Genetic variation in IL-4 activated tissue resident macrophages determines strain-specific synergistic responses to LPS epigenetically

Nat Commun. 2025 Jan 25;16(1):1030. doi: 10.1038/s41467-025-56379-8.

Abstract

How macrophages in the tissue environment integrate multiple stimuli depends on the genetic background of the host, but this is still poorly understood. We investigate IL-4 activation of male C57BL/6 and BALB/c strain specific in vivo tissue-resident macrophages (TRMs) from the peritoneal cavity. C57BL/6 TRMs are more transcriptionally responsive to IL-4 stimulation, with induced genes associated with more super enhancers, induced enhancers, and topologically associating domains (TAD) boundaries. IL-4-directed epigenomic remodeling reveals C57BL/6 specific enrichment of NF-κB, IRF, and STAT motifs. Additionally, IL-4-activated C57BL/6 TRMs demonstrate an augmented synergistic response upon in vitro lipopolysaccharide (LPS) exposure, despite naïve BALB/c TRMs displaying a more robust transcriptional response to LPS. Single-cell RNA sequencing (scRNA-seq) analysis of mixed bone marrow chimeras indicates that transcriptional differences and synergy are cell intrinsic within the same tissue environment. Hence, genetic variation alters IL-4-induced cell intrinsic epigenetic reprogramming resulting in strain specific synergistic responses to LPS exposure.

MeSH terms

  • Animals
  • Epigenesis, Genetic*
  • Genetic Variation*
  • Interleukin-4* / genetics
  • Interleukin-4* / metabolism
  • Interleukin-4* / pharmacology
  • Lipopolysaccharides* / pharmacology
  • Macrophage Activation / drug effects
  • Macrophage Activation / genetics
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C*
  • Mice, Inbred C57BL*
  • NF-kappa B / metabolism
  • Species Specificity

Substances

  • Lipopolysaccharides
  • Interleukin-4
  • NF-kappa B
  • Il4 protein, mouse