SPIONs enhances IL-10-producing macrophages to relieve sepsis via Cav1-Notch1/HES1-mediated autophagy

Int J Nanomedicine. 2019 Aug 23:14:6779-6797. doi: 10.2147/IJN.S215055. eCollection 2019.

Abstract

Background: Sepsis is a life-threatening condition caused by dysregulated host responses to infection. Macrophages, which recognize microbial infections through identification of bacterial markers such as lipopolysaccharide (LPS), are crucial to the pathogenesis of sepsis-associated liver injury. However, the understanding of the SPIONs-mediated modulation of macrophage responses in LPS-induced sepsis and liver injury is limited.

Materials and methods: Superparamagnetic iron oxide nanoparticles (SPIONs) of γ-Fe2O3 nanoparticles were prepared, and their morphology and magnetic properties were characterized.

Results: Using a murine model of LPS-induced sepsis and liver injury, we found that SPIONs alleviated LPS-induced sepsis, preventing infiltration of inflammatory cells into the liver. SPIONs also increased the level of interleukin-10 (IL-10) in liver macrophages, while SPIONs's effect on LPS-induced sepsis was abrogated in IL-10-/- mice, indicating that the protective effect of SPIONs is dependent on IL-10+ macrophages. Moreover, SPIONs activated macrophage autophagy to increase IL-10 production, which was markedly attenuated by autophagy inhibition. Furthermore, SPIONs upregulated the expression of Caveolin-1 (Cav1) in macrophages, which plays a role in cellular uptake of metallic nanoparticles. Interestingly, activation of Cav1 and Notch1/HES1 signaling was involved in SPIONs-induced autophagy in both RAW 264.7 cells and bone marrow-derived macrophages (BMDMs). Our data reveal a novel mechanism for SPIONs -induced autophagy in macrophages, which occurs through activation of the Cav1-Notch1/HES1 signaling pathway, which promotes the production of IL-10 in macrophages, leading to inhibition of inflammation in LPS-induced sepsis and liver injury.

Conclusion: Our results suggest that SPIONs may represent a potential therapeutic agent for the treatment of sepsis and sepsis-induced liver injury.

Keywords: IL-10; SPIONs; autophagy; liver injury; sepsis.

MeSH terms

  • Animals
  • Autophagy / drug effects*
  • Autophagy / physiology
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism
  • Ferric Compounds / chemistry
  • Ferric Compounds / pharmacology
  • Interleukin-10 / metabolism
  • Lipopolysaccharides / toxicity
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Macrophages / pathology
  • Magnetite Nanoparticles / chemistry
  • Magnetite Nanoparticles / therapeutic use*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • RAW 264.7 Cells
  • Receptor, Notch1 / metabolism
  • Sepsis / drug therapy*
  • Sepsis / metabolism
  • Sepsis / pathology
  • Transcription Factor HES-1 / metabolism

Substances

  • Cav1 protein, mouse
  • Caveolin 1
  • Ferric Compounds
  • Hes1 protein, mouse
  • IL10 protein, mouse
  • Lipopolysaccharides
  • Magnetite Nanoparticles
  • Notch1 protein, mouse
  • Receptor, Notch1
  • Transcription Factor HES-1
  • Interleukin-10
  • ferric oxide