The α7-nAChR/heme oxygenase-1/carbon monoxide pathway mediates the nicotine counteraction of renal inflammation and vasoconstrictor hyporeactivity in endotoxic male rats

Inflamm Res. 2020 Feb;69(2):217-231. doi: 10.1007/s00011-019-01309-w. Epub 2020 Jan 2.

Abstract

Objective: The objective of the study was to test the hypothesis that nicotine guards against endotoxemia-associated renal inflammation and vasoconstrictor dysfunction via the activation of α7-nicotinic acetylcholine receptors (α7-nAChRs)/heme oxygenase-1 (HO-1) cascade.

Materials: 91 male and female rats were included in the study.

Treatments: Lipopolysaccharide (LPS, 5 mg kg-1), nicotine (0.5-2 mg kg-1), pentoxifylline (PTX, TNFα inhibitor, 3 mg kg-1), methyllycaconitine (MLA, α7-nAChR blocker), zinc protoporphyrin (ZnPP, HO-1 inhibitor), hemin (HO-1 inducer), tricarbonyldichlororuthenium (carbon monoxide-releasing molecule, CORM-2) or bilirubin was administered before LPS.

Methods: Isolated perfused kidney was used to evaluate renal vasoconstriction and immunohistochemistry to assess inflammatory cytokines.

Results: LPS reduced renal vasoconstrictions induced by phenylephrine or vasopressin in perfused kidneys of male, but not female, rats. Higher elevations in serum interleukin-1β and renal expressions of inducible nitric oxide synthase (iNOS) and nuclear factor-κB (NF-κB) were observed in LPS-treated male rats, whereas greater HO-1 expression was evident in endotoxic female rats. LPS effects were reversed by nicotine or PTX. Further, the favorable nicotine actions were (i) diminished by MLA or ZnPP and (ii) replicated by hemin or CORM-2, but not bilirubin, and (iii) associated with exaggerated and MLA-sensitive increases in HO-1 expression.

Conclusions: α7-nAChR/HO-1/CO signaling mediates nicotine protection against renal inflammation and vasoconstrictor hyporeactivity in endotoxic male rats.

Keywords: Endotoxemia; Heme oxygenase-1; Inflammation; Nicotine; Renal vasoconstriction; α7-Nicotinic acetylcholine receptors.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology*
  • Carbon Monoxide / metabolism*
  • Endotoxemia / genetics*
  • Endotoxemia / physiopathology*
  • Female
  • Heme Oxygenase (Decyclizing) / genetics*
  • In Vitro Techniques
  • Inflammation / genetics*
  • Inflammation / physiopathology*
  • Interleukin-1beta / blood
  • Kidney / drug effects
  • Kidney / metabolism
  • Lipopolysaccharides
  • Male
  • Nicotine / pharmacology*
  • Perfusion
  • Rats
  • Rats, Wistar
  • Receptors, Nicotinic / genetics*
  • Signal Transduction / drug effects*
  • Vasoconstrictor Agents / pharmacology*

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • Chrna9 protein, rat
  • IL1B protein, rat
  • Interleukin-1beta
  • Lipopolysaccharides
  • Receptors, Nicotinic
  • Vasoconstrictor Agents
  • Nicotine
  • Carbon Monoxide
  • Heme Oxygenase (Decyclizing)
  • Hmox1 protein, rat