Cutting Edge: STAT4 Promotes Bhlhe40 Induction to Drive Protective IFN-γ from NK Cells during Viral Infection

J Immunol. 2023 Nov 15;211(10):1469-1474. doi: 10.4049/jimmunol.2300402.

Abstract

NK cells represent a cellular component of the mammalian innate immune system, and they mount rapid responses against viral infection, including the secretion of the potent antiviral effector cytokine IFN-γ. Following mouse CMV infection, Bhlhe40 was the most highly induced transcription factor in NK cells among the basic helix-loop-helix family. Bhlhe40 upregulation in NK cells depended upon IL-12 and IL-18 signals, with the promoter of Bhlhe40 enriched for STAT4 and the permissive histone H3K4me3, and with STAT4-deficient NK cells showing an impairment of Bhlhe40 induction and diminished H3K4me3. Transcriptomic and protein analysis of Bhlhe40-deficient NK cells revealed a defect in IFN-γ production during mouse CMV infection, resulting in diminished protective immunity following viral challenge. Finally, we provide evidence that Bhlhe40 directly promotes IFN-γ by binding throughout the Ifng loci in activated NK cells. Thus, our study reveals how STAT4-mediated control of Bhlhe40 drives protective IFN-γ secretion by NK cells during viral infection.

Publication types

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

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cytokines / metabolism
  • Cytomegalovirus Infections* / metabolism
  • Homeodomain Proteins / metabolism
  • Interferon-gamma
  • Interleukin-12 / metabolism
  • Killer Cells, Natural*
  • Mammals / metabolism
  • Mice
  • STAT4 Transcription Factor / metabolism

Substances

  • Interferon-gamma
  • Cytokines
  • Interleukin-12
  • STAT4 Transcription Factor
  • Bhlhe40 protein, mouse
  • Homeodomain Proteins
  • Basic Helix-Loop-Helix Transcription Factors