CXCR2 Activated JAK3/STAT3 Signaling Pathway Exacerbating Hepatotoxicity Associated with Tacrolimus

Drug Des Devel Ther. 2024 Dec 28:18:6331-6344. doi: 10.2147/DDDT.S496195. eCollection 2024.

Abstract

Purpose: Tacrolimus could induce hepatotoxicity during clinical use, and the mechanism was still unclear, which posed new challenge for the prevention and treatment of tacrolimus-induced hepatotoxicity. The aim of this study was to investigate the mechanism of tacrolimus-induced hepatotoxicity and provide reference for drug development target.

Methods: In this study, biochemical analysis, pathological staining, immunofluorescent staining, immunohistochemical staining, transcriptomic analysis, Western blotting was used to investigate the mechanism of tacrolimus-induced hepatotoxicity in gene knockout mice and Wistar rats.

Results: In gene knockout mice, compared to wild-type mice, CXCR2-deficiency alleviated tacrolimus-induced hepatotoxicity (P < 0.05 or P < 0.01). In Wistar rats, compared to control group, CXCL2-CXCR2, JAK3/STAT3 signaling pathway (phosphorylation of JAK3 and STAT3) were up-regulated, the expression of CIS was lowered and the expression of PIM1 was raised, inducing liver pathological change (P < 0.05 or P < 0.01); Inversely, blocking CXCR2 could reverse the expression of p-JAK3/p-STAT3 and tacrolimus-induced hepatotoxicity (P < 0.05 or P < 0.01).

Conclusion: CXCR2 activated JAK3/STAT3 signaling pathway (phosphorylation of JAK3 and STAT3) exacerbating hepatotoxicity associated with tacrolimus, meanwhile the expression of CIS was down-regulated, the expression of PIM1 was up-regulated. Blocking CXCR2 could reverse the expression of p-JAK3/p-STAT3, CIS, PIM1, and tacrolimus-induced hepatotoxicity.

Keywords: CIS; CXCR2; JAK3/STAT3 signaling pathway; PIM1; hepatotoxicity; tacrolimus.

MeSH terms

  • Animals
  • Chemical and Drug Induced Liver Injury* / metabolism
  • Chemical and Drug Induced Liver Injury* / pathology
  • Janus Kinase 3* / antagonists & inhibitors
  • Janus Kinase 3* / metabolism
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Rats
  • Rats, Wistar*
  • Receptors, Interleukin-8B* / antagonists & inhibitors
  • Receptors, Interleukin-8B* / metabolism
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction* / drug effects
  • Tacrolimus* / pharmacology
  • Tacrolimus* / toxicity

Substances

  • STAT3 Transcription Factor
  • Tacrolimus
  • Janus Kinase 3
  • Receptors, Interleukin-8B
  • Jak3 protein, mouse
  • Stat3 protein, mouse

Grants and funding

This work was supported by The Natural Science Foundation of Jiangsu Province (No. BK20241046), The Xuzhou Special Fund for Promoting Scientific and Technological Innovation (No. KC23254), The Medical Research Project of Jiangsu Provincial Health Commission (No. Z2023010).