Evolution-inspired redesign of the LPS receptor caspase-4 into an interleukin-1β converting enzyme

Sci Immunol. 2021 Aug 10;6(62):eabh3567. doi: 10.1126/sciimmunol.abh3567.

Abstract

Innate immune signaling pathways comprise multiple proteins that promote inflammation. This multistep means of information transfer suggests that complexity is a prerequisite for pathway design. Herein, we test this hypothesis by studying caspases that regulate inflammasome-dependent inflammation. Several caspases differ in their ability to recognize bacterial LPS and cleave interleukin-1β (IL-1β). No caspase is known to contain both activities, yet distinct caspases with complementary activities bookend an LPS-induced pathway to IL-1β cleavage. Using caspase-1/4 hybrid proteins present in canines as a guide, we identified molecular determinants of IL-1β cleavage specificity within caspase-1. This knowledge enabled the redesign of human caspase-4 to operate as a one-protein signaling pathway, which intrinsically links LPS detection to IL-1β cleavage and release, independent of inflammasomes. We identified caspase-4 homologues in multiple carnivorans which display the activities of redesigned human caspase-4. These findings illustrate natural signaling pathway diversity and highlight how multistep innate immune pathways can be condensed into a single protein.

Publication types

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

MeSH terms

  • Animals
  • Caspases, Initiator / immunology
  • Caspases, Initiator / metabolism*
  • Cells, Cultured
  • Dogs
  • Escherichia coli / chemistry
  • Humans
  • Interleukin-1beta / immunology
  • Interleukin-1beta / metabolism*
  • Lipopolysaccharide Receptors / immunology
  • Lipopolysaccharide Receptors / metabolism*
  • Lipopolysaccharides / immunology
  • Lipopolysaccharides / metabolism
  • Mice
  • Mice, Knockout

Substances

  • IL1B protein, human
  • Interleukin-1beta
  • Lipopolysaccharide Receptors
  • Lipopolysaccharides
  • CASP4 protein, human
  • Caspases, Initiator