Zinc finger protein 91 positively regulates the production of IL-1β in macrophages by activation of MAPKs and non-canonical caspase-8 inflammasome

Br J Pharmacol. 2018 Dec;175(23):4338-4352. doi: 10.1111/bph.14493. Epub 2018 Oct 15.

Abstract

Background and purpose: IL-1β is a cytokine of critical importance in inflammatory, infectious and autoimmune diseases. Zinc finger protein 91 (ZFP91) has been reported to be involved in multiple biological processes. Here, we identified a previously unknown role for ZFP91 in the production of biologically active IL-1β and investigated the underlying mechanisms of its effects.

Experimental approach: In vitro, the underlying mechanisms of ZFP91 at inhibiting the expression of IL-1β were investigated by ELISA, RT-PCR, Western blotting, immunoprecipitation and immunofluorescence assays. In vivo, colitis was induced by giving 4% dextran sulfate sodium (DSS) p.o. in drinking water for 5 days. Peritonitis was induced by injecting 700 μg alum i.p. for 12 h.

Key results: ZFP91 activated the non-canonical caspase-8 inflammasome, which resulted in robust IL-1β secretion. Using an immunoprecipitation assay and immunofluorescence assay, we found that ZFP91 promoted the assembly of the non-canonical caspase-8 inflammasome complex. Moreover, ZFP91 enhanced the activation of ERK, p38 MAPK and JNK in macrophages. In addition, our data demonstrate that the synthesis of pro-IL-1β is dependent on activation of these MAPK signalling pathways. In vivo experiments, the symptoms and colonic inflammation associated with DSS-induced colitis were ameliorated in mice deficient in ZFP91. Furthermore, the inflammation in alum-induced peritonitis was also attenuated in mice deficient in ZFP91.

Conclusions and implications: Our research describes a mechanism by which ZFP91 promotes production of IL-1β under physiological conditions and suggests that ZFP91 may be a promising therapeutic target for intervention in inflammatory, infectious and autoimmune-related diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Administration, Oral
  • Animals
  • Caspase 8 / metabolism*
  • Cells, Cultured
  • Colitis / chemically induced
  • Colitis / drug therapy
  • Colitis / metabolism
  • Dextran Sulfate / administration & dosage
  • Humans
  • Inflammasomes / metabolism*
  • Interleukin-1beta / biosynthesis*
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinases / metabolism*
  • THP-1 Cells
  • Ubiquitin-Protein Ligases / deficiency
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Inflammasomes
  • Interleukin-1beta
  • Dextran Sulfate
  • Ubiquitin-Protein Ligases
  • Mitogen-Activated Protein Kinases
  • CASP8 protein, human
  • Caspase 8
  • ZFP91 protein, human