Reprogramming using microRNA-302 improves drug sensitivity in hepatocellular carcinoma cells

Ann Surg Oncol. 2014 Dec:21 Suppl 4:S591-600. doi: 10.1245/s10434-014-3705-7. Epub 2014 Apr 18.

Abstract

Background: Although studies have shown that Oct4, Sox2, Klf4, and c-Myc (OKSM)-mediated induced pluripotent stem cell (iPSC) technology sensitizes cancer cells to drugs, the potential risk of inserting c-Myc and random insertions of exogenous sequences into the genome persists. Several authors, including us, have presented microRNA (miRNA)-mediated reprogramming as an alternative approach. Herein, we evaluated the efficacy of miRNA-mediated reprogramming on hepatocellular carcinoma (HCC) cells.

Methods: Among three miRNAs (miR-200c, miR-302s, and miR-369s) that were previously presented for miRNA-mediated reprogramming, miR-302 was expressed at low levels in HCC cells. After transfecting three times with miR-302, the cells were incubated in ES medium for 3 weeks and then characterized.

Results: iPSC-like spheres were obtained after the 3-week incubation. Spheres presented high NANOG and OCT4 expression, low proliferation, high apoptosis, low epithelial-mesenchymal transition marker expression (N-cadherin, TGFBR2), and sensitization to drugs. Several miRNAs were changed (e.g., low oncomiR miR-21, high miR-29b). cMyc was decreased, and methylation was elevated on histone 3 at lysine 4 (H3K4). Differentiated cells expressed markers of each germ layer (GFAP, FABP4, and ALB). AOF2 (also known as LSD1 or KDM1), one of the targets for miR-302, was repressed in iPSC-like-spheres. Silencing of AOF2 resulted in similar features of iPSC-like-spheres, including cMyc down-regulation and H3K4 methylation. In drug-resistant cells, sensitization was achieved through miR-302-mediated reprogramming.

Conclusions: miR-302-mediated iPSC technology reprogrammed HCC cells and improved drug sensitivity through AOF2 down-regulation, which caused H3K4 methylation and c-Myc repression.

MeSH terms

  • Apoptosis
  • Cadherins / metabolism
  • Carcinoma, Hepatocellular / drug therapy*
  • Carcinoma, Hepatocellular / genetics*
  • Cell Differentiation
  • Cell Proliferation
  • Down-Regulation
  • Drug Resistance, Neoplasm / genetics*
  • Epithelial-Mesenchymal Transition
  • Gene Silencing
  • Hep G2 Cells
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism*
  • Homeodomain Proteins / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism*
  • Kruppel-Like Factor 4
  • Liver Neoplasms / drug therapy*
  • Liver Neoplasms / genetics*
  • Methylation
  • MicroRNAs / genetics*
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3 / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins c-myc / metabolism
  • Receptor, Transforming Growth Factor-beta Type II
  • Receptors, Transforming Growth Factor beta / metabolism
  • Transfection

Substances

  • Cadherins
  • Homeodomain Proteins
  • KLF4 protein, human
  • Kruppel-Like Factor 4
  • MIRN302A microRNA, human
  • MYC protein, human
  • MicroRNAs
  • NANOG protein, human
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3
  • POU5F1 protein, human
  • Proto-Oncogene Proteins c-myc
  • Receptors, Transforming Growth Factor beta
  • Histone Demethylases
  • KDM1A protein, human
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type II