Betulinic acid derivative BA5, a dual NF-kB/calcineurin inhibitor, alleviates experimental shock and delayed hypersensitivity

Eur J Pharmacol. 2017 Nov 15:815:156-165. doi: 10.1016/j.ejphar.2017.09.008. Epub 2017 Sep 9.

Abstract

Betulinic acid (BA) is a naturally occurring triterpenoid with several biological properties already described, including immunomodulatory activity. Here we investigated the immunomodulatory activity of eight semi-synthetic amide derivatives of betulinic acid. Screening of derivatives BA1-BA8 led to the identification of compounds with superior immunomodulatory activity than BA on activated macrophages and lymphocytes. BA5, the most potent derivative, inhibited nitric oxide and TNFα production in a concentration-dependent manner, and decreased NF-κB activation in Raw 264.7 cells. Additionally, BA5 inhibited the proliferation of activated lymphocytes and the secretion of IL-2, IL-4 IL-6, IL-10, IL-17A and IFNɣ, in a concentration-dependent manner. Flow cytometry analysis in lymphocyte cultures showed that treatment with BA5 induces cell cycle arrest in pre-G1 phase followed by cell death by apoptosis. Moreover, BA5 also inhibited the activity of calcineurin, an enzyme that plays a critical role in the progression of cell cycle and T lymphocyte activation. BA5 has a synergistic inhibitory effect with dexamethasone on lymphoproliferation, showing a promising profile for drug combination. Finally, we observed immunosuppressive effects of BA5 in vivo in mouse models of lethal endotoxemia and delayed type hypersensitivity. Our results reinforce the potential use of betulinic acid and its derivatives in the search for potent immunomodulatory drugs.

Keywords: Betulinic acid derivative; Delayed type hypersensitivity, LPS-induced endotoxin shock; T lymphocyte activation.

MeSH terms

  • Amides / chemistry
  • Animals
  • Betulinic Acid
  • Calcineurin Inhibitors / chemistry
  • Calcineurin Inhibitors / pharmacology
  • Calcineurin Inhibitors / therapeutic use
  • Cell Cycle Checkpoints / drug effects
  • Cell Proliferation / drug effects
  • Cytokines / biosynthesis
  • Dexamethasone / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Synergism
  • Hypersensitivity, Delayed / chemically induced
  • Hypersensitivity, Delayed / drug therapy*
  • Hypersensitivity, Delayed / immunology*
  • Hypersensitivity, Delayed / metabolism
  • Immunomodulation / drug effects
  • Lipopolysaccharides / pharmacology
  • Lymphocyte Activation / drug effects
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / immunology
  • Mice
  • NF-kappa B / antagonists & inhibitors*
  • Pentacyclic Triterpenes
  • RAW 264.7 Cells
  • Shock, Septic / chemically induced
  • Shock, Septic / drug therapy*
  • Shock, Septic / immunology*
  • Shock, Septic / metabolism
  • T-Lymphocytes / cytology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • Triterpenes / chemistry*
  • Triterpenes / pharmacology*
  • Triterpenes / therapeutic use

Substances

  • Amides
  • Calcineurin Inhibitors
  • Cytokines
  • Lipopolysaccharides
  • NF-kappa B
  • Pentacyclic Triterpenes
  • Triterpenes
  • Dexamethasone
  • Betulinic Acid