Context-Dependent IL-1 mRNA-Destabilization by TTP Prevents Dysregulation of Immune Homeostasis Under Steady State Conditions

Front Immunol. 2020 Jul 7:11:1398. doi: 10.3389/fimmu.2020.01398. eCollection 2020.

Abstract

The bioavailability of the major pro-inflammatory cytokines IL-1α and IL-1β is tightly controlled by transcription and post-translational processing to prevent hyperinflammation. The role of mRNA decay in maintenance of physiological IL-1 amounts remained unknown. Here we show that the down-regulation of Il1a and Il1b mRNA by the mRNA-destabilizing protein TTP (gene Zfp36) is required for immune homeostasis. The TTP deficiency syndrome, a multi organ inflammation in TTP-/- mice, was significantly ameliorated upon deletion of the IL-1 receptor. Il1a and Il1b played non-redundant roles in triggering the pathological IL-1 signaling in TTP-/- mice. Accordingly, tissues from TTP-/- animals contained increased amounts of Il1b mRNA. Unexpectedly, TTP destabilized Il1b mRNA in cell type-specific ways as evident from RNA-Seq and mRNA stability assays. These results demonstrate that TTP-driven mRNA destabilization depends on the cellular context. Moreover, such context-defined mRNA decay is essential for keeping steady state IL-1 levels in the physiological range.

Keywords: Interleukin 1alpha; Interleukin 1beta; TTP; Zfp36; immune homeostasis; inflammation; mRNA stability; tristetraprolin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Homeostasis*
  • Immunity / genetics*
  • Inflammation / diagnosis
  • Inflammation / etiology
  • Inflammation / metabolism
  • Interleukin-1 / genetics*
  • Interleukin-1 / metabolism
  • Interleukin-1alpha / genetics
  • Interleukin-1beta / genetics
  • Mice
  • Mice, Knockout
  • RNA Stability
  • Real-Time Polymerase Chain Reaction
  • Severity of Illness Index
  • Tristetraprolin / metabolism*

Substances

  • IL1B protein, mouse
  • Il1a protein, mouse
  • Interleukin-1
  • Interleukin-1alpha
  • Interleukin-1beta
  • Tristetraprolin