Mechanistic insight into WEB-2170-induced apoptosis in human acute myelogenous leukemia cells: the crucial role of PTEN

Exp Hematol. 2009 Oct;37(10):1176-1185.e21. doi: 10.1016/j.exphem.2009.07.002. Epub 2009 Jul 15.

Abstract

Objective: This study aimed to investigate the mechanisms of action of WEB-2170, an inverse agonist of platelet-activating factor receptor, capable of inducing apoptosis in human acute myelogenous leukemia (AML) cells.

Material and methods: Gene expression profiling followed by cytofluorimetric, morphologic, and biologic analyses were used to monitor WEB-2170 effects in AML cell lines (ie, NB4, KG1, NB4-MR4, THP1, and U937) and blasts from patients with different AML (M0-M5) subtypes. PTEN silencing with small interfering RNA was also performed.

Results: We have demonstrated that drug-mediated cytostasis/apoptosis in NB4 cells is characterized by upregulation of cyclin G2, p21/WAF1, NIX, TNF-alpha, and PTEN expression, and downregulation of cyclin D2 and BCL2 expression. We observed an increase in PTEN protein accompanied by a decrease in phospho-extracellular signal-regulated kinase 2 (ERK2) and phospho-AKT, and by forkhead box O3a (FOXO3a) cytoplasmic-nuclear translocation; the mitochondrial cytochrome C release and PARP cleavage marked the late apoptotic steps. We have found that WEB-2170 triggered apoptosis in NB4, KG1, and NB4-MR4 cells where PTEN was expressed, but not in THP1 and U937 cells where PTEN was absent. Finally, we show that PTEN silencing in NB4 cells by PTEN-specific small interfering RNA resulted in a significant reduction of drug-induced apoptosis.

Conclusion: We demonstrated that WEB-2170 is a powerful antileukemic agent with interesting translational opportunities to treat AML and described mechanisms of drug-induced intrinsic and extrinsic apoptosis both in AML cell lines and blasts from AML patients by addressing PTEN as the master regulator of the whole process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Disease
  • Adult
  • Aged
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects*
  • Apoptosis / physiology
  • Azepines / pharmacology*
  • Cell Line, Tumor / drug effects
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Leukemic / drug effects
  • Gene Expression Regulation, Leukemic / physiology
  • Humans
  • Leukemia, Myeloid / pathology*
  • Male
  • Middle Aged
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / pathology
  • PTEN Phosphohydrolase / antagonists & inhibitors
  • PTEN Phosphohydrolase / biosynthesis
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / physiology*
  • Phosphorylation / drug effects
  • Polymerase Chain Reaction
  • Protein Processing, Post-Translational / drug effects
  • Protein Transport / drug effects
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • Resting Phase, Cell Cycle / drug effects
  • Triazoles / pharmacology*
  • Young Adult

Substances

  • Antineoplastic Agents
  • Azepines
  • Neoplasm Proteins
  • RNA, Small Interfering
  • Triazoles
  • bepafant
  • PTEN Phosphohydrolase
  • PTEN protein, human