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Sleep enhances IL-6 trans-signaling in humans

Stoyan Dimitrov^*, Tanja Lange, Christian Benedict^*, Mari A. Nowell, Simon A. Jones, Jürgen Scheller, Stefan Rose-John and Jan Born^*,1

^* Department of Neuroendocrinology, University of Lübeck, Germany;

Department of Internal Medicine, University of Lübeck, Germany;

Department of Medical Biochemistry and Immunology, The School of Medicine, Cardiff; University, Cardiff, Wales, UK; and

Department of Biochemistry, Christian-Albrechts University of Kiel, Kiel, Germany

¹Correspondence: Department of Neuroendocrinology, University of Lübeck, Ratzeburger Allee 160, Haus 23a, Lübeck 23538, Germany. E-mail: born{at}kfg.uni-luebeck.de

ABSTRACT

Sleep is commonly considered to support immune defense. The underlying sleep-immune interaction appears to rely critically on cytokines, like interleukin-6 (IL-6), that combine effects on immune and neuronal functions. The IL-6 signal is conveyed in two ways: it stimulates a restricted group of (mostly immune) cells via membrane-bound IL-6 receptors (mIL-6R) by forming a complex with soluble IL-6R (sIL-6R), and it stimulates (via membrane-bound gp130) a great variety of other cell types—a process termed trans-signaling. Focusing on the receptor side of IL-6 signaling, we examined the effect of sleep on sIL-6R plasma concentrations, mIL-6R expression, plasma sgp130, and numbers of IL-6-producing monocytes in healthy humans who were tested during a regular sleep-wake cycle and 24 h of wakefulness while blood was sampled repeatedly. Sleep strongly enhanced concentrations of sIL-6R, exceeding wake levels by 70% at the end of sleep. This rise was due to an increase in the PC (proteolytic cleavage) rather than the DS (differentially spliced) variant of sIL-6R. Sleep did not affect IL-6-producing monocytes, mIL-6R density, or sgp130 concentrations. The selective increase in sIL-6R implicates an enhanced trans-signaling capacity whereby sleep distinctly widens the profile of IL-6 actions, enabling an integrated influence on brain and peripheral organs.—Dimitrov, S., Lange, T., Benedict, C., Nowell, M. A., Jones, S. A., Scheller, J., Rose-John, S., Born, J. Sleep enhances IL-6 trans-signaling in humans.

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