A Thpok-Directed Transcriptional Circuitry Promotes Bcl6 and Maf Expression to Orchestrate T Follicular Helper Differentiation

Immunity. 2019 Sep 17;51(3):465-478.e6. doi: 10.1016/j.immuni.2019.06.023. Epub 2019 Aug 15.

Abstract

The generation of high-affinity neutralizing antibodies, the objective of most vaccine strategies, occurs in B cells within germinal centers (GCs) and requires rate-limiting "help" from follicular helper CD4+ T (Tfh) cells. Although Tfh differentiation is an attribute of MHC II-restricted CD4+ T cells, the transcription factors driving Tfh differentiation, notably Bcl6, are not restricted to CD4+ T cells. Here, we identified a requirement for the CD4+-specific transcription factor Thpok during Tfh cell differentiation, GC formation, and antibody maturation. Thpok promoted Bcl6 expression and bound to a Thpok-responsive region in the first intron of Bcl6. Thpok also promoted the expression of Bcl6-independent genes, including the transcription factor Maf, which cooperated with Bcl6 to mediate the effect of Thpok on Tfh cell differentiation. Our findings identify a transcriptional program that links the CD4+ lineage with Tfh differentiation, a limiting factor for efficient B cell responses, and suggest avenues to optimize vaccine generation.

Keywords: Bcl6; CD4 T cells; Maf; Thpok; follicular helper T cells; germinal center reaction.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Neutralizing / immunology
  • B-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Differentiation / immunology*
  • Female
  • Gene Expression Regulation / immunology
  • Germinal Center / immunology
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins c-bcl-6 / immunology*
  • Proto-Oncogene Proteins c-maf / immunology*
  • T-Lymphocytes, Helper-Inducer / immunology*
  • Transcription Factors / immunology*
  • Transcription, Genetic / immunology*

Substances

  • Antibodies, Neutralizing
  • Bcl6 protein, mouse
  • Maf protein, mouse
  • Proto-Oncogene Proteins c-bcl-6
  • Proto-Oncogene Proteins c-maf
  • Th-POK protein, mouse
  • Transcription Factors