Origin and Function of Stress-Induced IL-6 in Murine Models

Cell. 2020 Jul 23;182(2):372-387.e14. doi: 10.1016/j.cell.2020.05.054. Epub 2020 Jun 30.

Abstract

Acute psychological stress has long been known to decrease host fitness to inflammation in a wide variety of diseases, but how this occurs is incompletely understood. Using mouse models, we show that interleukin-6 (IL-6) is the dominant cytokine inducible upon acute stress alone. Stress-inducible IL-6 is produced from brown adipocytes in a beta-3-adrenergic-receptor-dependent fashion. During stress, endocrine IL-6 is the required instructive signal for mediating hyperglycemia through hepatic gluconeogenesis, which is necessary for anticipating and fueling "fight or flight" responses. This adaptation comes at the cost of enhancing mortality to a subsequent inflammatory challenge. These findings provide a mechanistic understanding of the ontogeny and adaptive purpose of IL-6 as a bona fide stress hormone coordinating systemic immunometabolic reprogramming. This brain-brown fat-liver axis might provide new insights into brown adipose tissue as a stress-responsive endocrine organ and mechanistic insight into targeting this axis in the treatment of inflammatory and neuropsychiatric diseases.

Keywords: IL-6; acute stress; beta-adrenergic receptors; brown adipose tissue; gluconeogenesis; immunometabolism; inflammation; neuroendocrine-immune axis; neuroimmunology; tolerance.

Publication types

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

MeSH terms

  • Adipose Tissue, Brown / metabolism*
  • Animals
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / metabolism
  • Bone Marrow Transplantation
  • Brain / metabolism
  • Chemokines / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Gluconeogenesis
  • Hyperglycemia / metabolism
  • Hyperglycemia / pathology
  • Interleukin-6 / blood
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism*
  • Liver / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Adrenergic, beta-3 / metabolism
  • Receptors, Interleukin-6 / metabolism
  • Stress, Psychological*
  • Uncoupling Protein 1 / deficiency
  • Uncoupling Protein 1 / genetics

Substances

  • Chemokines
  • Cytokines
  • Interleukin-6
  • Receptors, Adrenergic, beta-3
  • Receptors, Interleukin-6
  • Ucp1 protein, mouse
  • Uncoupling Protein 1