CCCTC-Binding Factor Translates Interleukin 2- and α-Ketoglutarate-Sensitive Metabolic Changes in T Cells into Context-Dependent Gene Programs

Immunity. 2017 Aug 15;47(2):251-267.e7. doi: 10.1016/j.immuni.2017.07.015.

Abstract

Despite considerable research connecting cellular metabolism with differentiation decisions, the underlying mechanisms that translate metabolite-sensitive activities into unique gene programs are still unclear. We found that aspects of the interleukin-2 (IL-2)-sensitive effector gene program in CD4+ and CD8+ T cells in type 1 conditions (Th1) were regulated by glutamine and alpha-ketoglutarate (αKG)-induced events, in part through changes in DNA and histone methylation states. We further identified a mechanism by which IL-2- and αKG-sensitive metabolic changes regulated the association of CCCTC-binding factor (CTCF) with select genomic sites. αKG-sensitive CTCF sites were often associated with loci containing IL-2- and αKG-sensitive genome organization patterns and gene expression in T cells. IL-2- and αKG-sensitive CTCF sites in T cells were also associated with genes from developmental pathways that had αKG-sensitive expression in embryonic stem cells. The data collectively support a mechanism wherein CTCF serves to translate αKG-sensitive metabolic changes into context-dependent differentiation gene programs.

MeSH terms

  • Animals
  • CCCTC-Binding Factor
  • Cell Differentiation* / genetics
  • Cells, Cultured
  • Cellular Microenvironment
  • DNA Methylation
  • Female
  • Gene Expression Regulation
  • Glutamine / metabolism
  • Histones / metabolism
  • Interleukin-2 / metabolism*
  • Ketoglutaric Acids / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Th1 Cells / immunology*

Substances

  • CCCTC-Binding Factor
  • Ctcf protein, mouse
  • Histones
  • Interleukin-2
  • Ketoglutaric Acids
  • Repressor Proteins
  • Glutamine