The N-end rule ubiquitin ligase UBR2 mediates NLRP1B inflammasome activation by anthrax lethal toxin

EMBO J. 2019 Jul 1;38(13):e101996. doi: 10.15252/embj.2019101996. Epub 2019 May 6.

Abstract

Anthrax lethal toxin (LT) is known to induce NLRP1B inflammasome activation and pyroptotic cell death in macrophages from certain mouse strains in its metalloprotease activity-dependent manner, but the underlying mechanism is unknown. Here, we establish a simple but robust cell system bearing dual-fluorescence reporters for LT-induced ASC specks formation and pyroptotic lysis. A genome-wide siRNA screen and a CRISPR-Cas9 knockout screen were applied to this system for identifying genes involved in LT-induced inflammasome activation. UBR2, an E3 ubiquitin ligase of the N-end rule degradation pathway, was found to be required for LT-induced NLRP1B inflammasome activation. LT is known to cleave NLRP1B after Lys44. The cleaved NLRP1B, bearing an N-terminal leucine, was targeted by UBR2-mediated ubiquitination and degradation. UBR2 partnered with an E2 ubiquitin-conjugating enzyme UBE2O in this process. NLRP1B underwent constitutive autocleavage before the C-terminal CARD domain. UBR2-mediated degradation of LT-cleaved NLRP1B thus triggered release of the noncovalent-bound CARD domain for subsequent caspase-1 activation. Our study illustrates a unique mode of inflammasome activation in cytosolic defense against bacterial insults.

Keywords: N-end rule pathway; NLRP1B inflammasome; UBR2; anthrax lethal toxin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Bacterial / adverse effects*
  • Apoptosis Regulatory Proteins / chemistry*
  • Apoptosis Regulatory Proteins / metabolism*
  • Bacterial Toxins / adverse effects*
  • CRISPR-Cas Systems
  • Caspase 1 / metabolism
  • Gene Knockout Techniques
  • HEK293 Cells
  • Humans
  • Inflammasomes / drug effects
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Mice
  • Protein Domains
  • Proteolysis / drug effects
  • RAW 264.7 Cells
  • RNA, Small Interfering / pharmacology
  • Ubiquitin-Conjugating Enzymes / metabolism
  • Ubiquitin-Protein Ligases / chemistry*
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination / drug effects

Substances

  • Antigens, Bacterial
  • Apoptosis Regulatory Proteins
  • Bacterial Toxins
  • Inflammasomes
  • RNA, Small Interfering
  • anthrax toxin
  • Ubiquitin-Conjugating Enzymes
  • Ubiquitin-Protein Ligases
  • Caspase 1