Enhancement of T cell receptor signaling by a mild oxidative shift in the intracellular thiol pool

J Immunol. 2000 Oct 15;165(8):4319-28. doi: 10.4049/jimmunol.165.8.4319.

Abstract

Exposure of T cells to the macrophage products hydrogen peroxide (HP) or L-lactate (LAC) was previously shown to enhance IL-2 production and to modulate glutathione (GSH) status. We now found that 50 microM HP and 30 mM LAC enhanced strongly the transcription from the IL-2 promoter in Jurkat T cells after stimulation with anti-CD28 together with or without anti-CD3 but not with anti-CD3 Abs alone. Therefore, we used anti-CD3 plus anti-CD28-stimulated cells to investigate the effect of the GSH reductase inhibitor 1, 3-bis(2-chloroethyl)-1-nitrosourea (BCNU) on the signal cascade. BCNU enhanced the transcription to a similar extent as HP or LAC. Lowering the intracellular GSH/GSH disulfide ratio by BCNU, HP, or NO resulted in all cases in the fulminant enhancement of Jun-N-terminal kinase and p38 mitogen-activated protein kinase but not extracellular signal-regulated kinase 1/2. Jun-N-terminal kinase and NF-kappaB activation was enhanced through pathways involving Rac, Vav1, PKCTheta, p56(lck), p59(fyn), and IkappaB kinases. In a cell-free system, the autophosphorylation of rFyn was stimulated by GSH disulfide but not by HP. These findings suggest that the oxidation of the cellular thiol pool may play a role as an amplifying mechanism for TCR/CD3 signals in immune responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal / pharmacology
  • CD28 Antigens / genetics
  • CD28 Antigens / immunology
  • Carmustine / pharmacology
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Genes, Reporter / drug effects
  • Genes, Reporter / immunology
  • Humans
  • Hydrogen Peroxide / pharmacology
  • I-kappa B Kinase
  • Interleukin-2 / biosynthesis
  • Interleukin-2 / genetics
  • Intracellular Fluid / metabolism*
  • Intracellular Fluid / physiology
  • JNK Mitogen-Activated Protein Kinases
  • Jurkat Cells
  • Lactic Acid / pharmacology
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck) / metabolism
  • Mitogen-Activated Protein Kinases / metabolism
  • Muromonab-CD3 / pharmacology
  • NF-kappa B / genetics
  • Oxidation-Reduction
  • Protein Serine-Threonine Kinases / metabolism
  • Protein-Tyrosine Kinases / physiology
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-fyn
  • Receptors, Antigen, T-Cell / physiology*
  • Response Elements / immunology
  • Signal Transduction / immunology*
  • Sulfhydryl Compounds / metabolism*
  • Sulfhydryl Compounds / physiology
  • T-Lymphocytes / enzymology
  • T-Lymphocytes / metabolism
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / immunology

Substances

  • Antibodies, Monoclonal
  • CD28 Antigens
  • Interleukin-2
  • Muromonab-CD3
  • NF-kappa B
  • Proto-Oncogene Proteins
  • Receptors, Antigen, T-Cell
  • Sulfhydryl Compounds
  • Lactic Acid
  • Hydrogen Peroxide
  • Protein-Tyrosine Kinases
  • FYN protein, human
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck)
  • Proto-Oncogene Proteins c-fyn
  • Protein Serine-Threonine Kinases
  • CHUK protein, human
  • I-kappa B Kinase
  • IKBKB protein, human
  • IKBKE protein, human
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases
  • Carmustine