Tyrosine kinase inhibitors induce down-regulation of c-Kit by targeting the ATP pocket

PLoS One. 2013 Apr 23;8(4):e60961. doi: 10.1371/journal.pone.0060961. Print 2013.

Abstract

The stem cell factor receptor (SCF) c-Kit plays a pivotal role in regulating cell proliferation and survival in many cell types. In particular, c-Kit is required for early amplification of erythroid progenitors, while it must disappear from cell surface for the cell entering the final steps of maturation in an erythropoietin-dependent manner. We initially observed that imatinib (IM), an inhibitor targeting the tyrosine kinase activity of c-Kit concomitantly down-regulated the expression of c-Kit and accelerated the Epo-driven differentiation of erythroblasts in the absence of SCF. We investigated the mechanism by which IM or related masitinib (MA) induce c-Kit down-regulation in the human UT-7/Epo cell line. We found that the down-regulation of c-Kit in the presence of IM or MA was inhibited by a pre-incubation with methyl-β-cyclodextrin suggesting that c-Kit was internalized in the absence of ligand. By contrast to SCF, the internalization induced by TKI was independent of the E3 ubiquitin ligase c-Cbl. Furthermore, c-Kit was degraded through lysosomal, but not proteasomal pathway. In pulse-chase experiments, IM did not modulate c-Kit synthesis or maturation. Analysis of phosphotyrosine peptides in UT-7/Epo cells treated or not with IM show that IM did not modify overall tyrosine phosphorylation in these cells. Furthermore, we showed that a T670I mutation preventing the full access of IM to the ATP binding pocket, did not allow the internalization process in the presence of IM. Altogether these data show that TKI-induced internalization of c-Kit is linked to a modification of the integrity of ATP binding pocket.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Benzamides / pharmacology*
  • Binding Sites / drug effects
  • Cell Line
  • Down-Regulation / drug effects*
  • Erythroblasts / cytology
  • Erythroblasts / drug effects
  • Erythroblasts / metabolism
  • Humans
  • Imatinib Mesylate
  • Ligands
  • Lysosomes / drug effects
  • Lysosomes / metabolism
  • Piperazines / pharmacology*
  • Piperidines
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Transport / drug effects
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Proteolysis / drug effects
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Pyridines
  • Pyrimidines / pharmacology*
  • Thiazoles / pharmacology*

Substances

  • Benzamides
  • Ligands
  • Piperazines
  • Piperidines
  • Protein Kinase Inhibitors
  • Pyridines
  • Pyrimidines
  • Thiazoles
  • Imatinib Mesylate
  • Adenosine Triphosphate
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-kit
  • masitinib

Grants and funding

This work was supported by grants from the Ligue Nationale Contre le Cancer (LNCC : Equipe labellisée) and by a grant from the Agence Nationale de la Recherche (ANR, CAPER). DD was supported by a grant from the Ministere de la Recherche et de l'Enseignement supérieur. JG, CD and CF were supported by a grant from the Association de Recherche contre le Cancer (ARC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript