Protein kinase CK2 protects multiple myeloma cells from ER stress-induced apoptosis and from the cytotoxic effect of HSP90 inhibition through regulation of the unfolded protein response

Clin Cancer Res. 2012 Apr 1;18(7):1888-900. doi: 10.1158/1078-0432.CCR-11-1789. Epub 2012 Feb 20.

Abstract

Purpose: Protein kinase CK2 promotes multiple myeloma cell growth by regulating critical signaling pathways. CK2 also modulates proper HSP90-dependent client protein folding and maturation by phosphorylating its co-chaperone CDC37. Because the endoplasmic reticulum (ER) stress/unfolded protein response (UPR) is central in myeloma pathogenesis, we tested the hypothesis that the CK2/CDC37/HSP90 axis could be involved in UPR in myeloma cells.

Experimental design: We analyzed CK2 activity upon ER stress, the effects of its inactivation on the UPR pathways and on ER stress-induced apoptosis. The consequences of CK2 plus HSP90 inhibition on myeloma cell growth in vitro and in vivo and CK2 regulation of HSP90-triggered UPR were determined.

Results: CK2 partly localized to the ER and ER stress triggered its kinase activity. CK2 inhibition reduced the levels of the ER stress sensors IRE1α and BIP/GRP78, increased phosphorylation of PERK and EIF2α, and enhanced ER stress-induced apoptosis. Simultaneous inactivation of CK2 and HSP90 resulted in a synergic anti-myeloma effect (combination index = 0.291) and in much stronger alterations of the UPR pathways as compared with the single inhibition of the two molecules. Cytotoxicity from HSP90 and CK2 targeting was present in a myeloma microenvironment model, on plasma cells from patients with myeloma and in an in vivo mouse xenograft model. Mechanistically, CK2 inhibition led to a reduction of IRE1α/HSP90/CDC37 complexes in multiple myeloma cells.

Conclusions: Our results place CK2 as a novel regulator of the ER stress/UPR cascades and HSP90 function in myeloma cells and offer the groundwork to design novel combination treatments for this disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Apoptosis / physiology*
  • Benzoquinones / pharmacology
  • Blotting, Western
  • Casein Kinase II / antagonists & inhibitors
  • Casein Kinase II / genetics
  • Casein Kinase II / metabolism*
  • Cell Line, Tumor
  • Cells, Cultured
  • Endoplasmic Reticulum Chaperone BiP
  • Endoplasmic Reticulum Stress / genetics
  • Endoplasmic Reticulum Stress / physiology*
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation, Neoplastic
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors
  • HSP90 Heat-Shock Proteins / genetics
  • HSP90 Heat-Shock Proteins / metabolism*
  • Humans
  • Lactams, Macrocyclic / pharmacology
  • Mice
  • Mice, SCID
  • Microscopy, Confocal
  • Multiple Myeloma / drug therapy
  • Multiple Myeloma / metabolism
  • Multiple Myeloma / physiopathology*
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Thapsigargin / pharmacology
  • Unfolded Protein Response / genetics
  • Unfolded Protein Response / physiology*
  • Xenograft Model Antitumor Assays

Substances

  • Benzoquinones
  • Endoplasmic Reticulum Chaperone BiP
  • Enzyme Inhibitors
  • HSP90 Heat-Shock Proteins
  • HSPA5 protein, human
  • Hspa5 protein, mouse
  • Lactams, Macrocyclic
  • tanespimycin
  • Thapsigargin
  • Casein Kinase II