Essential roles of S100A10 in Toll-like receptor signaling and immunity to infection

Cell Mol Immunol. 2020 Oct;17(10):1053-1062. doi: 10.1038/s41423-019-0278-1. Epub 2019 Aug 29.

Abstract

Toll-like receptors (TLRs) are key pattern recognition receptors that mediate innate immune responses to infection. However, uncontrolled TLR activation can lead to severe inflammatory disorders such as septic shock. The molecular mechanisms through which TLR responses are regulated are not fully understood. Here, we demonstrate an essential function of S100A10 in TLR signaling. S100A10 was constitutively expressed in macrophages, but was significantly downregulated upon TLR activation. S100A10-deficient macrophages were hyperresponsive to TLR stimulation, and S100A10-deficient mice were more sensitive to endotoxin-induced lethal shock and Escherichia coli-induced abdominal sepsis. Mechanistically, S100A10 regulated macrophage inflammatory responses by interfering with the appropriate recruitment and activation of the receptor-proximal signaling components and eventually inhibited TLR-triggered downstream signaling. These findings expand our understanding of TLR signaling and establish S100A10 as an essential negative regulator of TLR function and a potential therapeutic target for treating inflammatory diseases.

Keywords: Inflammation; Innate immunity; S100A10; Sepsis; TLR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Annexin A2 / deficiency
  • Annexin A2 / metabolism*
  • Cytokines / biosynthesis
  • Escherichia coli / physiology
  • Escherichia coli Infections / immunology*
  • Escherichia coli Infections / metabolism*
  • Escherichia coli Infections / microbiology
  • Humans
  • Immunity*
  • Inflammation / pathology
  • Inflammation Mediators / metabolism
  • Lipopolysaccharides
  • Macrophages / metabolism
  • Mice, Inbred C57BL
  • Myeloid Differentiation Factor 88 / metabolism
  • Phagocytosis / drug effects
  • Protein Binding
  • Protein Domains
  • S100 Proteins / deficiency
  • S100 Proteins / metabolism*
  • Sepsis / pathology
  • Signal Transduction*
  • Toll-Like Receptor 4 / chemistry
  • Toll-Like Receptor 4 / metabolism
  • Toll-Like Receptors / metabolism*

Substances

  • Adaptor Proteins, Vesicular Transport
  • Annexin A2
  • Cytokines
  • Inflammation Mediators
  • Lipopolysaccharides
  • Myeloid Differentiation Factor 88
  • S100 Proteins
  • S100 calcium binding protein A10
  • TICAM-1 protein, mouse
  • Toll-Like Receptor 4
  • Toll-Like Receptors