Fucoidan reduces NET accumulation and alleviates chemotherapy-induced peripheral neuropathy via the gut-blood-DRG axis

J Neuroinflammation. 2025 Apr 4;22(1):100. doi: 10.1186/s12974-025-03431-5.

Abstract

Background: Chemotherapy-induced peripheral neuropathy (CIPN) is a serious adverse reaction to chemotherapy with limited treatment options. Research has indicated that neutrophil extracellular traps (NETs) are critical for the pathogenesis of CIPN. LPS/HMGB1 serve as important inducers of NETs. Here, we aimed to target the inhibition of NET formation (NETosis) to alleviate CIPN.

Methods: Oxaliplatin (L-OHP) was used to establish a CIPN model. The mice were pretreated with fucoidan to investigate the therapeutic effect. SR-A1-/- mice were used to examine the role of scavenger receptor A1 (SR-A1) in CIPN. Bone marrow-derived macrophages (BMDMs) isolated from SR-A1-/- mice and WT mice were used to investigate the mechanism by which macrophage phagocytosis of NETs alleviates CIPN.

Results: Clinically, we found that the contents of LPS, HMGB1 and NETs in the plasma of CIPN patients were significantly increased and positively correlated with the VAS score. Fucoidan decreased the LPS/HMGB1/NET contents and relieved CIPN in mice. Mechanistically, fucoidan upregulated SR-A1 expression and promoted the phagocytosis of LPS/HMGB1 by BMDMs. Fucoidan also facilitated the engulfment of NETs by BMDMs via the recognition and localization of SR-A1 and HMGB1. The therapeutic effects of fucoidan were abolished by SR-A1 knockout. RNA-seq analysis revealed that fucoidan increased sqstm1 (p62) gene expression. Fucoidan promoted the competitive binding of sqstm1 and Nrf2 to Keap1, increasing Nrf2 nuclear translocation and SR-A1 transcription. Additionally, the sequencing analysis (16 S) of microbial diversity revealed that fucoidan increased the gut microbiota diversity and abundance and increased the Bacteroides/Firmicutes ratio.

Conclusions: Altogether, fucoidan promotes the SR-A1-mediated phagocytosis of LPS/HMGB1/NETs and maintains gut microbial homeostasis, which may provide a potential therapeutic strategy for CIPN.

Keywords: CIPN; Fucoidan; Gut; Macrophage; NETs; SR-A1.

MeSH terms

  • Animals
  • Antineoplastic Agents* / adverse effects
  • Antineoplastic Agents* / toxicity
  • Extracellular Traps* / drug effects
  • Extracellular Traps* / metabolism
  • Female
  • HMGB1 Protein / blood
  • Humans
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oxaliplatin / toxicity
  • Peripheral Nervous System Diseases* / chemically induced
  • Peripheral Nervous System Diseases* / drug therapy
  • Peripheral Nervous System Diseases* / metabolism
  • Phagocytosis / drug effects
  • Polysaccharides* / pharmacology
  • Polysaccharides* / therapeutic use
  • Scavenger Receptors, Class A / genetics
  • Scavenger Receptors, Class A / metabolism

Substances

  • fucoidan
  • Polysaccharides
  • Oxaliplatin
  • Antineoplastic Agents
  • HMGB1 Protein
  • Scavenger Receptors, Class A