mTOR inhibitors induce apoptosis in colon cancer cells via CHOP-dependent DR5 induction on 4E-BP1 dephosphorylation

Oncogene. 2016 Jan 14;35(2):148-57. doi: 10.1038/onc.2015.79. Epub 2015 Apr 13.

Abstract

The mammalian target of rapamycin (mTOR) is commonly activated in colon cancer. mTOR complex 1 (mTORC1) is a major downstream target of the PI3K/ATK pathway and activates protein synthesis by phosphorylating key regulators of messenger RNA translation and ribosome synthesis. Rapamycin analogs Everolimus and Temsirolimus are non-ATP-competitive mTORC1 inhibitors, and suppress proliferation and tumor angiogenesis and invasion. We now show that apoptosis plays a key role in their anti-tumor activities in colon cancer cells and xenografts through the DR5, FADD and caspase-8 axis, and is strongly enhanced by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and 5-fluorouracil. The induction of DR5 by rapalogs is mediated by the ER stress regulator and transcription factor CHOP, but not the tumor suppressor p53, on rapid and sustained inhibition of 4E-BP1 phosphorylation, and attenuated by eIF4E expression. ATP-competitive mTOR/PI3K inhibitors also promote DR5 induction and FADD-dependent apoptosis in colon cancer cells. These results establish activation of ER stress and the death receptor pathway as a novel anticancer mechanism of mTOR inhibitors.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Cell Cycle Proteins
  • Cell Line, Tumor / drug effects
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Everolimus / pharmacology
  • Female
  • Humans
  • Mice, Nude
  • Phosphoproteins / metabolism*
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology*
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / metabolism
  • Sirolimus / analogs & derivatives
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases / antagonists & inhibitors*
  • TOR Serine-Threonine Kinases / metabolism
  • Transcription Factor CHOP / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents
  • Cell Cycle Proteins
  • DDIT3 protein, human
  • EIF4EBP1 protein, human
  • Phosphoproteins
  • Protein Kinase Inhibitors
  • Receptors, TNF-Related Apoptosis-Inducing Ligand
  • Transcription Factor CHOP
  • temsirolimus
  • Everolimus
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • Sirolimus