miR-92a-3p and MYCBP2 are involved in MS-275-induced and c-myc-mediated TRAIL-sensitivity in melanoma cells

Int Immunopharmacol. 2016 Nov:40:235-243. doi: 10.1016/j.intimp.2016.09.004. Epub 2016 Sep 10.

Abstract

Increasing evidence has demonstrated that in several tumors c-myc acts either as an oncogène or as a proapoptotic agent, depending on binding partner interactions. Recently, we showed that up-regulation of this gene by the histone deacetylase inhibitor MS-275 was responsible for sensitization to TRAIL-induced apoptosis through c-FLIP repression in melanoma. The present study aimed at investigating whether, in addition to inducing H3 hyperacetylation at the c-myc promoter, MS-275 could enhance cell death through the regulation of miRNAs involved in apoptosis, such as the miR-17-92 cluster. Following MS-275 treatment, a decrease in miR-92a-3p was observed either in TRAIL-resistant or TRAIL-sensitive cutaneous and uveal melanoma cells. Prediction tools revealed that miR-92a-3p targeted MYCBP2. Gain- and loss-of-function experiments showed that the 3'-UTR of MYCBP2 mRNA was the target of miR-92a-3p, as ectopic expression of miR-92a-3p resulted in MYCBP2 downregulation whereas miR-92a-3p knockdown markedly increased the expression of MYCBP2. Silencing of MYCBP2 counteracted the pro-apoptotic effects exerted by the down-regulation of miR-92a-3p and prevented c-myc-induced repression of c-FLIP, indicating a pivotal role of MYCBP2 as a mediator of miR-92a-3p and c-myc function. Together, our findings indicate that the MS-275-triggered downregulation of the oncogenic miR-92a-3p- which leads to the overexpression of its target gene MYCBP2 - is an event required for the enhanced susceptibility of melanoma cells to TRAIL-mediated apoptosis. Our data illustrate another epigenetic mechanism activated by MS-275 at the post-transcriptional level in melanoma, in addition to its best-known effects at the transcriptional level.

Keywords: Apoptosis; MS-275; MYCBP2; Melanoma; miR-92a-3p.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Aged
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Benzamides / pharmacology*
  • CASP8 and FADD-Like Apoptosis Regulating Protein / genetics
  • Cell Line, Tumor
  • Female
  • Humans
  • Male
  • Melanoma / metabolism
  • MicroRNAs / metabolism*
  • Middle Aged
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Pyridines / pharmacology*
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents
  • Benzamides
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • MIRN92 microRNA, human
  • MYC protein, human
  • MicroRNAs
  • Proto-Oncogene Proteins c-myc
  • Pyridines
  • RNA, Messenger
  • RNA, Small Interfering
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFSF10 protein, human
  • entinostat
  • MYCBP2 protein, human
  • Ubiquitin-Protein Ligases