Aberrant DNA methylation of pregnane X receptor underlies metabolic gene alterations in the diabetic kidney

Am J Physiol Renal Physiol. 2018 Apr 1;314(4):F551-F560. doi: 10.1152/ajprenal.00390.2017. Epub 2017 Dec 6.

Abstract

Epigenetic abnormalities have been suggested to mediate metabolic memory observed in diabetic complications. We have shown that epigenetic alterations may induce persistent phenotypic changes in the proximal tubules of the diabetic kidneys. In this study, we show that pregnane X receptor (PXR), a xenobiotic nuclear receptor, is epigenetically altered and upregulated and may have a possible function in the diabetic kidney. PXR has been shown to play a critical role in metabolic changes in obesity and diabetes; however, its distribution and function in the kidney are unknown. In the normal kidney, Pxr was selectively expressed in the proximal tubular cells with demethylation in the promoter DNA. In db/db mice, significant increases in Pxr mRNA, further demethylation of DNA, and stimulatory histone marks in the promoter were observed. Epigenetic changes are likely to play a causative role in PXR induction, since a DNA methyltransferase inhibitor increased PXR mRNA in cultured human proximal tubular cells. Administration of a PXR agonist increased mRNA levels of solute carrier organic anion transporter family member 2B1 ( Slco2b1), a xenobiotic transporter; response gene to complement 32 ( Rgc32), a molecule known to exert fibrotic effects in the kidney; and phosphoenolpyruvate carboxykinase 1 ( Pck1), a gluconeogenic enzyme in the kidney. The expressions of these genes were inhibited by PXR small interfering RNA in cultured proximal tubular cells. Increased mRNA levels of Slco2b1, Rgc32, and Pck1 were also observed in the kidney of db/db mice. These data indicate that PXR is upregulated in the diabetic kidney with aberrant epigenetic modifications and may modulate the course of diabetic kidney disease through the activation of these genes.

Keywords: DNA methylation; diabetic kidney disease; epigenetics; pregnane X receptor; proximal tubules.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cell Line
  • DNA Methylation*
  • Diabetic Nephropathies / genetics*
  • Diabetic Nephropathies / metabolism
  • Disease Models, Animal
  • Energy Metabolism / genetics*
  • Epigenesis, Genetic*
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Kidney Tubules, Proximal / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Organic Anion Transporters / genetics
  • Organic Anion Transporters / metabolism
  • Phenotype
  • Phosphoenolpyruvate Carboxykinase (GTP) / genetics
  • Phosphoenolpyruvate Carboxykinase (GTP) / metabolism
  • Pregnane X Receptor / genetics*
  • Pregnane X Receptor / metabolism
  • Promoter Regions, Genetic

Substances

  • Cell Cycle Proteins
  • Intracellular Signaling Peptides and Proteins
  • Muscle Proteins
  • NR1I2 protein, human
  • Nerve Tissue Proteins
  • Nr1i2 protein, mouse
  • Nuclear Proteins
  • Organic Anion Transporters
  • Pregnane X Receptor
  • RGCC protein, human
  • Rgc-32 protein, mouse
  • SLCO2B1 protein, human
  • Slco2b1 protein, mouse
  • PCK1 protein, human
  • Pck1 protein, mouse
  • Phosphoenolpyruvate Carboxykinase (GTP)