Interleukin 37 reverses the metabolic cost of inflammation, increases oxidative respiration, and improves exercise tolerance

Proc Natl Acad Sci U S A. 2017 Feb 28;114(9):2313-2318. doi: 10.1073/pnas.1619011114. Epub 2017 Feb 13.

Abstract

IL-1 family member interleukin 37 (IL-37) has broad antiinflammatory properties and functions as a natural suppressor of innate inflammation. In this study, we demonstrate that treatment with recombinant human IL-37 reverses the decrease in exercise performance observed during systemic inflammation. This effect was associated with a decrease in the levels of plasma and muscle cytokines, comparable in extent to that obtained upon IL-1 receptor blockade. Exogenous administration of IL-37 to healthy mice, not subjected to an inflammatory challenge, also improved exercise performance by 82% compared with vehicle-treated mice (P = 0.01). Treatment with eight daily doses of IL-37 resulted in a further 326% increase in endurance running time compared with the performance level of mice receiving vehicle (P = 0.001). These properties required the engagement of the IL-1 decoy receptor 8 (IL-1R8) and the activation of AMP-activated protein kinase (AMPK), because both inhibition of AMPK and IL-1R8 deficiency abrogated the positive effects of IL-37 on exercise performance. Mechanistically, treatment with IL-37 induced marked metabolic changes with higher levels of muscle AMPK, greater rates of oxygen consumption, and increased oxidative phosphorylation. Metabolomic analyses of plasma and muscles of mice treated with IL-37 revealed an increase in AMP/ATP ratio, reduced levels of proinflammatory mediator succinate and oxidative stress-related metabolites, as well as changes in amino acid and purine metabolism. These effects of IL-37 to limit the metabolic costs of chronic inflammation and to foster exercise tolerance provide a rationale for therapeutic use of IL-37 in the treatment of inflammation-mediated fatigue.

Keywords: AMPK; fatigue; inflammation; interleukin 37; metabolism.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Cell Line
  • Cell Respiration / drug effects
  • Exercise Test
  • Exercise Tolerance / drug effects*
  • Exercise Tolerance / physiology
  • Gene Expression Regulation
  • Humans
  • Inflammation / chemically induced
  • Inflammation / drug therapy*
  • Inflammation / genetics
  • Inflammation / pathology
  • Interleukin-1 / pharmacology*
  • Lipopolysaccharides
  • Male
  • Metabolome / drug effects*
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Skeletal / drug effects*
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology
  • Myoblasts / drug effects
  • Myoblasts / metabolism
  • Myoblasts / pathology
  • Oxidative Phosphorylation / drug effects
  • Physical Conditioning, Animal / physiology
  • Receptors, Interleukin-1 / genetics
  • Receptors, Interleukin-1 / metabolism
  • Recombinant Proteins / pharmacology
  • Rotarod Performance Test
  • Running / physiology

Substances

  • IL37 protein, human
  • Interleukin-1
  • Lipopolysaccharides
  • Receptors, Interleukin-1
  • Recombinant Proteins
  • SIGIRR protein, mouse
  • AMP-Activated Protein Kinases