Selective autophagy of RIPosomes maintains innate immune homeostasis during bacterial infection

EMBO J. 2022 Dec 1;41(23):e111289. doi: 10.15252/embj.2022111289. Epub 2022 Oct 11.

Abstract

The NOD1/2-RIPK2 is a key cytosolic signaling complex that activates NF-κB pro-inflammatory response against invading pathogens. However, uncontrolled NF-κB signaling can cause tissue damage leading to chronic diseases. The mechanisms by which the NODs-RIPK2-NF-κB innate immune axis is activated and resolved remain poorly understood. Here, we demonstrate that bacterial infection induces the formation of endogenous RIPK2 oligomers (RIPosomes) that are self-assembling entities that coat the bacteria to induce NF-κB response. Next, we show that autophagy proteins IRGM and p62/SQSTM1 physically interact with NOD1/2, RIPK2 and RIPosomes to promote their selective autophagy and limit NF-κB activation. IRGM suppresses RIPK2-dependent pro-inflammatory programs induced by Shigella and Salmonella. Consistently, the therapeutic inhibition of RIPK2 ameliorates Shigella infection- and DSS-induced gut inflammation in Irgm1 KO mice. This study identifies a unique mechanism where the innate immune proteins and autophagy machinery are recruited together to the bacteria for defense as well as for maintaining immune homeostasis.

Keywords: Irgm1; NOD1/2-RIPK2-NF-κB; RIPosomes; autophagy; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy
  • Bacterial Infections*
  • Homeostasis
  • Immunity, Innate
  • Mice
  • Mice, Inbred NOD
  • NF-kappa B* / metabolism

Substances

  • NF-kappa B