HIV-1 Tat-induced diarrhea is improved by the PPARalpha agonist, palmitoylethanolamide, by suppressing the activation of enteric glia

J Neuroinflammation. 2018 Mar 24;15(1):94. doi: 10.1186/s12974-018-1126-4.

Abstract

Background: Diarrhea is a severe complication in HIV-1-infected patients with Trans-activator of transcription (HIV-1 Tat) protein being recognized as a major underlying cause. Beside its direct enterotoxic effects, Tat protein has been recently shown to affect enteric glial cell (EGC) activity. EGCs regulate intestinal inflammatory responses by secreting pro-inflammatory molecules; nonetheless, they might also release immune-regulatory factors, as palmytoilethanolamide (PEA), which exerts anti-inflammatory effects by activating PPARα receptors. We aimed at clarifying whether EGCs are involved in HIV-1 Tat-induced diarrhea and if PEA exerts antidiarrheal activity.

Methods: Diarrhea was induced by intracolonic administration of HIV-1 Tat protein in rats at day 1. PEA alone or in the presence of peroxisome proliferator-activated receptor (PPAR) antagonists was given intraperitoneally from day 2 to day 7. S100B, iNOS, NF-kappaB, TLR4 and GFAP expression were evaluated in submucosal plexi, while S100B and NO levels were measured in EGC submucosal plexi lysates, respectively. To verify whether PEA effects were PPARα-mediated, PPARα-/- mice were also used. After 7 days from diarrhea induction, endogenous PEA levels were measured in submucosal plexi homogenates deriving from rats and PPARα-/- mice.

Results: HIV-1 Tat protein induced rapid onset diarrhea alongside with a significant activation of EGCs. Tat administration significantly increased all hallmarks of neuroinflammation by triggering TLR4 and NF-kappaB activation and S100B and iNOS expression. Endogenous PEA levels were increased following HIV-1 Tat exposure in both wildtype and knockout animals. In PPARα-/- mice, PEA displayed no effects. In wildtype rats, PEA, via PPARα-dependent mechanism, resulted in a significant antidiarrheal activity in parallel with marked reduction of EGC-sustained neuroinflammation.

Conclusions: EGCs mediate HIV-1 Tat-induced diarrhea by sustaining the intestinal neuroinflammatory response. These effects are regulated by PEA through a selective PPARα-dependent mechanism. PEA might be considered as an adjuvant therapy in HIV-1-induced diarrhea.

Keywords: Diarrhea; EGCs; HIV-1 Tat protein; Neuroinflammation; PEA.

MeSH terms

  • Amides
  • Anesthetics, Local / therapeutic use
  • Animals
  • Antiviral Agents / therapeutic use*
  • Diarrhea / chemically induced*
  • Diarrhea / drug therapy*
  • Disease Models, Animal
  • Ethanolamines / metabolism
  • Ethanolamines / therapeutic use*
  • Gastrointestinal Tract / pathology
  • Gastrointestinal Tract / virology
  • Gene Expression Regulation, Viral / drug effects
  • Lidocaine / therapeutic use
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / metabolism
  • Neuroglia / drug effects*
  • PPAR alpha / deficiency
  • PPAR alpha / genetics
  • Palmitic Acids / metabolism
  • Palmitic Acids / therapeutic use*
  • Rats
  • Rats, Wistar
  • S100 Calcium Binding Protein beta Subunit / metabolism
  • tat Gene Products, Human Immunodeficiency Virus / toxicity*

Substances

  • Amides
  • Anesthetics, Local
  • Antiviral Agents
  • Ethanolamines
  • NF-kappa B
  • PPAR alpha
  • Palmitic Acids
  • S100 Calcium Binding Protein beta Subunit
  • tat Gene Products, Human Immunodeficiency Virus
  • palmidrol
  • Lidocaine