Myricanol represses renal fibrosis by activating TFAM and ZNRF1 to inhibit tubular epithelial cells ferroptosis

Eur J Pharmacol. 2024 Dec 5:984:176999. doi: 10.1016/j.ejphar.2024.176999. Epub 2024 Sep 28.

Abstract

Background: Mitochondrial dysfunction induces ferroptosis in renal tubular epithelial cells (TECs). Studies have shown that myricanol maintains muscle cell function by enhancing mitochondrial energy metabolism.

Hypothesis: Myricanol delays renal fibrosis by maintaining mitochondrial integrity and inhibiting ferroptosis in TECs.

Methods: Mice kidney lacking mitochondrial transcription factor A (TFAM), blood specimens, or pathological sections of renal tissue from patients with renal failure were used to explore the relationship between mitochondrial and renal functions. Erastin induced-TECs ferroptosis was used to study the potential mechanism by which TFAM regulates renal fibrosis. Chronic kidney disease (CKD) mice were utilized to explore the anti-fibrotic effects of myricanol.

Results: The number of mitochondria and TFAM expression were decreased in human blood samples and pathological sections. Renal TFAM-deficient mice exhibited abnormalities in renal function, including ferroptosis and fibrosis. Ferrostatin-1 significantly inhibited renal fibrosis by preventing TECs ferroptosis. Transcriptional sequencing results indicated that zinc and ring finger 1 (ZNRF1) were important downstream genes of TFAM that regulate ferroptosis. We demonstrated that TFAM deficiency and ferroptosis, which destroyed interaction between ZNRF1 and the iron transport-related protein lipocalin-2 (LCN2), but myricanol clould reverse this effect. Overexpression of ZNRF1 efficiently maintained mitochondrial integrity and inhibited renal fibrosis. Myricanol ameliorated transforming growth factor β1-induced mitochondrial impairment. We firstly confirmed that myricanol efficiently improved renal function and suppresses fibrosis in CKD mice.

Conclusions: Myricanol efficiently inhibit fibrosis through activating TFAM to stimulate the interaction between ZNRF1 and LCN2.

Keywords: Ferroptosis; LCN2; Myricanol; Renal fibrosis; TFAM; ZNRF1.

MeSH terms

  • Animals
  • Cyclohexylamines
  • DNA-Binding Proteins* / deficiency
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Epithelial Cells* / drug effects
  • Epithelial Cells* / metabolism
  • Epithelial Cells* / pathology
  • Fatty Alcohols / pharmacology
  • Fatty Alcohols / therapeutic use
  • Ferroptosis* / drug effects
  • Fibrosis*
  • High Mobility Group Proteins
  • Humans
  • Kidney Tubules* / drug effects
  • Kidney Tubules* / metabolism
  • Kidney Tubules* / pathology
  • Lipocalin-2 / genetics
  • Lipocalin-2 / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Mitochondrial Proteins* / genetics
  • Mitochondrial Proteins* / metabolism
  • Phenylenediamines / pharmacology
  • Phenylenediamines / therapeutic use
  • Renal Insufficiency, Chronic / drug therapy
  • Renal Insufficiency, Chronic / metabolism
  • Renal Insufficiency, Chronic / pathology
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • DNA-Binding Proteins
  • Transcription Factors
  • Mitochondrial Proteins
  • Tfam protein, mouse
  • TFAM protein, human
  • Lipocalin-2
  • Fatty Alcohols
  • ferrostatin-1
  • Phenylenediamines
  • Cyclohexylamines
  • High Mobility Group Proteins