Cotargeting signaling pathways driving survival and cell cycle circumvents resistance to Kit inhibitors in leukemia

Blood. 2012 May 3;119(18):4228-41. doi: 10.1182/blood-2011-07-368316. Epub 2012 Mar 20.

Abstract

Oncogenic mutations leading to persistent kinase activities are associated with malignancies. Therefore, deciphering the signaling networks downstream of these oncogenic stimuli remains a challenge to gather insights into targeted therapy. To elucidate the biochemical networks connecting the Kit mutant to leukemogenesis, in the present study, we performed a global profiling of tyrosine-phosphorylated proteins from mutant Kit-driven murine leukemia proerythroblasts and identified Shp2 and Stat5 as proximal effectors of Kit. Shp2 or Stat5 gene depletion by sh-RNA, combined with pharmacologic inhibition of PI3kinase or Mek/Erk activities, revealed 2 distinct and independent signaling pathways contributing to malignancy. We demonstrate that cell survival is driven by the Kit/Shp2/Ras/Mek/Erk1/2 pathway, whereas the G(1)/S transition during the cell cycle is accelerated by both the Kit/Stat5 and Kit/PI3K/Akt pathways. The combined use of the clinically relevant drugs NVP-BEZ235, which targets the cell cycle, and Obatoclax, which targets survival, demonstrated synergistic effects to inhibit leukemia cell growth. This synergy was confirmed with a human mast leukemia cell line (HMC-1.2) that expresses mutant Kit. The results of the present study using liquid chromatography/tandem mass spectrometry analysis have elucidated signaling networks downstream of an oncogenic kinase, providing a molecular rationale for pathway-targeted therapy to treat cancer cells refractory to tyrosine kinase inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenylate Kinase / antagonists & inhibitors
  • Adenylate Kinase / physiology
  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Cycle / drug effects
  • Cell Line, Tumor / metabolism
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm / drug effects*
  • Female
  • Humans
  • Imidazoles / pharmacology
  • Indoles
  • Leukemia, Mast-Cell / pathology
  • Mice
  • Mice, Nude
  • Mice, Transgenic
  • Neoplasm Proteins / antagonists & inhibitors*
  • Phosphatidylinositol 3-Kinases / physiology
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Phosphotyrosine / analysis
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Processing, Post-Translational / drug effects
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / antagonists & inhibitors
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / physiology
  • Proto-Oncogene Proteins c-kit / antagonists & inhibitors*
  • Pyrroles / pharmacology
  • Quinolines / pharmacology
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • STAT5 Transcription Factor / antagonists & inhibitors
  • STAT5 Transcription Factor / genetics
  • STAT5 Transcription Factor / physiology
  • Signal Transduction / drug effects*
  • Tumor Stem Cell Assay

Substances

  • Antineoplastic Agents
  • Imidazoles
  • Indoles
  • Neoplasm Proteins
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Kinase Inhibitors
  • Pyrroles
  • Quinolines
  • RNA, Small Interfering
  • STAT5 Transcription Factor
  • Phosphotyrosine
  • Proto-Oncogene Proteins c-kit
  • Adenylate Kinase
  • adenylate kinase 1
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Ptpn11 protein, mouse
  • obatoclax
  • dactolisib