Transient T-bet expression functionally specifies a distinct T follicular helper subset

J Exp Med. 2018 Nov 5;215(11):2705-2714. doi: 10.1084/jem.20180927. Epub 2018 Sep 19.

Abstract

T follicular helper (Tfh) cells express transcription factor BCL-6 and cytokine IL-21. Mature Tfh cells are also capable of producing IFN-γ without expressing the Th1 transcription factor T-bet. Whether this IFN-γ-producing Tfh population represents a unique Tfh subset with a distinct differentiation pathway is poorly understood. By using T-bet fate-mapping mouse strains, we discovered that almost all the IFN-γ-producing Tfh cells have previously expressed T-bet and express high levels of NKG2D. DNase I hypersensitivity analysis indicated that the Ifng gene locus is partially accessible in this "ex-T-bet" population with a history of T-bet expression. Furthermore, multicolor tissue imaging revealed that the ex-T-bet Tfh cells found in germinal centers express IFN-γ in situ. Finally, we found that IFN-γ-expressing Tfh cells are absent in T-bet-deficient mice, but fully present in mice with T-bet deletion at late stages of T cell differentiation. Together, our findings demonstrate that transient expression of T-bet epigenetically imprints the Ifng locus for cytokine production in this Th1-like Tfh cell subset.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology*
  • Genomic Imprinting / immunology*
  • Germinal Center / cytology
  • Germinal Center / immunology*
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interleukins / genetics
  • Interleukins / immunology
  • Male
  • Mice
  • Mice, Transgenic
  • Proto-Oncogene Proteins c-bcl-6 / genetics
  • Proto-Oncogene Proteins c-bcl-6 / immunology
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / immunology*
  • Th1 Cells / cytology
  • Th1 Cells / immunology*

Substances

  • Bcl6 protein, mouse
  • IFNG protein, mouse
  • Interleukins
  • Proto-Oncogene Proteins c-bcl-6
  • T-Box Domain Proteins
  • T-box transcription factor TBX21
  • Interferon-gamma
  • interleukin-21