Gut microbiota mediates the protective effects of β-hydroxybutyrate against cisplatin-induced acute kidney injury

Biomed Pharmacother. 2024 Jun:175:116752. doi: 10.1016/j.biopha.2024.116752. Epub 2024 May 17.

Abstract

The gut microbiota has been reported to be perturbed by chemotherapeutic agents and to modulate side effects. However, the critical role of β-hydroxybutyrate (BHB) in the regulation of the gut microbiota and the pathogenesis of chemotherapeutic agents related nephrotoxicity remains unknown. We conducted a comparative analysis of the composition and function of gut microbiota in healthy, cisplatin-challenged, BHB-treated, and high-fat diet-treated mice using 16 S rDNA gene sequencing. To understand the crucial involvement of intestinal flora in BHB's regulation of cisplatin -induced nephrotoxicity, we administered antibiotics to deplete the gut microbiota and performed fecal microbiota transplantation (FMT) before cisplatin administration. 16 S rDNA gene sequencing analysis demonstrated that both endogenous and exogenous BHB restored gut microbiota dysbiosis and cisplatin-induced intestinal barrier disruption in mice. Additionally, our findings suggested that the LPS/TLR4/NF-κB pathway was responsible for triggering renal inflammation in the gut-kidney axis. Furthermore, the ablation of the gut microbiota ablation using antibiotics eliminated the renoprotective effects of BHB against cisplatin-induced acute kidney injury. FMT also confirmed that administration of BHB-treated gut microbiota provided protection against cisplatin-induced nephrotoxicity. This study elucidated the mechanism by which BHB affects the gut microbiota mediation of cisplatin-induced nephrotoxicity by inhibiting the inflammatory response, which may help develop novel therapeutic approaches that target the composition of the microbiota.

Keywords: Acute kidney injury; Cisplatin; Gut microbiota; Inflammation; β-hydroxybutyrate.

MeSH terms

  • 3-Hydroxybutyric Acid* / pharmacology
  • Acute Kidney Injury* / chemically induced
  • Acute Kidney Injury* / prevention & control
  • Animals
  • Anti-Bacterial Agents / adverse effects
  • Anti-Bacterial Agents / pharmacology
  • Antineoplastic Agents / adverse effects
  • Antineoplastic Agents / toxicity
  • Cisplatin* / adverse effects
  • Diet, High-Fat / adverse effects
  • Dysbiosis* / chemically induced
  • Fecal Microbiota Transplantation
  • Gastrointestinal Microbiome* / drug effects
  • Kidney / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • NF-kappa B / metabolism
  • Protective Agents / pharmacology
  • Toll-Like Receptor 4 / metabolism

Substances

  • Cisplatin
  • 3-Hydroxybutyric Acid
  • NF-kappa B
  • Toll-Like Receptor 4
  • Protective Agents
  • Anti-Bacterial Agents
  • Antineoplastic Agents