Retinoic acid enhances TRAIL-induced apoptosis in cancer cells by upregulating TRAIL receptor 1 expression

Cancer Res. 2011 Aug 1;71(15):5245-54. doi: 10.1158/0008-5472.CAN-10-4180. Epub 2011 Jun 17.

Abstract

Many human cancer cells are sensitive to killing by the proapoptotic ligand TNF-related apoptosis-inducing ligand (TRAIL), which is under study for cancer treatment in clinical trials. The TRAIL receptor (TRAIL-R1; also known as death receptor 4) is a transmembrane receptor that mediates TRAIL-induced apoptosis in cancer cells. In this study, we show that retinoids sensitize cancer cells to TRAIL-induced apoptosis by upregulating expression of TRAIL-R1. All-trans retinoic acid (ATRA) upregulated TRAIL-R1 expression in human cancer cells at the transcriptional level. The ability of ATRA to activate TRAIL-R1 expression was inhibited by retinoic acid receptor (RAR) antagonists or siRNAs, but augmented by several RAR agonists. In analyzing how ATRA induces RAR-dependent transcriptional upregulation of TRAIL-R1, we identified 2 putative retinoic acid response elements termed Pal-17 (a palindrome separated by 17 bases) and DR-11 (a direct repeat separated by 11 bases) in the 5'-flanking region of TRAIL-R1 gene. Deletion of DR-11, but not Pal-17, abrogated the ability of ATRA to stimulate TRAIL-R1 promoter activity. Consistent with this observation, RAR binding to DR-11, but not to Pal-17, was detected by chromatin immunoprecipitation assay in ATRA-treated cells, arguing that DR-11 was responsible for ATRA-mediated activation of the TRAIL-R1 gene. ATRA augmented TRAIL-induced apoptosis of cancer cells, and this activity was attenuated by a blockade to upregulation of TRAIL-R1 expression. Taken together, our findings establish that ATRA accentuates TRAIL-induced apoptosis, reveal a novel mechanism by which retinoids modulate apoptosis, and suggest a novel strategy to augment the anti-cancer activity of TRAIL.

Publication types

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

MeSH terms

  • 5' Flanking Region / genetics
  • Apoptosis / drug effects*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Carcinoma, Squamous Cell / pathology
  • Cell Line, Tumor / cytology
  • Cell Line, Tumor / drug effects
  • Chromatin Immunoprecipitation
  • Gene Expression Regulation, Neoplastic / drug effects
  • Head and Neck Neoplasms / pathology
  • Humans
  • Lung Neoplasms / pathology
  • RNA, Small Interfering / pharmacology
  • Receptors, Retinoic Acid / drug effects
  • Receptors, Retinoic Acid / genetics
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / agonists*
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / biosynthesis
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / genetics
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / genetics
  • Recombinant Proteins / pharmacology
  • Response Elements / drug effects
  • Response Elements / genetics
  • TNF-Related Apoptosis-Inducing Ligand / pharmacology*
  • Transcriptional Activation / drug effects

Substances

  • RNA, Small Interfering
  • Receptors, Retinoic Acid
  • Receptors, TNF-Related Apoptosis-Inducing Ligand
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFRSF10A protein, human
  • TNFSF10 protein, human