The Btk-dependent PIP5K1γ lipid kinase activation by Fas counteracts FasL-induced cell death

Apoptosis. 2017 Nov;22(11):1344-1352. doi: 10.1007/s10495-017-1415-x.

Abstract

The Fas/FasL system plays a critical role in death by apoptosis and immune escape of cancer cells. The Fas receptor being ubiquitously expressed in tissues, its apoptotic-inducing function, initiated upon FasL binding, is tightly regulated by several negative regulatory mechanisms to prevent inappropriate cell death. One of them, involving the non-receptor tyrosine kinase Btk, was reported mainly in B cells and only poorly described. We report here that Btk negatively regulates, through its tyrosine kinase activity, the FasL-mediated cell death in epithelial cell lines from colon cancer origin. More importantly, we show that Btk interacts not only with Fas but also with the phosphatidylinositol-4-phosphate 5-kinase, PIP5K1γ, which, upon stimulation by Fas ligand, is responsible of a rapid and transient synthesis of phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2). This production requires both the presence and the tyrosine kinase activity of Btk, and participates in the negative regulation of FasL-mediated cell death since knocking down PIP5K1γ expression significantly strengthens the apoptotic signal upon FasL engagement. Altogether, our data demonstrate the cooperative role of Btk and PIP5K1γ in a FasL-induced PI(4,5)P2 production, both proteins participating to the threshold setting of FasL-induced apoptotic commitment in colorectal cell lines.

Keywords: Btk; Cell death; Fas; PI(4,5)P2; PIP5K1γ.

MeSH terms

  • Agammaglobulinaemia Tyrosine Kinase
  • Cell Death / drug effects*
  • Cell Death / genetics
  • Cell Line
  • Cell Line, Tumor
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Fas Ligand Protein / genetics
  • Fas Ligand Protein / metabolism
  • Fas Ligand Protein / pharmacology*
  • Gene Expression Regulation
  • HT29 Cells
  • Humans
  • Killer Cells, Natural
  • Lymphocytes / cytology
  • Lymphocytes / drug effects
  • Lymphocytes / metabolism
  • Phosphatidylinositol 4,5-Diphosphate / biosynthesis
  • Phosphotransferases (Alcohol Group Acceptor) / antagonists & inhibitors
  • Phosphotransferases (Alcohol Group Acceptor) / genetics*
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / genetics*
  • Protein-Tyrosine Kinases / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • fas Receptor / genetics*
  • fas Receptor / metabolism

Substances

  • FAS protein, human
  • FASLG protein, human
  • Fas Ligand Protein
  • Phosphatidylinositol 4,5-Diphosphate
  • RNA, Small Interfering
  • fas Receptor
  • Phosphotransferases (Alcohol Group Acceptor)
  • 1-phosphatidylinositol-4-phosphate 5-kinase
  • Protein-Tyrosine Kinases
  • Agammaglobulinaemia Tyrosine Kinase
  • BTK protein, human