Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells

Blood. 2006 Jun 15;107(12):4907-16. doi: 10.1182/blood-2005-08-3531. Epub 2006 Feb 28.

Abstract

Multiple myeloma (MM) is an incurable plasma cell malignancy. The 26S proteasome inhibitor, bortezomib, selectively induces apoptosis in MM cells; however, the nature of its selectivity remains unknown. Here we demonstrate that 5 different MM cell lines display similar patterns of sensitivity to 3 proteasome inhibitors (PIs) but respond differently to specific NF-kappaB inhibition. We further show that PIs initiate the unfolded protein response (UPR), a signaling pathway activated by the accumulation of misfolded proteins within the endoplasmic reticulum (ER). Consistent with reports that prosurvival/physiologic UPR components are required for B-cell differentiation into antibody-secreting cells, we found that MM cells inherently expressed the ER chaperones GRP78/Bip and GRP94/gp96. However, bortezomib rapidly induced components of the proapoptotic/terminal UPR, including PERK, the ER stress-specific eIF-2alpha kinase; ATF4, an ER stress-induced transcription factor; and its proapoptotic target, CHOP/GADD153. Consistent with our hypothesis that PIs induce the accumulation of misfolded ER-processed proteins, we found that the amount of immunoglobulin subunits retained within MM cells correlated with their sensitivity to PIs. These findings suggest that MM cells have a lower threshold for PI-induced UPR induction and ER stress-induced apoptosis because they constitutively express ER stress survival factors to function as secretory cells.

Publication types

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

MeSH terms

  • Apoptosis / drug effects
  • Boronic Acids / pharmacology*
  • Boronic Acids / therapeutic use
  • Bortezomib
  • Cell Differentiation / drug effects
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Endoplasmic Reticulum / enzymology
  • Endoplasmic Reticulum Chaperone BiP
  • Humans
  • Multiple Myeloma / drug therapy
  • Multiple Myeloma / enzymology*
  • Neoplasm Proteins / biosynthesis
  • Plasma Cells / enzymology
  • Plasma Cells / pathology
  • Protease Inhibitors / pharmacology*
  • Protease Inhibitors / therapeutic use
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteasome Inhibitors
  • Protein Folding*
  • Pyrazines / pharmacology*
  • Pyrazines / therapeutic use
  • Signal Transduction / drug effects*

Substances

  • Boronic Acids
  • Endoplasmic Reticulum Chaperone BiP
  • HSPA5 protein, human
  • Neoplasm Proteins
  • Protease Inhibitors
  • Proteasome Inhibitors
  • Pyrazines
  • Bortezomib
  • Proteasome Endopeptidase Complex
  • ATP dependent 26S protease