IL-1 Transcriptional Responses to Lipopolysaccharides Are Regulated by a Complex of RNA Binding Proteins

J Immunol. 2020 Mar 1;204(5):1334-1344. doi: 10.4049/jimmunol.1900650. Epub 2020 Jan 17.

Abstract

The IL1A and IL1B genes lie in close proximity on chromosome 2 near the gene for their natural inhibitor, IL1RN Despite diverse functions, they are all three inducible through TLR4 signaling but with distinct kinetics. This study analyzed transcriptional induction kinetics, chromosome looping, and enhancer RNA production to understand the distinct regulation of these three genes in human cells. IL1A, IL1B, and IL1RN were rapidly induced after stimulation with LPS; however, IL1B mRNA production was less inhibitable by iBET151, suggesting it does not use pause-release regulation. Surprisingly, chromatin looping contacts between IL1A and IL1B were highly intermingled, although those of IL1RN were distinct, and we focused on comparing IL1A and IL1B transcriptional pathways. Our studies demonstrated that enhancer RNAs were produced from a subset of the regulatory regions, that they were critical for production of the mRNAs, and that they bound a diverse array of RNA binding proteins, including p300 but not CBP. We, furthermore, demonstrated that recruitment of p300 was dependent on MAPKs. Integrator is another RNA binding protein recruited to the promoters and enhancers, and its recruitment was more dependent on NF-κB than MAPKs. We found that integrator and NELF, an RNA polymerase II pausing protein, were associated with RNA in a manner that facilitated interaction. We conclude that IL1A and IL1B share many regulatory contacts, signaling pathways, and interactions with enhancer RNAs. A complex of protein interactions with enhancer RNAs emphasize the role of enhancer RNAs and the overall structural aspects of transcriptional regulation.

Publication types

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

MeSH terms

  • Cell Line
  • E1A-Associated p300 Protein / genetics
  • E1A-Associated p300 Protein / immunology*
  • Humans
  • Interleukin 1 Receptor Antagonist Protein / genetics
  • Interleukin 1 Receptor Antagonist Protein / immunology*
  • Interleukin-1alpha / genetics
  • Interleukin-1alpha / immunology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology*
  • Lipopolysaccharides / pharmacology*
  • Monocytes / immunology*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / immunology*
  • Transcription, Genetic* / drug effects
  • Transcription, Genetic* / immunology

Substances

  • IL1A protein, human
  • IL1B protein, human
  • IL1RN protein, human
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1alpha
  • Interleukin-1beta
  • Lipopolysaccharides
  • RNA-Binding Proteins
  • E1A-Associated p300 Protein
  • EP300 protein, human