The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway

Mol Biol Cell. 2005 Jan;16(1):348-57. doi: 10.1091/mbc.e04-05-0369. Epub 2004 Nov 10.

Abstract

Phosphoinositide-3 kinase (PI-3 kinase) and its downstream signaling molecules PDK-1 and Akt were analyzed in SK-N-SH and SK-N-BE(2) human neuroblastoma cell lines. When cells were stimulated with insulin, PI-3 kinase was activated in both cell lines, whereas the translocation of PDK-1 to the membrane fraction and phosphorylated Akt were observed only in SK-N-SH cells. Analyses of the insulin-mediated reactive oxygen species (ROS) generation and Phosphatase and Tensin homolog (PTEN) oxidation indicate that PTEN oxidation occurred in SK-N-SH cells, which can produce ROS, but not in SK-N-BE(2) cells, which cannot increase ROS in response to insulin stimulation. When SK-N-SH cells were pretreated with the NADPH oxidase inhibitor diphenyleneiodonium chloride before insulin stimulation, insulin-mediated translocation of PDK-1 to the membrane fraction and phosphorylation of Akt were remarkably reduced, whereas PI-3 kinase activity was not changed significantly. These results indicate that not only PI-3 kinase activation but also inhibition of PTEN by ROS is needed to increase cellular level of phosphatidylinositol 3,4,5-trisphosphate for recruiting downstream signaling molecules such as PDK-1 and Akt in insulin-mediated signaling. Moreover, the ROS generated by insulin stimulation mainly contributes to the inactivation of PTEN and not to the activation of PI-3 kinase in the PI-3 kinase/Akt pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Phosphoinositide-Dependent Protein Kinases
  • Cell Line, Tumor
  • Cell Membrane / metabolism
  • Electrophoresis, Polyacrylamide Gel
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Immunoblotting
  • Immunoprecipitation
  • Insulin / metabolism*
  • NADPH Oxidases / metabolism
  • Onium Compounds / pharmacology
  • Oxygen / metabolism
  • PTEN Phosphohydrolase
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphoric Monoester Hydrolases / metabolism*
  • Phosphorylation
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Transport
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Reactive Oxygen Species
  • Time Factors
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Enzyme Inhibitors
  • Insulin
  • Onium Compounds
  • Proto-Oncogene Proteins
  • Reactive Oxygen Species
  • Tumor Suppressor Proteins
  • diphenyleneiodonium
  • Hydrogen Peroxide
  • NADPH Oxidases
  • 3-Phosphoinositide-Dependent Protein Kinases
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Phosphoric Monoester Hydrolases
  • PTEN Phosphohydrolase
  • PTEN protein, human
  • Oxygen