Impact of the ACE2 activator xanthenone on tacrolimus nephrotoxicity: Modulation of uric acid/ERK/p38 MAPK and Nrf2/SOD3/GCLC signaling pathways

Life Sci. 2022 Jan 1:288:120154. doi: 10.1016/j.lfs.2021.120154. Epub 2021 Nov 17.

Abstract

Aims: The calcineurin inhibitor tacrolimus is an effective and widely used immunosuppressant after organ transplantation to reduce graft rejection. However, its nephrotoxic effect could compel the patients to treatment discontinuation. The beneficial effects of angiotensin-converting enzyme 2 (ACE2) on the kidney and other organs have been investigated in several studies, but its role in tacrolimus nephrotoxicity still needs to be elucidated. Our study was designed to investigate effects of the ACE2 activator xanthenone on tacrolimus-induced renal injury.

Materials and methods: Male Wistar rats were administered xanthenone (2 mg/kg) concurrently with tacrolimus (1 mg/kg) for 3 weeks, then blood and kidney tissue samples were collected for biochemical and molecular investigations.

Key findings: Co-administration of xanthenone significantly improved renal functions in tacrolimus-treated rats, where serum creatinine, urea, and uric acid levels were close to those of the normal control. Besides, xanthenone reduced renal angiotensin (ANG) II content, while elevated ANG (1-7). Relative protein expressions of p-ERK/ERK and p-p38 MAPK/p38 MAPK inflammatory signals were downregulated upon xanthenone administration with tacrolimus. In addition, xanthenone reinforced antioxidant defense against tacrolimus by enhancing protein expression of the transcription factor Nrf2 with subsequently increased mRNA expressions of the antioxidants SOD3 and GCLC.

Significance: These protective effects of xanthenone could be attributed to ANG II degradation to ANG (1-7) by ACE2 activation resulting in regulated inflammatory and oxidative responses in the kidney. Therefore, administration of xanthenone along with tacrolimus could be a promising therapeutic strategy to reduce the adverse effects and increase the tolerability to tacrolimus immunosuppressive therapy.

Keywords: ACE2 activation; ERK/p38 MAPK; Nrf2/SOD3/GCLC; Tacrolimus; Uric acid; Xanthenone.

MeSH terms

  • Angiotensin II / genetics
  • Angiotensin II / metabolism
  • Angiotensin-Converting Enzyme 2 / metabolism*
  • Animals
  • Calcineurin Inhibitors / toxicity
  • Enzyme Activation
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Gene Expression Regulation / drug effects*
  • Glutamate-Cysteine Ligase / genetics
  • Glutamate-Cysteine Ligase / metabolism
  • Kidney Diseases / chemically induced
  • Kidney Diseases / drug therapy*
  • Kidney Diseases / metabolism
  • Kidney Diseases / pathology
  • Male
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism
  • Rats
  • Rats, Wistar
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Tacrolimus / toxicity*
  • Uric Acid / metabolism
  • Xanthenes / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Calcineurin Inhibitors
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, rat
  • Xanthenes
  • Angiotensin II
  • Uric Acid
  • Sod3 protein, rat
  • Superoxide Dismutase
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Ace2 protein, rat
  • Angiotensin-Converting Enzyme 2
  • Glutamate-Cysteine Ligase
  • GCLC protein, rat
  • Tacrolimus