Convallatoxin inhibits IL-1β production by suppressing zinc finger protein 91 (ZFP91)-mediated pro-IL-1β ubiquitination and caspase-8 inflammasome activity

Br J Pharmacol. 2022 May;179(9):1887-1907. doi: 10.1111/bph.15758. Epub 2022 Feb 23.

Abstract

Background and purpose: ZFP91 positively regulates IL-1β production in macrophages and may be a potential therapeutic target to treat inflammatory-related diseases. We investigated whether this process is modulated by convallatoxin, which is a cardiac glycoside isolated from the traditional Chinese medicinal plant Adonis amurensis Regel et Radde.

Experimental approach: In vitro, the mechanisms by which convallatoxin inhibits ZFP91-regulated IL-1β expression were investigated using molecular docking, western blotting, RT-PCR, ELISA, immunofluorescence and immunoprecipitation assays.In vivo, mice liver injury was induced by an intraperitoneal injection of D-GalN and LPS, colitis was induced by oral administration of dextran sulfate sodium (DSS) in drinking water and peritonitis was induced by an intraperitoneal injection of alum.

Key results: We confirmed that convallatoxin inhibited the release of IL-1β by down-regulating ZFP91. Importantly, we found that convallatoxin significantly reduced K63-linked polyubiquitination of pro-IL-1β regulated by ZFP91 and decreased the efficacy of pro-IL-1β cleavage. Moreover, convallatoxin suppressed ZFP91-mediated activation of the non-canonical cysteine-requiring aspartate protease-8 (caspase-8) inflammasome and MAPK signalling pathways in macrophages. Furthermore, we showed that ZFP91 promoted the assembly of the caspase-8 inflammasome complex, whereas convallatoxin treatment reversed this result. Mice in vivo studies further demonstrated that convallatoxin ameliorated D-GalN/LPS-induced liver injury, DSS-induced colitis and alum-induced peritonitis by down-regulating ZFP91.

Conclusion and implications: We show for the first time that convallatoxin-mediated inhibition of ZFP91 is an important regulatory event that prevents inappropriate inflammatory responses to maintain immune homeostasis. This mechanism provides new insight for the development of convallatoxin as a novel anti-inflammatory drug targeting ZFP91.

Linked articles: This article is part of a themed issue on Inflammation, Repair and Ageing. To view the other articles in this section visit http://onlinelibrary.wiley.com/doi/10.1111/bph.v179.9/issuetoc.

Keywords: IL-1β; ZFP91; convallatoxin; inflammasome; polyubiquitination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caspase 1 / metabolism
  • Caspase 8* / metabolism
  • DNA-Binding Proteins / antagonists & inhibitors
  • Inflammasomes* / drug effects
  • Inflammasomes* / metabolism
  • Interleukin-1beta* / antagonists & inhibitors
  • Interleukin-1beta* / biosynthesis
  • Mice
  • Mice, Inbred C57BL
  • Molecular Docking Simulation
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism
  • Strophanthins* / pharmacology
  • Transcription Factors / antagonists & inhibitors
  • Ubiquitination
  • Zinc Fingers

Substances

  • DNA-Binding Proteins
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Strophanthins
  • Transcription Factors
  • Casp8 protein, mouse
  • Caspase 8
  • Caspase 1
  • convallatoxin