Dapagliflozin improves diabetic kidney disease by inhibiting ferroptosis through β-hydroxybutyrate production

Ren Fail. 2025 Dec;47(1):2438857. doi: 10.1080/0886022X.2024.2438857. Epub 2025 Jan 2.

Abstract

Background: Diabetic kidney disease (DKD) is the leading cause of end-stage renal disease. Sodium-glucose cotransporter protein 2 inhibitors (SGLT2i) are antihyperglycemic agents that provide additional renal-protective effects in patients with DKD, independent of their glucose-lowering effects. However, the underlying mechanism remains unclear. This study hypothesized that SGLT2i could alleviate diabetic kidney injury by inhibiting ferroptosis and explored its potential mechanisms.

Methods: C57BL/6J mice were randomly divided into the control, DKD, DKD+dapagliflozin, and DKD+insulin treatment groups. Blood glucose levels and body weight were monitored. Renal function, tissue pathology, mitochondrial morphology and function, and lipid peroxidation biomarkers (lipid peroxidation [LPO], malondialdehyde [MDA], glutathione peroxidase 4 [GPX4], glutathione [GSH], and cystine transporter solute carrier family 7 member 11 [SLC7A11]) were evaluated. Human proximal tubule cells (HK2 cells) were exposed to high glucose alone or in combination with dapagliflozin. The mitochondrial membrane potential (MMP), adenosine triphosphate (ATP) level, NAD+/NADH ratio (oxidized/reduced ratio of nicotinamide adenine dinucleotide), and lipid peroxidation were measured. In addition, the role of the β-hydroxybutyrate- Calcium/Calmodulin Dependent Protein Kinase Kinase 2 (BHB-CaMKK2) axis in mediating dapagliflozin regulating ferroptosis was examined.

Results: Dapagliflozin significantly ameliorated kidney injury in mice with DKD. Typical changes in ferroptosis, including lipid peroxidation and impaired antioxidant capacity, increased in mice with DKD and HG-treated HK-2 cells. Dapagliflozin significantly improves ferroptosis-related lipid peroxidation and mitochondrial dysfunction. Furthermore, dapagliflozin suppressed the expression of CaMKK2, a key ferroptosis regulator. Specific CaMKK2 inhibitors alleviated mitochondrial damage and ferroptosis, whereas a CaMKK2 agonist counteracted the protective effects of dapagliflozin against mitochondrial, antioxidant, and anti-ferroptosis effects. In addition, dapagliflozin increased BHB production, which mediates its nephroprotective effects.

Conclusion: Dapagliflozin improves DKD by inhibiting ferroptosis, promoting BHB production, and regulating CaMKK2.

Keywords: CaMKK2; SGLT2i; dapagliflozin; diabetic kidney disease; ferroptosis.

Plain language summary

Dapagliflozin protects against diabetic kidney damage both in vivo and in vitro.Dapagliflozin is effective in attenuating diabetic kidney damage related ferroptosis.Dapagliflozin improves diabetic kidney disease by promoting β-hydroxybutyrate production.

MeSH terms

  • 3-Hydroxybutyric Acid* / pharmacology
  • Amino Acid Transport System y+
  • Animals
  • Benzhydryl Compounds* / pharmacology
  • Benzhydryl Compounds* / therapeutic use
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism
  • Cell Line
  • Diabetes Mellitus, Experimental / complications
  • Diabetes Mellitus, Experimental / drug therapy
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetic Nephropathies* / drug therapy
  • Diabetic Nephropathies* / metabolism
  • Diabetic Nephropathies* / pathology
  • Ferroptosis* / drug effects
  • Glucosides* / pharmacology
  • Glucosides* / therapeutic use
  • Humans
  • Kidney Tubules, Proximal / drug effects
  • Kidney Tubules, Proximal / metabolism
  • Kidney Tubules, Proximal / pathology
  • Lipid Peroxidation* / drug effects
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Mice, Inbred C57BL*
  • Sodium-Glucose Transporter 2 Inhibitors* / pharmacology
  • Sodium-Glucose Transporter 2 Inhibitors* / therapeutic use

Substances

  • dapagliflozin
  • Glucosides
  • Benzhydryl Compounds
  • Sodium-Glucose Transporter 2 Inhibitors
  • 3-Hydroxybutyric Acid
  • Slc7a11 protein, mouse
  • Blood Glucose
  • Amino Acid Transport System y+