Bcl-2 phosphorylation confers resistance on chronic lymphocytic leukaemia cells to the BH3 mimetics ABT-737, ABT-263 and ABT-199 by impeding direct binding

Br J Pharmacol. 2016 Feb;173(3):471-83. doi: 10.1111/bph.13370. Epub 2016 Jan 16.

Abstract

Background and purpose: Although the ongoing clinical trials of ABT-263 and ABT-199 in chronic lymphocytic leukaemia (CLL) have indicated that BH3 mimetics hold considerable promise, understanding the mechanism of CLL resistance to BH3 mimetics remains a challenge.

Experimental approach: The LD50 values of ABT-737, ABT-263 and ABT-199 in a number of primary CLL cells from 40 patients, were determined. The levels of Bcl-2 family proteins, including phosphorylated Bcl-2 (pBcl-2) and their interactions were measured by immunoblotting and co-immunoprecipitation. In vitro binding assays were performed by isothermal titration calorimetry and ELISA. BH3 profiling in isolated mitochondria was analysed.

Key results: The ratio of (Mcl-1 + pBcl-2) to Bcl-2 expression provided the most significant predictive marker for the cytotoxic potential of ABT-737, ABT-263 and ABT-199 in the panel of CLL samples. Mechanistically, pBcl-2 inhibited the effects of the ABT compounds on the displacement of Bax and Bim from Bcl-2, thereby suppressing mitochondrial apoptosis. The ABT compounds exhibited 100-300-fold lower binding affinity to the glutamic acid, phosphomimetic, mutant of Bcl-2 (T69E, S70E and S87E; EEE-Bcl-2). BH3 peptides exhibited different rank orders of binding affinities to full-length WT-Bcl-2 and full-length EEE-Bcl-2.

Conclusions and implications: Our study suggested that a structural alteration in the BH3-binding groove was induced by phosphorylation of Bcl-2. Our data also provided a framework to overcome resistance of CLL cells to the ABT compounds by combining pBcl-2 kinase inhibitors with the ABT compounds.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aniline Compounds / pharmacology*
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Biphenyl Compounds / pharmacology*
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology*
  • Cell Line
  • Cell Survival / drug effects
  • Cells, Cultured
  • Drug Resistance, Neoplasm*
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell / metabolism*
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Nitrophenols / pharmacology*
  • Peptide Fragments
  • Phosphorylation
  • Piperazines / pharmacology
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • Sulfonamides / pharmacology*

Substances

  • ABT-737
  • Aniline Compounds
  • Antineoplastic Agents
  • Bax protein (53-86)
  • Biphenyl Compounds
  • Bridged Bicyclo Compounds, Heterocyclic
  • Nitrophenols
  • Peptide Fragments
  • Piperazines
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Sulfonamides
  • venetoclax
  • navitoclax