Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells

Immunity. 2010 Jan 29;32(1):79-90. doi: 10.1016/j.immuni.2009.11.012. Epub 2010 Jan 21.

Abstract

Interleukin(IL)-2 and inflammation regulate effector and memory cytolytic T-lymphocyte (CTL) generation during infection. We demonstrate a complex interplay between IL-2 and inflammatory signals during CTL differentiation. IL-2 stimulation induced the transcription factor eomesodermin (Eomes), upregulated perforin (Prf1) transcription, and repressed re-expression of memory CTL markers Bcl6 and IL-7Ralpha. Binding of Eomes and STAT5 to Prf1 cis-regulatory regions correlated with transcriptional initiation (increased recruitment of RNA polymerase II to the Prf1 promoter). Inflammation (CpG, IL-12) enhanced expression of IL-2Ralpha and the transcription factor T-bet, but countered late Eomes and perforin induction while preventing IL-7Ralpha repression by IL-2. After infection of mice with lymphocytic choriomeningitis virus, IL-2Ralpha-deficient effector CD8(+) T cells expressed more Bcl6 but less perforin and granzyme B, formed fewer KLRG-1(+) and T-bet-expressing CTL, and killed poorly. Thus, inflammation influences both effector and memory CTL differentiation, whereas persistent IL-2 stimulation promotes effector at the expense of memory CTL development.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology*
  • Cell Separation
  • Cytotoxicity, Immunologic / genetics
  • Cytotoxicity, Immunologic / immunology
  • Flow Cytometry
  • Gene Expression
  • Gene Expression Regulation / immunology*
  • Immunologic Memory / genetics
  • Immunologic Memory / immunology
  • Immunoprecipitation
  • Inflammation / immunology*
  • Inflammation / metabolism
  • Interleukin-2 / genetics
  • Interleukin-2 / immunology*
  • Interleukin-2 / metabolism
  • Mice
  • Mice, Transgenic
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • T-Lymphocyte Subsets / cytology*
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocytes, Cytotoxic / cytology*
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism
  • Transcription, Genetic

Substances

  • Interleukin-2