Analysis of gamma c-family cytokine target genes. Identification of dual-specificity phosphatase 5 (DUSP5) as a regulator of mitogen-activated protein kinase activity in interleukin-2 signaling

J Biol Chem. 2003 Feb 14;278(7):5205-13. doi: 10.1074/jbc.M209015200. Epub 2002 Nov 14.

Abstract

Interleukin (IL)-2, IL-4, IL-7, IL-9, IL-15, and IL-21 form a family of cytokines based on their sharing the common cytokine receptor gamma chain, gamma(c), which is mutated in X-linked severe combined immunodeficiency (SCID). As a step toward further elucidating the mechanism of action of these cytokines in T-cell biology, we compared the gene expression profiles of IL-2, IL-4, IL-7, and IL-15 in T cells using cDNA microarrays. IL-2, IL-7, and IL-15 each induced a highly similar set of genes, whereas IL-4 induced distinct genes correlating with differential STAT protein activation by this cytokine. One gene induced by IL-2, IL-7, and IL-15 but not IL-4 was dual-specificity phosphatase 5 (DUSP5). In IL-2-dependent CTLL-2 cells, we show that IL-2-induced ERK-1/2 activity was inhibited by wild type DUSP5 but markedly increased by an inactive form of DUSP5, suggesting a negative feedback role for DUSP5 in IL-2 signaling. Our findings provide insights into the shared versus distinctive actions by different members of the gamma(c) family of cytokines. Moreover, we have identified a DUSP5-dependent negative regulatory pathway for MAPK activity in T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Dual-Specificity Phosphatases
  • Gene Expression Regulation
  • Humans
  • Interleukin-2 / genetics
  • Interleukin-2 / metabolism*
  • MAP Kinase Signaling System / genetics
  • Protein Tyrosine Phosphatases / analysis
  • Protein Tyrosine Phosphatases / genetics
  • Protein Tyrosine Phosphatases / metabolism*
  • Receptors, Cytokine / genetics
  • Receptors, Cytokine / metabolism
  • Signal Transduction / genetics*
  • T-Lymphocytes / metabolism*

Substances

  • Interleukin-2
  • Receptors, Cytokine
  • DUSP5 protein, human
  • Dual-Specificity Phosphatases
  • Protein Tyrosine Phosphatases