Human umbilical cord mesenchymal stem cell-derived extracellular vesicles carrying miR-655-3p inhibit the development of esophageal cancer by regulating the expression of HIF-1α via a LMO4/HDAC2-dependent mechanism

Cell Biol Toxicol. 2023 Aug;39(4):1319-1339. doi: 10.1007/s10565-022-09759-5. Epub 2022 Oct 12.

Abstract

Objective: This study clarified the function of human umbilical cord mesenchymal stem cell (hUCMSC)-derived extracellular vesicle (EV)-enclosed miR-655-3p in esophageal squamous cell carcinoma (ESCC).

Methods: A Chi-square test and the Kaplan-Meier estimator were used to analyze the prognosis of ESCC in relation to the expression of miR-655-3p. ESCC cells were incubated with PBS or hUCMSC-derived EVs (hUCMSC-EVs) in the conditions of gene modification, after which the malignant behaviors of ESCC cells were assessed and the molecular interactions were determined. The effect of hUCMSC-derived EV-miR-655-3p was also investigated in a nude mouse model of ESCC.

Results: Low expression of miR-655-3p indicated poor prognosis of ESCC. hUCMSC-EVs suppressed the malignant behaviors of ESCC cells and the growth and liver metastasis of transplanted tumors. Inhibition of miR-655-3p in hUCMSCs impaired the therapeutic effect of hUCMSC-EVs. LMO4, targeted by miR-655-3p, activated the transcription of HIF-1α by sequestering HDAC2 from HIF-1α promoter. Knockdown of LMO4 suppressed ESCC cell activities, while overexpression of HIF-1α counteracted the tumor suppressive effect of LMO4 knockdown.

Conclusion: miR-655-3p enclosed in hUCMSC-derived EVs inhibits ESCC progression partially by inactivating HIF-1α via the LMO4/HDAC2 axis.

Keywords: Esophageal cancer; Extracellular vesicle; HDAC2; HIF-1α; Human umbilical cord mesenchymal stem cell; LMO4; miR-655-3p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Cell Line, Tumor
  • Esophageal Neoplasms* / genetics
  • Esophageal Neoplasms* / metabolism
  • Esophageal Neoplasms* / pathology
  • Esophageal Squamous Cell Carcinoma* / genetics
  • Esophageal Squamous Cell Carcinoma* / metabolism
  • Esophageal Squamous Cell Carcinoma* / pathology
  • Extracellular Vesicles*
  • Histone Deacetylase 2 / genetics
  • Histone Deacetylase 2 / metabolism
  • Humans
  • LIM Domain Proteins / genetics
  • LIM Domain Proteins / metabolism
  • Mesenchymal Stem Cells* / metabolism
  • Mice
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Umbilical Cord

Substances

  • MicroRNAs
  • LMO4 protein, human
  • Adaptor Proteins, Signal Transducing
  • LIM Domain Proteins
  • HDAC2 protein, human
  • Histone Deacetylase 2
  • MIRN655 microRNA, human