Aryl-functionalised α,α'-Trehalose 6,6'-Glycolipid Induces Mincle-independent Pyroptotic Cell Death

Inflammation. 2023 Aug;46(4):1365-1380. doi: 10.1007/s10753-023-01814-5. Epub 2023 May 4.

Abstract

α,α'-Trehalose 6,6'-glycolipids have long been known for their immunostimulatory properties. The adjuvanticity of α,α'-trehalose 6,6'-glycolipids is mediated by signalling through the macrophage inducible C-type lectin (Mincle) and the induction of an inflammatory response. Herein, we present an aryl-functionalised trehalose glycolipid, AF-2, that leads to the release of cytokines and chemokines, including IL-6, MIP-2 and TNF-α, in a Mincle-dependent manner. Furthermore, plate-coated AF-2 also leads to the Mincle-independent production of IL-1β, which is unprecedented for this class of glycolipid. Upon investigation into the mode of action of plate-coated AF-2, it was observed that the treatment of WT and Mincle-/- bone marrow derived macrophages (BMDM), murine RAW264.7 cells, and human monocytes with AF-2 led to lytic cell death, as evidenced using Sytox Green and lactate dehydrogenase assays, and confocal and scanning electron microscopy. The requirement for functional Gasdermin D and Caspase-1 for IL-1β production and cell death by AF-2 confirmed pyroptosis as the mode of action of AF-2. The inhibition of NLRP3 and K+ efflux reduced AF-2 mediated IL-1β production and cell death, and allowed us to conclude that AF-2 leads to Capase-1 dependent NLRP3 inflammasome-mediated cell death. The unique mode of action of plate-coated AF-2 was surprising and highlights how the physical presentation of Mincle ligands can lead to dramatically different immunological outcomes.

Keywords: Caspase-1.; adjuvant; inflammasome; macrophage; mincle; pyroptosis.

MeSH terms

  • Animals
  • Furylfuramide
  • Glycolipids* / metabolism
  • Glycolipids* / pharmacology
  • Humans
  • Lectins, C-Type / metabolism
  • Mice
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Pyroptosis*
  • Trehalose / metabolism

Substances

  • Glycolipids
  • Trehalose
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Furylfuramide
  • Lectins, C-Type