host gene RAPGEF5, was upregulated in ICC. In vitro and in vivo assays showed that Circ-RAPGEF5 promoted ICC tumor proliferation and metastasis, and inhibited apoptosis. Additionally, high Circ-RAPGEF5 expression was significantly correlated with a poor prognosis. Further investigation showed that SAE1, a potential target of Circ-RAPGEF5, was also associated with poor oncological outcomes. RNA pull-down and dual-luciferase reporter assays showed an interaction of miR-3185 with Circ-RAPGEF5 and SAE1. Co-IP and western blot assays showed that Circ-RAPGEF5 is capable of regulating SUMOylation.

Conclusion: Circ-RAPGEF5 promotes ICC tumor progression and SUMOylation by acting as a sponge for miR-3185 to stabilize SAE1. Targeting Circ-RAPGEF5 or SAE1 might be a novel diagnostic and therapeutic strategy in ICC.

Keywords: AKT; Circ-RAPGEF5; Intrahepatic cholangiocarcinoma; SAE1; SUMOylation.

MeSH terms

  • Bile Duct Neoplasms* / genetics
  • Bile Ducts, Intrahepatic
  • Cholangiocarcinoma* / genetics
  • Humans
  • MicroRNAs*
  • RNA, Circular / genetics
  • Sumoylation
  • Ubiquitin-Activating Enzymes
  • ras Guanine Nucleotide Exchange Factors

Substances

  • RNA, Circular
  • MicroRNAs
  • RAPGEF5 protein, human
  • ras Guanine Nucleotide Exchange Factors
  • SAE1 protein, human
  • Ubiquitin-Activating Enzymes