Empagliflozin Attenuates Neointima Formation After Arterial Injury and Inhibits Smooth Muscle Cell Proliferation and Migration by Suppressing Platelet-Derived Growth Factor-Related Signaling

J Am Heart Assoc. 2024 Nov 19;13(22):e035044. doi: 10.1161/JAHA.124.035044. Epub 2024 Nov 7.

Abstract

Background: Sodium-glucose cotransporter 2 (SGLT2) inhibitors reduce cardiovascular events. However, the precise mechanisms beyond glycemic control are not fully understood. The objective of this study was to determine the role of PDGF (platelet-derived growth factor)-related signaling in empagliflozin-mediated inhibition of neointima formation.

Methods and results: Adult male nondiabetic Wistar rats were subjected to carotid artery balloon injury. Empagliflozin (30 mg/kg per day) was administered by oral gavage for 18 days beginning 4 days before surgery. The in vitro effects of empagliflozin on rat aortic vascular smooth muscle cell (VSMC) proliferation and migration were also determined. Empagliflozin attenuated balloon injury-induced neointima formation in carotid arteries. In VSMCs, empagliflozin attenuated PDGF-BB-induced proliferation and migration. Moreover, empagliflozin-treated VSMCs did not undergo apoptosis or cytotoxic death. Empagliflozin suppressed PDGF-related signaling, including phosphorylation of PDGF receptor β, Akt, and STAT3 (signal transducer and activator of transcription 3). Overactivation of PDGF signaling attenuated empagliflozin-mediated inhibition of VSMC function. SGLT2 mRNA levels in rat VSMCs were undetectable, and SGLT2 silencing did not alter the empagliflozin-mediated effects, supporting the SGLT2-independent effects of empagliflozin on VSMC.

Conclusions: This study highlights the crucial role of suppressing PDGF-related signaling in mediating the beneficial effects of empagliflozin on neointima formation and VSMC function, which are independent of SGLT2 and glycemic control. Our study provides a novel mechanistic aspect of empagliflozin for the prevention of vascular stenosis disorders.

Keywords: empagliflozin; neointima formation; platelet‐derived growth factor; sodium–glucose cotransporter 2; vascular smooth muscle cells.

MeSH terms

  • Animals
  • Becaplermin / metabolism
  • Becaplermin / pharmacology
  • Benzhydryl Compounds* / pharmacology
  • Carotid Artery Injuries* / drug therapy
  • Carotid Artery Injuries* / metabolism
  • Carotid Artery Injuries* / pathology
  • Cell Movement* / drug effects
  • Cell Proliferation* / drug effects
  • Cells, Cultured
  • Disease Models, Animal
  • Glucosides* / pharmacology
  • Male
  • Muscle, Smooth, Vascular* / drug effects
  • Muscle, Smooth, Vascular* / metabolism
  • Muscle, Smooth, Vascular* / pathology
  • Myocytes, Smooth Muscle* / drug effects
  • Myocytes, Smooth Muscle* / metabolism
  • Myocytes, Smooth Muscle* / pathology
  • Neointima*
  • Phosphorylation
  • Platelet-Derived Growth Factor / metabolism
  • Platelet-Derived Growth Factor / pharmacology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Rats, Wistar*
  • Receptor, Platelet-Derived Growth Factor beta / genetics
  • Receptor, Platelet-Derived Growth Factor beta / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction* / drug effects
  • Sodium-Glucose Transporter 2 Inhibitors* / pharmacology

Substances

  • empagliflozin
  • Glucosides
  • Benzhydryl Compounds
  • Sodium-Glucose Transporter 2 Inhibitors
  • STAT3 Transcription Factor
  • Stat3 protein, rat
  • Proto-Oncogene Proteins c-akt
  • Becaplermin
  • Receptor, Platelet-Derived Growth Factor beta
  • Platelet-Derived Growth Factor