Role of the stress kinase pathway in signaling via the T cell costimulatory receptor 4-1BB

J Immunol. 1999 Sep 15;163(6):2990-8.

Abstract

4-1BB is a member of the TNFR superfamily expressed on activated CD4+ and CD8+ T cells. 4-1BB can costimulate IL-2 production by resting primary T cells independently of CD28 ligation. In this study, we report signaling events following 4-1BB receptor aggregation using an Ak-restricted costimulation-dependent T cell hybridoma, C8.A3. Aggregation of 4-1BB on the surface of C8.A3 cells induces TNFR-associated factor 2 recruitment, which in turn recruits and activates apoptosis signal-regulating kinase-1, leading to downstream activation of c-Jun N-terminal/stress-activated protein kinases (JNK/SAPK). 4-1BB ligation also enhances anti-CD3-induced JNK/SAPK activation in primary T cells. Overexpression of a catalytically inactive form of apoptosis signal-regulating kinase-1 in C8.A3 T cells interferes with activation of the SAPK cascade and with IL-2 secretion, consistent with a critical role for JNK/SAPK activation in 4-1BB-dependent IL-2 production. Given the ability of both CD28 and 4-1BB to induce JNK/SAPK activation, we asked whether hyperosmotic shock, another inducer of this cascade, could function to provide a costimulatory signal to T cells. Osmotic shock of resting primary T cells in conjunction with anti-CD3 treatment was found to costimulate IL-2 production by the T cells, consistent with a pivotal role for JNK/SAPK in T cell costimulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD
  • Calcium-Calmodulin-Dependent Protein Kinases / physiology*
  • Enzyme Activation / immunology
  • Hybridomas / enzymology
  • Hybridomas / immunology
  • Hybridomas / metabolism
  • Interleukin-2 / biosynthesis
  • JNK Mitogen-Activated Protein Kinases
  • Lymphocyte Activation
  • MAP Kinase Kinase Kinase 5
  • MAP Kinase Kinase Kinases*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinases*
  • Osmotic Pressure
  • Protein Serine-Threonine Kinases / metabolism
  • Proteins / metabolism
  • Receptor Aggregation / immunology
  • Receptors, Nerve Growth Factor / immunology
  • Receptors, Nerve Growth Factor / metabolism
  • Receptors, Nerve Growth Factor / physiology*
  • Receptors, Tumor Necrosis Factor / immunology
  • Receptors, Tumor Necrosis Factor / metabolism
  • Receptors, Tumor Necrosis Factor / physiology*
  • Signal Transduction / immunology*
  • T-Lymphocytes / enzymology*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • TNF Receptor-Associated Factor 2
  • Tumor Necrosis Factor Receptor Superfamily, Member 9

Substances

  • Antigens, CD
  • Interleukin-2
  • Proteins
  • Receptors, Nerve Growth Factor
  • Receptors, Tumor Necrosis Factor
  • TNF Receptor-Associated Factor 2
  • Tnfrsf9 protein, mouse
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Protein Serine-Threonine Kinases
  • Calcium-Calmodulin-Dependent Protein Kinases
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • MAP Kinase Kinase Kinases
  • Map3k5 protein, mouse