Sex-, Species-, and Tissue-Specific Metabolism of Empagliflozin in Male Mouse Kidney Forms an Unstable Hemiacetal Metabolite (M466/2) That Degrades to 4-Hydroxycrotonaldehyde, a Reactive and Cytotoxic Species

Chem Res Toxicol. 2015 Jan 20;28(1):103-15. doi: 10.1021/tx500380t. Epub 2015 Jan 5.

Abstract

Following oral administration of empagliflozin (1000 mg/kg/day) to male and female CD-1 mice for 2 years, renal tubular injury was identified in male mice. Renal injury was not detected in male mice (≤300 mg/kg/day), in female mice (1000 mg/kg/day), or in male or female Han Wistar rats (700 mg/kg/day). Using transfected HEK293 cells and Xenopus oocytes, empagliflozin was found to be a substrate of various mouse and rat organic anion transporters (oat/Oat) and organic anion transporting polypeptide (oatp/Oatp) transporters: mouse oat3, rat Oat3, mouse oatp1a1, and rat Oatp1a1. However, using isolated kidney slices from male and female mice and rats, no sex-based difference in the extent of uptake of empagliflozin occurred. Metabolism studies using hepatic and renal microsomes from male and female mice, rats, and humans revealed a hemiacetal metabolite of empagliflozin (M466/2), predominantly formed in male mouse kidney microsomes. Formation of M466/2 in male mouse kidney microsomes was 31-fold higher compared to that in female mouse kidney microsomes and was ∼29- and ∼20-fold higher compared to that in male and female mouse liver microsomes, respectively. M466/2 is unstable and degrades to form a phenol metabolite (M380/1) and 4-hydroxycrotonaldehyde (4-OH CTA). Formed 4-OH CTA was trapped by reduced GSH, and the structure of the GSH adduct was confirmed by mass spectrometry. Stoichiometric formation of M380/1 from M466/2 was observed (93-96% at 24 h); however, formation of 4-OH CTA was considerably lower (∼17.5% at 40 h), which is consistent with 4-OH CTA being a highly reactive species. These data represent a highly selective tissue-, species-, and sex-specific lesion in male CD-1 mice associated with a cytotoxic metabolite product, 4-OH CTA. In humans, glucuronidation of empagliflozin is the most prevalent metabolic pathway, and oxidation is a minor pathway. Thus, renal toxicity due to the formation of 4-OH CTA from empagliflozin is not expected in humans.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehydes / metabolism*
  • Animals
  • Benzhydryl Compounds / metabolism*
  • Cytotoxins / metabolism*
  • Female
  • Glucosides / metabolism*
  • HEK293 Cells
  • Humans
  • Hypoglycemic Agents / metabolism*
  • Kidney / metabolism*
  • Kidney Diseases / chemically induced
  • Kidney Diseases / metabolism
  • Liver / metabolism
  • Male
  • Mice
  • Microsomes / metabolism
  • Oocytes / metabolism
  • Organic Anion Transporters / metabolism
  • Rats, Wistar
  • Sex Factors
  • Species Specificity
  • Xenopus laevis

Substances

  • Aldehydes
  • Benzhydryl Compounds
  • Cytotoxins
  • Glucosides
  • Hypoglycemic Agents
  • Organic Anion Transporters
  • penitricin B
  • empagliflozin