Postprandial macrophage-derived IL-1β stimulates insulin, and both synergistically promote glucose disposal and inflammation

Nat Immunol. 2017 Mar;18(3):283-292. doi: 10.1038/ni.3659. Epub 2017 Jan 16.

Abstract

The deleterious effect of chronic activation of the IL-1β system on type 2 diabetes and other metabolic diseases is well documented. However, a possible physiological role for IL-1β in glucose metabolism has remained unexplored. Here we found that feeding induced a physiological increase in the number of peritoneal macrophages that secreted IL-1β, in a glucose-dependent manner. Subsequently, IL-1β contributed to the postprandial stimulation of insulin secretion. Accordingly, lack of endogenous IL-1β signaling in mice during refeeding and obesity diminished the concentration of insulin in plasma. IL-1β and insulin increased the uptake of glucose into macrophages, and insulin reinforced a pro-inflammatory pattern via the insulin receptor, glucose metabolism, production of reactive oxygen species, and secretion of IL-1β mediated by the NLRP3 inflammasome. Postprandial inflammation might be limited by normalization of glycemia, since it was prevented by inhibition of the sodium-glucose cotransporter SGLT2. Our findings identify a physiological role for IL-1β and insulin in the regulation of both metabolism and immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Diabetes Mellitus, Type 2 / immunology*
  • Glucose / metabolism
  • Humans
  • Inflammasomes / metabolism
  • Inflammation / immunology*
  • Insulin / metabolism
  • Insulin-Secreting Cells / physiology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Macrophages / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Postprandial Period
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Sodium-Glucose Transporter 2 / metabolism

Substances

  • Inflammasomes
  • Insulin
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Reactive Oxygen Species
  • Slc5a2 protein, mouse
  • Sodium-Glucose Transporter 2
  • Glucose