Induction of the transcriptional repressor ZBTB4 in prostate cancer cells by drug-induced targeting of microRNA-17-92/106b-25 clusters

Mol Cancer Ther. 2012 Sep;11(9):1852-62. doi: 10.1158/1535-7163.MCT-12-0181. Epub 2012 Jun 29.

Abstract

Androgen-insensitive DU145 and PC3 human prostate cancer cells express high levels of specificity protein (Sp) transcription factors Sp1, Sp3, and Sp4, and treatment of cells with methyl 2-cyano-3,11-dioxo-18β-olean-1,12-dien-30-oate (CDODA-Me) inhibited cell growth and downregulated Sp1, Sp3, and Sp4 expression. CDODA-Me (15 mg/kg/d) was a potent inhibitor of tumor growth in a mouse xenograft model (PC3 cells) and also decreased expression of Sp transcription factors in tumors. CDODA-Me-mediated downregulation of Sp1, Sp3, and Sp4 was due to induction of the transcriptional repressor ZBTB4, which competitively binds and displaces Sp transcription factors from GC-rich sites in Sp1-, Sp3-, Sp4-, and Sp-regulated gene promoters. ZBTB4 levels are relatively low in DU145 and PC3 cells due to suppression by miR paralogs that are members of the miR-17-92 (miR-20a/17-5p) and miR-106b-25 (miR-106b/93) clusters. Examination of publically available prostate cancer patient array data showed an inverse relationship between ZBTB4 and miRs-20a/17-5p/106b/93 expression, and increased ZBTB4 in patients with prostate cancer was a prognostic factor for increased survival. CDODA-Me induces ZBTB4 in prostate cancer cells through disruption of miR-ZBTB4 interactions, and this results in downregulation of pro-oncogenic Sp transcription factors and Sp-regulated genes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genes, Reporter
  • Glycyrrhetinic Acid / analogs & derivatives*
  • Glycyrrhetinic Acid / pharmacology
  • Glycyrrhetinic Acid / therapeutic use
  • Humans
  • Luciferases / biosynthesis
  • Luciferases / genetics
  • Male
  • Mice
  • Mice, Nude
  • MicroRNAs / genetics
  • Multigene Family*
  • Promoter Regions, Genetic
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / metabolism*
  • Prostatic Neoplasms / pathology
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Sp Transcription Factors / genetics
  • Sp Transcription Factors / metabolism
  • Transcriptional Activation*
  • Tumor Burden / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • MIRN106 microRNA, human
  • MIRN17 microRNA, human
  • MIRN25 microRNA, human
  • MIRN92 microRNA, human
  • MicroRNAs
  • Repressor Proteins
  • Sp Transcription Factors
  • ZBTB4 protein, human
  • methyl 2-cyano-3,11-dioxo-18beta-olean-1,12-dien-30-oate
  • Luciferases
  • Glycyrrhetinic Acid