Metallothionein 3-Zinc Axis Suppresses Caspase-11 Inflammasome Activation and Impairs Antibacterial Immunity

Front Immunol. 2021 Nov 12:12:755961. doi: 10.3389/fimmu.2021.755961. eCollection 2021.

Abstract

Non-canonical inflammasome activation by mouse caspase-11 (or human CASPASE-4/5) is crucial for the clearance of certain gram-negative bacterial infections, but can lead to severe inflammatory damage. Factors that promote non-canonical inflammasome activation are well recognized, but less is known about the mechanisms underlying its negative regulation. Herein, we identify that the caspase-11 inflammasome in mouse and human macrophages (Mϕ) is negatively controlled by the zinc (Zn2+) regulating protein, metallothionein 3 (MT3). Upon challenge with intracellular lipopolysaccharide (iLPS), Mϕ increased MT3 expression that curtailed the activation of caspase-11 and its downstream targets caspase-1 and interleukin (IL)-1β. Mechanistically, MT3 increased intramacrophage Zn2+ to downmodulate the TRIF-IRF3-STAT1 axis that is prerequisite for caspase-11 effector function. In vivo, MT3 suppressed activation of the caspase-11 inflammasome, while caspase-11 and MT3 synergized in impairing antibacterial immunity. The present study identifies an important yin-yang relationship between the non-canonical inflammasome and MT3 in controlling inflammation and immunity to gram-negative bacteria.

Keywords: MT3; caspase-11 non-canonical inflammasome; innate immunity; macrophage; metallothionein; non-canonical inflammasome; zinc.

Publication types

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

MeSH terms

  • Animals
  • Caspases / immunology*
  • Caspases / metabolism
  • Gram-Negative Bacterial Infections / immunology*
  • Gram-Negative Bacterial Infections / metabolism
  • Humans
  • Inflammasomes / immunology*
  • Inflammasomes / metabolism
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Metallothionein 3 / immunology*
  • Metallothionein 3 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Zinc / immunology*
  • Zinc / metabolism

Substances

  • Inflammasomes
  • Metallothionein 3
  • Caspases
  • Zinc