Pancreatic, but not myeloid-cell, expression of interleukin-1alpha is required for maintenance of insulin secretion and whole body glucose homeostasis

Mol Metab. 2021 Feb:44:101140. doi: 10.1016/j.molmet.2020.101140. Epub 2020 Dec 5.

Abstract

Objective: The expression of the interleukin-1 receptor type I (IL-1R) is enriched in pancreatic islet β-cells, signifying that ligands activating this pathway are important for the health and function of the insulin-secreting cell. Using isolated mouse, rat, and human islets, we identified the cytokine IL-1α as a highly inducible gene in response to IL-1R activation. In addition, IL-1α is elevated in mouse and rat models of obesity and Type 2 diabetes. Since less is known about the biology of IL-1α relative to IL-1β in pancreatic tissue, our objective was to investigate the contribution of IL-1α to pancreatic β-cell function and overall glucose homeostasis in vivo.

Methods: We generated a novel mouse line with conditional IL-1α alleles and subsequently produced mice with either pancreatic- or myeloid lineage-specific deletion of IL-1α.

Results: Using this in vivo approach, we discovered that pancreatic (IL-1αPdx1-/-), but not myeloid-cell, expression of IL-1α (IL-1αLysM-/-) was required for the maintenance of whole body glucose homeostasis in both male and female mice. Moreover, pancreatic deletion of IL-1α led to impaired glucose tolerance with no change in insulin sensitivity. This observation was consistent with our finding that glucose-stimulated insulin secretion was reduced in islets isolated from IL-1αPdx1-/- mice. Alternatively, IL-1αLysM-/- mice (male and female) did not have any detectable changes in glucose tolerance, respiratory quotient, physical activity, or food intake when compared with littermate controls.

Conclusions: Taken together, we conclude that there is an important physiological role for pancreatic IL-1α to promote glucose homeostasis by supporting glucose-stimulated insulin secretion and islet β-cell mass in vivo.

Keywords: Cytokine receptors; Cytokines; Inflammation; Pancreatic islet; Rodent.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Line
  • Cytokines / metabolism
  • Diabetes Mellitus, Type 2 / metabolism
  • Female
  • Glucose / metabolism*
  • Glucose Intolerance / metabolism
  • Homeodomain Proteins
  • Homeostasis*
  • Inflammation
  • Insulin / blood
  • Insulin / metabolism
  • Insulin Resistance
  • Insulin Secretion / physiology*
  • Insulin-Secreting Cells / metabolism
  • Interleukin-1alpha / metabolism*
  • Islets of Langerhans / metabolism
  • Male
  • Mice
  • Myeloid Cells / metabolism*
  • Pancreas / metabolism*
  • Rats
  • Receptors, Cytokine
  • Receptors, Interleukin-1 Type I / metabolism
  • Trans-Activators

Substances

  • Cytokines
  • Homeodomain Proteins
  • Insulin
  • Interleukin-1alpha
  • Receptors, Cytokine
  • Receptors, Interleukin-1 Type I
  • Trans-Activators
  • pancreatic and duodenal homeobox 1 protein
  • Glucose