Ribosomal Biogenesis and Translational Flux Inhibition by the Selective Inhibitor of Nuclear Export (SINE) XPO1 Antagonist KPT-185

PLoS One. 2015 Sep 4;10(9):e0137210. doi: 10.1371/journal.pone.0137210. eCollection 2015.

Abstract

Mantle cell lymphoma (MCL) is an aggressive B-cell lymphoma characterized by the aberrant expression of several growth-regulating, oncogenic effectors. Exportin 1 (XPO1) mediates the nucleocytoplasmic transport of numerous molecules including oncogenic growth-regulating factors, RNAs, and ribosomal subunits. In MCL cells, the small molecule KPT-185 blocks XPO1 function and exerts anti-proliferative effects. In this study, we investigated the molecular mechanisms of this putative anti-tumor effect on MCL cells using cell growth/viability assays, immunoblotting, gene expression analysis, and absolute quantification proteomics. KPT-185 exhibited a p53-independent anti-lymphoma effect on MCL cells, by suppression of oncogenic mediators (e.g., XPO1, cyclin D1, c-Myc, PIM1, and Bcl-2 family members), repression of ribosomal biogenesis, and downregulation of translation/chaperone proteins (e.g., PIM2, EEF1A1, EEF2, and HSP70) that are part of the translational/transcriptional network regulated by heat shock factor 1. These results elucidate a novel mechanism in which ribosomal biogenesis appears to be a key component through which XPO1 contributes to tumor cell survival. Thus, we propose that the blockade of XPO1 could be a promising, novel strategy for the treatment of MCL and other malignancies overexpressing XPO1.

Publication types

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

MeSH terms

  • Acrylates / pharmacology*
  • Active Transport, Cell Nucleus / drug effects
  • Antineoplastic Agents / pharmacology*
  • B-Lymphocytes / drug effects*
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • Cell Line, Tumor
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Elongation Factor 2 Kinase / genetics
  • Elongation Factor 2 Kinase / metabolism
  • Exportin 1 Protein
  • Gene Expression Regulation, Neoplastic*
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / metabolism
  • Heat Shock Transcription Factors
  • Humans
  • Karyopherins / antagonists & inhibitors*
  • Karyopherins / genetics
  • Karyopherins / metabolism
  • Organelle Biogenesis
  • Peptide Elongation Factor 1 / genetics
  • Peptide Elongation Factor 1 / metabolism
  • Protein Biosynthesis / drug effects
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • Proto-Oncogene Proteins c-pim-1 / genetics
  • Proto-Oncogene Proteins c-pim-1 / metabolism
  • Receptors, Cytoplasmic and Nuclear / antagonists & inhibitors*
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Ribosomes / drug effects*
  • Ribosomes / metabolism
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic / drug effects
  • Triazoles / pharmacology*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Acrylates
  • Antineoplastic Agents
  • DNA-Binding Proteins
  • EEF1A1 protein, human
  • HSP70 Heat-Shock Proteins
  • Heat Shock Transcription Factors
  • KPT-185
  • Karyopherins
  • PIM2 protein, human
  • Peptide Elongation Factor 1
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Proto-Oncogene Proteins c-myc
  • Receptors, Cytoplasmic and Nuclear
  • Transcription Factors
  • Triazoles
  • Tumor Suppressor Protein p53
  • Cyclin D1
  • EEF2K protein, human
  • PIM1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-pim-1
  • Elongation Factor 2 Kinase

Associated data

  • GEO/GSE70479