PTEN permits acute increases in D3-phosphoinositide levels following TCR stimulation but inhibits distal signaling events by reducing the basal activity of Akt

Eur J Immunol. 2004 Nov;34(11):3165-75. doi: 10.1002/eji.200425206.

Abstract

Phosphoinositide 3-kinase (PI3K) is important in TCR signaling. PI3K generates phosphatidylinositol 3, 4, 5-trisphosphate (PI-3,4,5-P3), which regulates membrane localization and/or activity of multiple signaling proteins. PTEN (phosphatase and tensin homologue deleted on chromosome 10) opposes PI3K, reversing this reaction. Maintaining the balance between these two enzymes is important for normal T cell function. Here we use the PTEN-null Jurkat T cell line to address the role of PTEN in modulating proximal and distal TCR-signaling events. PTEN expression at levels that restored low basal Akt phosphorylation (an indicator of PI-3,4,5-P3 levels), but which were not themselves cytotoxic, had minimal effect on TCR-stimulated activation of phospholipase Cgamma1 and Ca2+ flux, but reduced the duration of extracellular signal-regulated kinase (Erk) activation. Distal signaling events, including nuclear factor of activated T cells (NFAT) activation, CD69 expression and IL-2 production, were all inhibited by PTEN expression. Notably, PTEN did not block TCR-stimulated PI-3,4,5-P3 accumulation. The effect of PTEN on distal TCR signaling events was strongly correlated with the loss of the constitutive Akt activation and glycogen synthase kinase-3 (GSK3) inhibition that is typical of Jurkat cells, and could be reversed by expression of activated Akt or pharmacologic inhibition of GSK3. These results suggest that PTEN acts in T cells primarily to control basal PI-3,4,5-P3 levels, rather than opposing PI3K acutely during TCR stimulation.

MeSH terms

  • Androstadienes / pharmacology
  • Antigens, CD / immunology
  • Antigens, Differentiation, T-Lymphocyte / immunology
  • Calcium / immunology
  • DNA-Binding Proteins
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / immunology
  • Humans
  • Interleukin-2 / antagonists & inhibitors
  • Interleukin-2 / immunology
  • Jurkat Cells
  • Lectins, C-Type
  • Microscopy, Confocal
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / immunology
  • NFATC Transcription Factors
  • Nuclear Proteins
  • PTEN Phosphohydrolase
  • Phosphatidylinositol Phosphates / immunology*
  • Phospholipase C gamma
  • Phosphoric Monoester Hydrolases / immunology*
  • Phosphoric Monoester Hydrolases / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • Protein Serine-Threonine Kinases / immunology
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Proto-Oncogene Proteins / immunology
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Receptors, Antigen, T-Cell / immunology*
  • Signal Transduction / immunology
  • Transcription Factors
  • Tumor Suppressor Proteins / immunology*
  • Tumor Suppressor Proteins / metabolism
  • Type C Phospholipases / immunology
  • Wortmannin

Substances

  • Androstadienes
  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD69 antigen
  • DNA-Binding Proteins
  • Interleukin-2
  • Lectins, C-Type
  • NFATC Transcription Factors
  • Nuclear Proteins
  • Phosphatidylinositol Phosphates
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Receptors, Antigen, T-Cell
  • Transcription Factors
  • Tumor Suppressor Proteins
  • phosphatidylinositol 3,4,5-triphosphate
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinase 1
  • Glycogen Synthase Kinase 3
  • Phosphoric Monoester Hydrolases
  • PTEN Phosphohydrolase
  • PTEN protein, human
  • Type C Phospholipases
  • Phospholipase C gamma
  • Calcium
  • Wortmannin