Interdependent and independent roles of type I interferons and IL-6 in innate immune, neuroinflammatory and sickness behaviour responses to systemic poly I:C

Brain Behav Immun. 2015 Aug:48:274-86. doi: 10.1016/j.bbi.2015.04.009. Epub 2015 Apr 18.

Abstract

Type I interferons (IFN-I) are expressed in the brain during many inflammatory and neurodegenerative conditions and have multiple effects on CNS function. IFN-I is readily induced in the brain by systemic administration of the viral mimetic, poly I:C (synthetic double-stranded RNA). We hypothesised that IFN-I contributes to systemically administered poly I:C-induced sickness behaviour, metabolic and neuroinflammatory changes. IFN-I receptor 1 deficient mice (IFNAR1(-/-)) displayed significantly attenuated poly I:C-induced hypothermia, hypoactivity and weight loss compared to WT C57BL/6 mice. This amelioration of sickness was associated with equivalent IL-1β and TNF-α responses but much reduced IL-6 responses in plasma, hypothalamus and hippocampus of IFNAR1(-/-) mice. IFN-β injection induced trivial IL-6 production and limited behavioural change and the poly I:C-induced IFN-β response did not preceed, and would not appear to mediate, IL-6 induction. Rather, IFNAR1(-/-) mice lack basal IFN-I activity, have lower STAT1 levels and show significantly lower levels of several inflammatory transcripts, including stat1. Basal IFN-I activity appears to play a facilitatory role in the full expression of the IL-6 response and activation of the tryptophan-kynurenine metabolism pathway. The deficient IL-6 response in IFNAR1(-/-) mice partially explains the observed incomplete sickness behaviour response. Reconstitution of circulating IL-6 revealed that the role of IFNAR in burrowing activity is mediated via IL-6, while IFN-I and IL-6 have additive effects on hypoactivity, but the role of IFN-I in anorexia is independent of IL-6. Hence, we have demonstrated both interdependent and independent roles for IFN-I and IL-6 in systemic inflammation-induced changes in brain function.

Keywords: Behaviour; Burrowing; Cytokine; Depression; Hippocampus; Hypoactivity; IDO; IFN-α; IFN-β; IL-6; Interferon; Kynurenine; Neuroinflammation; STAT1; Sickness; Viral.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / drug effects*
  • Brain / metabolism
  • Illness Behavior / drug effects*
  • Illness Behavior / physiology
  • Immunity, Innate / drug effects*
  • Immunity, Innate / physiology
  • Inflammation / metabolism*
  • Interferon Type I / metabolism*
  • Interleukin-1beta / metabolism
  • Interleukin-6 / metabolism*
  • Kynurenine / metabolism
  • Mice
  • Mice, Knockout
  • Motor Activity / drug effects
  • Motor Activity / physiology
  • Poly I-C / pharmacology*
  • Receptors, Interferon / genetics
  • Receptors, Interferon / metabolism
  • Tryptophan / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interferon Type I
  • Interleukin-1beta
  • Interleukin-6
  • Receptors, Interferon
  • Tumor Necrosis Factor-alpha
  • Kynurenine
  • Tryptophan
  • Poly I-C