CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms

Mol Cell Biol. 2005 Nov;25(21):9543-53. doi: 10.1128/MCB.25.21.9543-9553.2005.

Abstract

CTLA-4 and PD-1 are receptors that negatively regulate T-cell activation. Ligation of both CTLA-4 and PD-1 blocked CD3/CD28-mediated upregulation of glucose metabolism and Akt activity, but each accomplished this regulation using separate mechanisms. CTLA-4-mediated inhibition of Akt phosphorylation is sensitive to okadaic acid, providing direct evidence that PP2A plays a prominent role in mediating CTLA-4 suppression of T-cell activation. In contrast, PD-1 signaling inhibits Akt phosphorylation by preventing CD28-mediated activation of phosphatidylinositol 3-kinase (PI3K). The ability of PD-1 to suppress PI3K/AKT activation was dependent upon the immunoreceptor tyrosine-based switch motif located in its cytoplasmic tail, adding further importance to this domain in mediating PD-1 signal transduction. Lastly, PD-1 ligation is more effective in suppressing CD3/CD28-induced changes in the T-cell transcriptional profile, suggesting that differential regulation of PI3K activation by PD-1 and CTLA-4 ligation results in distinct cellular phenotypes. Together, these data suggest that CTLA-4 and PD-1 inhibit T-cell activation through distinct and potentially synergistic mechanisms.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antigens, CD
  • Antigens, Differentiation / physiology*
  • Antigens, Surface / physiology*
  • Apoptosis Regulatory Proteins / physiology*
  • CD28 Antigens / metabolism
  • CD3 Complex / metabolism
  • CTLA-4 Antigen
  • Enzyme Activation
  • Gene Expression Regulation
  • Humans
  • In Vitro Techniques
  • Lymphocyte Activation / physiology*
  • Okadaic Acid / pharmacology
  • Oncogene Protein v-akt / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphatidylinositols / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphoprotein Phosphatases / antagonists & inhibitors
  • Phosphoprotein Phosphatases / metabolism
  • Phosphorylation
  • Programmed Cell Death 1 Receptor
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / physiology*

Substances

  • Antigens, CD
  • Antigens, Differentiation
  • Antigens, Surface
  • Apoptosis Regulatory Proteins
  • CD28 Antigens
  • CD3 Complex
  • CTLA-4 Antigen
  • CTLA4 protein, human
  • PDCD1 protein, human
  • Phosphatidylinositols
  • Phosphoinositide-3 Kinase Inhibitors
  • Programmed Cell Death 1 Receptor
  • Okadaic Acid
  • Oncogene Protein v-akt
  • Phosphoprotein Phosphatases