Akkermansia muciniphila phospholipid induces homeostatic immune responses

Nature. 2022 Aug;608(7921):168-173. doi: 10.1038/s41586-022-04985-7. Epub 2022 Jul 27.

Abstract

Multiple studies have established associations between human gut bacteria and host physiology, but determining the molecular mechanisms underlying these associations has been challenging1-3. Akkermansia muciniphila has been robustly associated with positive systemic effects on host metabolism, favourable outcomes to checkpoint blockade in cancer immunotherapy and homeostatic immunity4-7. Here we report the identification of a lipid from A. muciniphila's cell membrane that recapitulates the immunomodulatory activity of A. muciniphila in cell-based assays8. The isolated immunogen, a diacyl phosphatidylethanolamine with two branched chains (a15:0-i15:0 PE), was characterized through both spectroscopic analysis and chemical synthesis. The immunogenic activity of a15:0-i15:0 PE has a highly restricted structure-activity relationship, and its immune signalling requires an unexpected toll-like receptor TLR2-TLR1 heterodimer9,10. Certain features of the phospholipid's activity are worth noting: it is significantly less potent than known natural and synthetic TLR2 agonists; it preferentially induces some inflammatory cytokines but not others; and, at low doses (1% of EC50) it resets activation thresholds and responses for immune signalling. Identifying both the molecule and an equipotent synthetic analogue, its non-canonical TLR2-TLR1 signalling pathway, its immunomodulatory selectivity and its low-dose immunoregulatory effects provide a molecular mechanism for a model of A. muciniphila's ability to set immunological tone and its varied roles in health and disease.

MeSH terms

  • Akkermansia* / chemistry
  • Akkermansia* / cytology
  • Akkermansia* / immunology
  • Cell Membrane / chemistry
  • Cell Membrane / immunology
  • Cytokines / immunology
  • Homeostasis* / immunology
  • Humans
  • Immunity*
  • Inflammation Mediators / chemical synthesis
  • Inflammation Mediators / chemistry
  • Inflammation Mediators / immunology
  • Phosphatidylethanolamines* / chemical synthesis
  • Phosphatidylethanolamines* / chemistry
  • Phosphatidylethanolamines* / immunology
  • Structure-Activity Relationship
  • Toll-Like Receptor 1 / immunology
  • Toll-Like Receptor 2 / agonists
  • Toll-Like Receptor 2 / immunology

Substances

  • Cytokines
  • Inflammation Mediators
  • Phosphatidylethanolamines
  • TLR1 protein, human
  • TLR2 protein, human
  • Toll-Like Receptor 1
  • Toll-Like Receptor 2

Supplementary concepts

  • Akkermansia muciniphila