Inhibition of vagally mediated immune-to-brain signaling by vanadyl sulfate speeds recovery from sickness

Proc Natl Acad Sci U S A. 2005 Oct 18;102(42):15184-9. doi: 10.1073/pnas.0507191102. Epub 2005 Oct 10.

Abstract

To the ill patient with diabetes, the behavioral symptoms of sickness such as fatigue and apathy are debilitating and can prevent recuperation. Here we report that peripherally administered insulin-like growth factor 1 (IGF-1) attenuates LPS-dependent depression of social exploration (sickness) in nondiabetic (db/+) but not in diabetic (db/db) mice. We show that the insulin/IGF-1 mimetic vanadyl sulfate (VS) is effective at augmenting recovery from sickness in both db/+ and db/db mice. Specifically, peak illness was reached at 2 h for both VS and control animals injected with LPS, and VS mice recovered 50% faster than non-VS-treated animals. Examination of the mechanism of VS action in db/+ mice showed that VS paradoxically augmented peritoneal macrophage responsivity to LPS, increasing both peritoneal and ex vivo macrophage production of IL-1beta and IL-6 but not TNF-alpha. The effects of VS in promoting recovery from sickness were not restricted to LPS, because they were also observed after direct administration of IL-1beta. To explore the possibility that VS impairs immune-to-brain communication via vagal afferents, the vagally mediated satiety-inducing effects of cholecystokinin 8 were tested in db/+ mice. Cholecystokinin decreased food intake in saline-injected mice but not in VS-treated mice. VS also inhibited LPS-dependent up-regulation of IL-1beta and IL-6 mRNA in the brain, while increasing by 50% the cerebral expression of transcripts of the specific antagonist of IL-1 receptors IL-1RA and IL-1R2. Taken together, these data indicate that VS improves recovery from LPS-induced sickness by blocking vagally mediated immune-to-brain signaling and by up-regulating brain expression of IL-1beta antagonists.

Publication types

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

MeSH terms

  • Animals
  • Brain / physiology*
  • Cells, Cultured
  • Cholecystokinin / pharmacology
  • Diabetes Mellitus / drug therapy
  • Eating / drug effects
  • Exploratory Behavior / drug effects*
  • Humans
  • Hypoglycemic Agents / pharmacology*
  • Hypoglycemic Agents / therapeutic use
  • Immune System / physiology*
  • Insulin-Like Growth Factor I / pharmacology
  • Insulin-Like Growth Factor I / therapeutic use
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1 / metabolism
  • Interleukin-6 / metabolism
  • Lipopolysaccharides / pharmacology
  • Macrophages, Peritoneal / cytology
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / immunology
  • Male
  • Mice
  • Sialoglycoproteins / metabolism
  • Signal Transduction / drug effects*
  • Signal Transduction / physiology
  • Tumor Necrosis Factor-alpha / metabolism
  • Vagus Nerve / metabolism*
  • Vanadium Compounds / pharmacology*
  • Vanadium Compounds / therapeutic use

Substances

  • Hypoglycemic Agents
  • IL1RN protein, human
  • Il1rn protein, mouse
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1
  • Interleukin-6
  • Lipopolysaccharides
  • Sialoglycoproteins
  • Tumor Necrosis Factor-alpha
  • Vanadium Compounds
  • Insulin-Like Growth Factor I
  • vanadyl sulfate
  • Cholecystokinin