Abrogation of adenosine A1 receptor signalling improves metabolic regulation in mice by modulating oxidative stress and inflammatory responses

Diabetologia. 2015 Jul;58(7):1610-20. doi: 10.1007/s00125-015-3570-3. Epub 2015 Apr 3.

Abstract

Aims/hypothesis: Adenosine is an important regulator of metabolism; however, the role of the A1 receptor during ageing and obesity is unclear. The aim of this study was to investigate the effects of A1 signalling in modulating metabolic function during ageing.

Methods: Age-matched young and aged A 1 (also known as Adora1)-knockout (A1(-/-)) and wild-type (A1(+/+)) mice were used. Metabolic regulation was evaluated by body composition, and glucose and insulin tolerance tests. Isolated islets and islet arterioles were used to detect islet endocrine and vascular function. Oxidative stress and inflammation status were measured in metabolic organs and systemically.

Results: Advanced age was associated with both reduced glucose clearance and insulin sensitivity, as well as increased visceral adipose tissue (VAT) in A1(+/+) compared with A1(-/-) mice. Islet morphology and insulin content were similar between genotypes, but relative changes in in vitro insulin release following glucose stimulation were reduced in aged A1(+/+) compared with A1(-/-) mice. Islet arteriolar responses to angiotensin II were stronger in aged A1(+/+) mice, this being associated with increased NADPH oxidase activity. Ageing resulted in multiple changes in A1(+/+) compared with A1(-/-) mice, including enhanced NADPH oxidase-derived O2(-) formation and NADPH oxidase isoform 2 (Nox2) protein expression in pancreas and VAT; elevated levels of circulating insulin, leptin and proinflammatory cytokines (TNF-α, IL-1β, IL-6 and IL-12); and accumulation of CD4(+) T cells in VAT. This was associated with impaired insulin signalling in VAT from aged A1(+/+) mice.

Conclusions/interpretation: These studies emphasise that A1 receptors regulate metabolism and islet endocrine and vascular functions during ageing, including via the modulation of oxidative stress and inflammatory responses, among other things.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / metabolism
  • Aging / metabolism
  • Angiotensin II / pharmacology
  • Animals
  • Body Composition / genetics
  • CD4-Positive T-Lymphocytes / metabolism
  • Cytokines / metabolism
  • Female
  • Glucose Intolerance / genetics
  • Inflammation / genetics*
  • Insulin / metabolism
  • Insulin Resistance
  • Islets of Langerhans / blood supply
  • Male
  • Membrane Glycoproteins / metabolism
  • Metabolism / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NADPH Oxidase 2
  • NADPH Oxidases / metabolism
  • Oxidative Stress / genetics*
  • Receptor, Adenosine A1 / genetics*
  • Regional Blood Flow / physiology
  • Signal Transduction / genetics

Substances

  • Cytokines
  • Insulin
  • Membrane Glycoproteins
  • Receptor, Adenosine A1
  • Angiotensin II
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases