New Pathways for the Skin's Stress Response: The Cholinergic Neuropeptide SLURP-1 Can Activate Mast Cells and Alter Cytokine Production in Mice

Front Immunol. 2021 Mar 18:12:631881. doi: 10.3389/fimmu.2021.631881. eCollection 2021.

Abstract

Background: The alpha7 nicotinic acetylcholine receptor (Chrna7) plays an essential anti-inflammatory role in immune homeostasis and was recently found on mast cells (MC). Psychosocial stress can trigger MC hyperactivation and increases pro-inflammatory cytokines in target tissues such as the skin. If the cholinergic system (CS) and Chrna7 ligands play a role in these cascades is largely unknown. Objective: To elucidate the role of the CS in the response to psychosocial stress using a mouse-model for stress-triggered cutaneous inflammatory circuits. Methods: Key CS markers (ACh, Ch, SLURP-1, SLURP-2, Lynx1, Chrm3, Chrna7, Chrna9, ChAT, VAChT, Oct3, AChE, and BChE) in skin and its MC (sMC), MC activation, immune parameters (TNFα, IL1β, IL10, TGFβ, HIF1α, and STAT3) and oxidative stress were analyzed in skin from 24 h noise-stressed mice and in cultured MC (cMC) from C57BL/6 or Chrna7-Knockout mice. Results: First, Chrna7 and SLURP-1 mRNA were exclusively upregulated in stressed skin. Second, histomorphometry located Chrna7 and SLURP-1 in nerves and sMC and demonstrated upregulated contacts and increased Chrna7+ sMC in stressed skin, while 5 ng/mL SLURP-1 degranulated cMC. Third, IL1β+ sMC were high in stressed skin, and while SLURP-1 alone had no significant effect on cMC cytokines, it upregulated IL1β in cMC from Chrna7-KO and in IL1β-treated wildtype cMC. In addition, HIF1α+ sMC were high in stressed skin and Chrna7-agonist AR-R 17779 induced ROS in cMC while SLURP-1 upregulated TNFα and IL1β in cMC when HIF1α was blocked. Conclusions: These data infer that the CS plays a role in the regulation of stress-sensitive inflammatory responses but may have a surprising pro-inflammatory effect in healthy skin, driving IL1β expression if SLURP-1 is involved.

Keywords: Chrna7 knockout; alpha7 nicotinic acetylcholine receptor; cholinergic system; hypoxia inducible factor 1 alpha; mast cells; secreted Ly-6/uPAR-related protein 1; stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Ly / genetics
  • Antigens, Ly / metabolism*
  • Cell Degranulation
  • Cholinergic Agents / metabolism*
  • Cytokines / metabolism*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Inflammation / metabolism
  • Mast Cells / metabolism*
  • Mice
  • Mice, Knockout
  • Nerve Fibers / metabolism
  • Neuropeptides / genetics
  • Neuropeptides / metabolism*
  • Noise / adverse effects
  • Oxidative Stress
  • Skin / metabolism*
  • Stress, Psychological / metabolism
  • Urokinase-Type Plasminogen Activator / genetics
  • Urokinase-Type Plasminogen Activator / metabolism*
  • alpha7 Nicotinic Acetylcholine Receptor / genetics
  • alpha7 Nicotinic Acetylcholine Receptor / metabolism

Substances

  • Antigens, Ly
  • Cholinergic Agents
  • Chrna7 protein, mouse
  • Cytokines
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Neuropeptides
  • SLURP-1 protein, mouse
  • alpha7 Nicotinic Acetylcholine Receptor
  • Urokinase-Type Plasminogen Activator