IGF-1 suppresses Bim expression in multiple myeloma via epigenetic and posttranslational mechanisms

Blood. 2010 Mar 25;115(12):2430-40. doi: 10.1182/blood-2009-07-232801. Epub 2010 Jan 19.

Abstract

Insulin-like growth factor-1 (IGF-1) is an important growth and survival factor in multiple myeloma (MM). Here, we demonstrate that IGF-1 induces significant down-regulation of the proapoptotic BH3-only protein Bim in MM cells. Reduced Bim levels by RNA interference (RNAi) protected cells from drug-induced cell death. The IGF-1-mediated down-regulation of Bim was the result of (1) reduced transcription by activation of the Akt pathway and inactivation of the transcription factor FoxO3a, (2) increased proteasome-mediated degradation of the Bim extra-long protein by activation of the mitogen-activated protein kinase pathway, and (3) epigenetic regulation of both the Bim and the FoxO3a promoter. Treatment of cells with the histone deacetylase inhibitor LBH589 resulted in a clear up-regulation in the expression of Bim. Furthermore, the methylation inhibitor 5-aza-2'deoxycytidine (decitabine) significantly increased the effects of LBH589. On IGF-1 treatment, the Bim promoter region was found to be unmethylated, whereas chromatin immunoprecipitation analysis of the IGF-1-treated cells showed both a reduced histone H3 tail Lys9 (H3K9) acetylation and an increased H3K9 dimethylation, which contributed actively to its silencing. These data identify a new mechanism in the IGF-1-dependent survival of MM cells and emphasize the need for IGF-1-targeted drug therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • Apoptosis Regulatory Proteins / genetics*
  • Bcl-2-Like Protein 11
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / physiology
  • Down-Regulation / physiology
  • Epigenesis, Genetic / physiology*
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / physiology*
  • Gene Silencing
  • Histones / metabolism
  • Humans
  • Hydroxamic Acids / pharmacology
  • Immunoglobulin G / pharmacology
  • Indoles
  • Insulin-Like Growth Factor I / metabolism*
  • Insulin-Like Growth Factor I / pharmacology
  • Kidney / cytology
  • Melphalan / pharmacology
  • Membrane Proteins / genetics*
  • Mice
  • Mice, Inbred C57BL
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Multiple Myeloma / genetics*
  • Multiple Myeloma / pathology
  • Panobinostat
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Processing, Post-Translational
  • Proto-Oncogene Proteins / genetics*

Substances

  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • FOXO3 protein, human
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors
  • Histones
  • Hydroxamic Acids
  • Immunoglobulin G
  • Indoles
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • antineoplastic agent K 18
  • Insulin-Like Growth Factor I
  • Panobinostat
  • Phosphatidylinositol 3-Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Melphalan