Geniposide ameliorates diabetic nephropathy in type 2 diabetic mice by targeting AGEs-RAGE-dependent inflammatory pathway

Phytomedicine. 2024 Dec:135:156046. doi: 10.1016/j.phymed.2024.156046. Epub 2024 Sep 12.

Abstract

Background: Diabetic nephropathy (DN) is a prevalent complication of diabetes mellitus and the primary cause of morbidity and mortality in end-stage renal disease. The receptor for advanced glycation end products (RAGE) plays a crucial role in mediating AGE-triggered inflammation, which has been implicated in DN pathogenesis. While geniposide, a natural compound, has demonstrated anti-inflammatory and hypoglycemic properties, its potential to mitigate AGE-induced renal inflammation and consequently impede DN progression remains unexplored.

Purpose: The objective of this study was to ascertain whether geniposide is a novel natural AGEs-RAGE blocker and to investigate its protective effect on renal DN in type 2 diabetic mice.

Methods: Binding affinity between geniposide and RAGE was assessed using MicroScale Thermophoresis (MST), molecular docking, and co-immunoprecipitation. RAGE was then subjected to knockdown and overexpression in cellular experiments to evaluate geniposide's effects on AGE-induced inflammatory responses and the RAGE pathway. Finally, db/db mice were employed to validate the renoprotective effects of geniposide in DN.

Results: Geniposide exhibited higher binding affinity to RAGE's V domain than AGEs, competitively inhibiting AGEs-RAGE interaction through hydrogen bonding. It suppressed RAGE expression and RAGE-dependent inflammatory responses to AGEs, comparable to RAGE siRNA effects. In RAGE-overexpressing cells, geniposide further inhibited AGEs-induced ERK1/2 and NFκB P65 activation, reducing inflammatory marker levels. Long-term oral administration of geniposide to db/db mice improved plasma creatinine, urea, and proteinuria levels, ameliorated pathological changes, and downregulated inflammatory factors such as TNF-α and IL-1β. Moreover, it dose-dependently attenuated enhanced renal expression of RAGE, phosphorylated ERK1/2, IκB-α, and NF-κB P65.

Conclusion: Geniposide effectively attenuates AGEs-induced RAGE activation by directly blocking AGEs-RAGE signal transduction, thereby mitigating inflammatory responses. These findings suggest that geniposide has potential as a high-affinity RAGE antagonist, potentially playing a crucial role in the treatment of DN.

Keywords: AGEs; Diabetic nephropathy; Geniposide; Inflammatory response; RAGE.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Diabetes Mellitus, Experimental / drug therapy
  • Diabetes Mellitus, Type 2* / complications
  • Diabetes Mellitus, Type 2* / drug therapy
  • Diabetic Nephropathies* / drug therapy
  • Glycation End Products, Advanced* / metabolism
  • Humans
  • Inflammation / drug therapy
  • Interleukin-1beta / metabolism
  • Iridoids* / pharmacology
  • Kidney / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Molecular Docking Simulation
  • NF-kappa B / metabolism
  • Receptor for Advanced Glycation End Products* / metabolism
  • Signal Transduction / drug effects
  • Transcription Factor RelA / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Iridoids
  • geniposide
  • Receptor for Advanced Glycation End Products
  • Glycation End Products, Advanced
  • Anti-Inflammatory Agents
  • Interleukin-1beta
  • Transcription Factor RelA
  • Tumor Necrosis Factor-alpha
  • Mitogen-Activated Protein Kinase 3
  • NF-kappa B
  • Rela protein, mouse