Activation of ATF4 mediates unwanted Mcl-1 accumulation by proteasome inhibition

Blood. 2012 Jan 19;119(3):826-37. doi: 10.1182/blood-2011-07-366492. Epub 2011 Nov 29.

Abstract

Myeloid cell leukemia-1 (Mcl-1) protein is an anti-apoptotic Bcl-2 family protein that plays essential roles in multiple myeloma (MM) survival and drug resistance. In MM, it has been demonstrated that proteasome inhibition can trigger the accumulation of Mcl-1, which has been shown to confer MM cell resistance to bortezomib-induced lethality. However, the mechanisms involved in this unwanted Mcl-1 accumulation are still unclear. The aim of the present study was to determine whether the unwanted Mcl-1 accumulation could be induced by the unfolded protein response (UPR) and to elucidate the role of the endoplasmic reticulum stress response in regulating Mcl-1 expression. Using quantitative RT-PCR and Western blot, we found that the translation of activating transcription factor-4 (ATF4), an important effector of the UPR, was also greatly enhanced by proteasome inhibition. ChIP analysis further revealed that bortezomib stimulated binding of ATF4 to a regulatory site (at position -332 to -324) at the promoter of the Mcl-1 gene. Knocking down ATF4 was paralleled by down-regulation of Mcl-1 induction by bortezomib and significantly increased bortezomib-induced apoptosis. These data identify the UPR and, more specifically, its ATF4 branch as an important mechanism mediating up-regulation of Mcl-1 by proteasome inhibition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 4 / genetics
  • Activating Transcription Factor 4 / metabolism*
  • Antineoplastic Agents / pharmacology
  • Apoptosis
  • Blotting, Western
  • Boronic Acids / pharmacology
  • Bortezomib
  • Cell Line, Tumor
  • Cell Proliferation
  • Chromatin Immunoprecipitation
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum Stress / drug effects
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Multiple Myeloma / drug therapy
  • Multiple Myeloma / metabolism*
  • Multiple Myeloma / pathology
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Proto-Oncogene Proteins c-bcl-2 / genetics*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • Pyrazines / pharmacology
  • RNA Splicing
  • RNA, Messenger / genetics
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Regulatory Factor X Transcription Factors
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Unfolded Protein Response / drug effects
  • Unfolded Protein Response / physiology*

Substances

  • ATF4 protein, human
  • Antineoplastic Agents
  • Boronic Acids
  • DNA-Binding Proteins
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Proto-Oncogene Proteins c-bcl-2
  • Pyrazines
  • RNA, Messenger
  • RNA, Small Interfering
  • Regulatory Factor X Transcription Factors
  • Transcription Factors
  • Activating Transcription Factor 4
  • Bortezomib