Class IIa HDAC4 and HDAC7 cooperatively regulate gene transcription in Th17 cell differentiation

Proc Natl Acad Sci U S A. 2024 Apr 30;121(18):e2312111121. doi: 10.1073/pnas.2312111121. Epub 2024 Apr 24.

Abstract

Class II histone deacetylases (HDACs) are important in regulation of gene transcription during T cell development. However, our understanding of their cell-specific functions is limited. In this study, we reveal that class IIa Hdac4 and Hdac7 (Hdac4/7) are selectively induced in transcription, guiding the lineage-specific differentiation of mouse T-helper 17 (Th17) cells from naive CD4+ T cells. Importantly, Hdac4/7 are functionally dispensable in other Th subtypes. Mechanistically, Hdac4 interacts with the transcription factor (TF) JunB, facilitating the transcriptional activation of Th17 signature genes such as Il17a/f. Conversely, Hdac7 collaborates with the TF Aiolos and Smrt/Ncor1-Hdac3 corepressors to repress transcription of Th17 negative regulators, including Il2, in Th17 cell differentiation. Inhibiting Hdac4/7 through pharmacological or genetic methods effectively mitigates Th17 cell-mediated intestinal inflammation in a colitis mouse model. Our study uncovers molecular mechanisms where HDAC4 and HDAC7 function distinctively yet cooperatively in regulating ordered gene transcription during Th17 cell differentiation. These findings suggest a potential therapeutic strategy of targeting HDAC4/7 for treating Th17-related inflammatory diseases, such as ulcerative colitis.

Keywords: HDAC4 and HDAC7; Th17 cell differentiation; drug discovery; gene transcription.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation*
  • Colitis* / genetics
  • Colitis* / immunology
  • Colitis* / metabolism
  • Gene Expression Regulation
  • Histone Deacetylases* / genetics
  • Histone Deacetylases* / metabolism
  • Humans
  • Interleukin-17 / metabolism
  • Interleukin-2 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Receptor Co-Repressor 1*
  • Nuclear Receptor Co-Repressor 2 / genetics
  • Nuclear Receptor Co-Repressor 2 / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Th17 Cells* / cytology
  • Th17 Cells* / immunology
  • Th17 Cells* / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic

Substances

  • Histone Deacetylases
  • Hdac7 protein, mouse
  • Hdac5 protein, mouse
  • JunB protein, mouse
  • Transcription Factors
  • Ncor1 protein, mouse
  • Nuclear Receptor Co-Repressor 2
  • Interleukin-17
  • Ncor2 protein, mouse
  • Il17a protein, mouse
  • histone deacetylase 3
  • Repressor Proteins
  • Interleukin-2
  • Nuclear Receptor Co-Repressor 1