Allosteric Inhibition of Bcr-Abl Kinase by High Affinity Monobody Inhibitors Directed to the Src Homology 2 (SH2)-Kinase Interface

J Biol Chem. 2016 Apr 15;291(16):8836-47. doi: 10.1074/jbc.M115.707901. Epub 2016 Feb 24.

Abstract

Bcr-Abl is a constitutively active kinase that causes chronic myelogenous leukemia. We have shown that a tandem fusion of two designed binding proteins, termed monobodies, directed to the interaction interface between the Src homology 2 (SH2) and kinase domains and to the phosphotyrosine-binding site of the SH2 domain, respectively, inhibits the Bcr-Abl kinase activity. Because the latter monobody inhibits processive phosphorylation by Bcr-Abl and the SH2-kinase interface is occluded in the active kinase, it remained undetermined whether targeting the SH2-kinase interface alone was sufficient for Bcr-Abl inhibition. To address this question, we generated new, higher affinity monobodies with single nanomolar KD values targeting the kinase-binding surface of SH2. Structural and mutagenesis studies revealed the molecular underpinnings of the monobody-SH2 interactions. Importantly, the new monobodies inhibited Bcr-Abl kinase activity in vitro and in cells, and they potently induced cell death in chronic myelogenous leukemia cell lines. This work provides strong evidence for the SH2-kinase interface as a pharmacologically tractable site for allosteric inhibition of Bcr-Abl.

Keywords: ABL tyrosine kinase; FN3; PPI inhibitor; Src homology 2 domain (SH2 domain); enzyme inhibitor; protein engineering; protein-protein interaction; x-ray crystallography.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Allosteric Regulation / drug effects
  • Allosteric Regulation / immunology
  • Antibodies, Monoclonal, Murine-Derived / chemistry*
  • Antibodies, Monoclonal, Murine-Derived / immunology
  • Antibodies, Monoclonal, Murine-Derived / pharmacology
  • Cell Line, Tumor
  • Fusion Proteins, bcr-abl / antagonists & inhibitors*
  • Fusion Proteins, bcr-abl / chemistry*
  • Fusion Proteins, bcr-abl / immunology
  • Fusion Proteins, bcr-abl / metabolism
  • Humans
  • src Homology Domains

Substances

  • Antibodies, Monoclonal, Murine-Derived
  • BCR-ABL1 fusion protein, human
  • Fusion Proteins, bcr-abl

Associated data

  • PDB/1FNA
  • PDB/1OPK
  • PDB/1OPL
  • PDB/2ABL
  • PDB/2FO0
  • PDB/3K2M
  • PDB/3T04
  • PDB/5DC0
  • PDB/5DC4
  • PDB/5DC9