The proteasome inhibitor carfilzomib functions independently of p53 to induce cytotoxicity and an atypical NF-κB response in chronic lymphocytic leukemia cells

Clin Cancer Res. 2013 May 1;19(9):2406-19. doi: 10.1158/1078-0432.CCR-12-2754. Epub 2013 Mar 20.

Abstract

Purpose: The proteasome consists of chymotrypsin-like (CT-L), trypsin-like, and caspase-like subunits that cleave substrates preferentially by amino acid sequence. Proteasomes mediate degradation of regulatory proteins of the p53, Bcl-2, and nuclear factor-κB (NF-κB) families that are aberrantly active in chronic lymphocytic leukemia (CLL). CLL remains an incurable disease, and new treatments are especially needed in the relapsed/refractory setting. We therefore investigated the effects of the proteasome inhibitor carfilzomib (CFZ) in CLL cells.

Experimental design: Tumor cells from CLL patients were assayed in vitro using immunoblotting, real-time polymerase chain reaction, and electrophoretic mobility shift assays. In addition, a p53 dominant-negative construct was generated in a human B-cell line.

Results: Unlike bortezomib, CFZ potently induces apoptosis in CLL patient cells in the presence of human serum. CLL cells have significantly lower basal CT-L activity compared to normal B and T cells, although activity is inhibited similarly in T cells versus CLL. Co-culture of CLL cells on stroma protected from CFZ-mediated cytotoxicity; however, PI3K inhibition significantly diminished this stromal protection. CFZ-mediated cytotoxicity in leukemic B cells is caspase-dependent and occurs irrespective of p53 status. In CLL cells, CFZ promotes atypical activation of NF-κB evidenced by loss of cytoplasmic IκBα, phosphorylation of IκBα, and increased p50/p65 DNA binding, without subsequent increases in canonical NF-κB target gene transcription.

Conclusions: Together, these data provide new mechanistic insights into the activity of CFZ in CLL and support phase I investigation of CFZ in this disease.

Publication types

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

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Apoptosis
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / enzymology
  • Benzyl Compounds / pharmacology
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Caspase Inhibitors / pharmacology
  • Caspases / metabolism
  • Cell Survival / drug effects
  • Cyclic N-Oxides
  • Drug Evaluation, Preclinical
  • Humans
  • Hydrocarbons, Fluorinated / pharmacology
  • Indolizines
  • Leukemia, Lymphocytic, Chronic, B-Cell / drug therapy*
  • NF-kappa B / metabolism*
  • Oligopeptides / pharmacology*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Proteasome Endopeptidase Complex / metabolism
  • Proteasome Inhibitors / pharmacology*
  • Protein Subunits / antagonists & inhibitors
  • Protein Subunits / metabolism
  • Pyridinium Compounds / pharmacology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / enzymology
  • Tumor Cells, Cultured / drug effects
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • Antineoplastic Agents
  • Benzyl Compounds
  • Boc-D-FMK
  • Bridged Bicyclo Compounds, Heterocyclic
  • Caspase Inhibitors
  • Cyclic N-Oxides
  • Hydrocarbons, Fluorinated
  • Indolizines
  • NF-kappa B
  • Oligopeptides
  • Phosphoinositide-3 Kinase Inhibitors
  • Proteasome Inhibitors
  • Protein Subunits
  • Pyridinium Compounds
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • dinaciclib
  • carfilzomib
  • Caspases
  • Proteasome Endopeptidase Complex