Towards a Molecular Understanding of the Link between Imatinib Resistance and Kinase Conformational Dynamics

PLoS Comput Biol. 2015 Nov 25;11(11):e1004578. doi: 10.1371/journal.pcbi.1004578. eCollection 2015 Nov.

Abstract

Due to its inhibition of the Abl kinase domain in the BCR-ABL fusion protein, imatinib is strikingly effective in the initial stage of chronic myeloid leukemia with more than 90% of the patients showing complete remission. However, as in the case of most targeted anti-cancer therapies, the emergence of drug resistance is a serious concern. Several drug-resistant mutations affecting the catalytic domain of Abl and other tyrosine kinases are now known. But, despite their importance and the adverse effect that they have on the prognosis of the cancer patients harboring them, the molecular mechanism of these mutations is still debated. Here by using long molecular dynamics simulations and large-scale free energy calculations complemented by in vitro mutagenesis and microcalorimetry experiments, we model the effect of several widespread drug-resistant mutations of Abl. By comparing the conformational free energy landscape of the mutants with those of the wild-type tyrosine kinases we clarify their mode of action. It involves significant and complex changes in the inactive-to-active dynamics and entropy/enthalpy balance of two functional elements: the activation-loop and the conserved DFG motif. What is more the T315I gatekeeper mutant has a significant impact on the binding mechanism itself and on the binding kinetics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Computational Biology
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Drug Resistance, Neoplasm / physiology*
  • Fusion Proteins, bcr-abl / chemistry*
  • Fusion Proteins, bcr-abl / genetics*
  • Fusion Proteins, bcr-abl / metabolism
  • Humans
  • Imatinib Mesylate / chemistry
  • Imatinib Mesylate / metabolism
  • Imatinib Mesylate / pharmacology*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive
  • Molecular Dynamics Simulation
  • Mutagenesis, Site-Directed
  • Thermodynamics

Substances

  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl

Grants and funding

This work was supported by the Spanish Ministerio de Economia y Competitividad 425 (MEC) grant (BIO2010-20166, AlteredDynamics”) and in part by the Engineering and Physical Sciences Research Council [grant number EP/M013898/1]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.