Harnessing Noxa demethylation to overcome Bortezomib resistance in mantle cell lymphoma

Oncotarget. 2015 Sep 29;6(29):27332-42. doi: 10.18632/oncotarget.2903.

Abstract

Bortezomib (BZM) is the first proteasome inhibitor approved for relapsed Mantle Cell Lymphoma (MCL) with durable responses seen in 30%-50% of patients. Given that a large proportion of patients will not respond, BZM resistance is a significant barrier to use this agent in MCL. We hypothesized that a subset of aberrantly methylated genes may be modulating BZM response in MCL patients. Genome-wide DNA methylation analysis using a NimbleGen array platform revealed a striking promoter hypomethylation in MCL patient samples following BZM treatment. Pathway analysis of differentially methylated genes identified molecular mechanisms of cancer as a top canonical pathway enriched among hypomethylated genes in BZM treated samples. Noxa, a pro-apoptotic Bcl-2 family member essential for the cytotoxicity of BZM, was significantly hypomethylated and induced following BZM treatment. Therapeutically, we could demethylate Noxa and induce anti-lymphoma activity using BZM and the DNA methytransferase inhibitor Decitabine (DAC) and their combination in vitro and in vivo in BZM resistant MCL cells. These findings suggest a role for dynamic Noxa methylation for the therapeutic benefit of BZM. Potent and synergistic cytotoxicity between BZM and DAC in vitro and in vivo supports a strategy for using epigenetic priming to overcome BZM resistance in relapsed MCL patients.

Keywords: Bortezomib; Noxa; mantle cell lymphoma; methylation; resistance.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Azacitidine / analogs & derivatives
  • Azacitidine / chemistry
  • Bortezomib / pharmacology*
  • Cell Line, Tumor
  • Cell Survival
  • DNA (Cytosine-5-)-Methyltransferases / antagonists & inhibitors
  • DNA Methylation
  • Decitabine
  • Drug Resistance, Neoplasm*
  • Epigenesis, Genetic
  • Female
  • Humans
  • Lymphoma, Mantle-Cell / drug therapy*
  • Mice
  • Mice, Nude
  • Neoplasm Transplantation
  • Oligonucleotide Array Sequence Analysis
  • Promoter Regions, Genetic
  • Proteasome Inhibitors / chemistry
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Recurrence

Substances

  • Antineoplastic Agents
  • PMAIP1 protein, human
  • Proteasome Inhibitors
  • Proto-Oncogene Proteins c-bcl-2
  • Bortezomib
  • Decitabine
  • DNA (Cytosine-5-)-Methyltransferases
  • Azacitidine