Mesenchymal stem cells alleviate bacteria-induced liver injury in mice by inducing regulatory dendritic cells

Hepatology. 2014 Feb;59(2):671-82. doi: 10.1002/hep.26670. Epub 2013 Dec 20.

Abstract

Fulminant hepatic failure (FHF) is a clinical syndrome characterized by sudden and severe impairment of liver function. Mesenchymal stem cells (MSCs) have been proposed as a promising therapeutic approach for FHF. In this study we used Propionibacterium acnes (P. acnes)-primed, lipopolysaccharide (LPS)-induced liver injury in mice as an animal model of human FHF. We demonstrated that administration of MSCs significantly ameliorated liver injury and improved the survival rates of mice subjected to P. acnes plus LPS-induced FHF. Allogeneic MSCs showed similar treatment efficacy as autologous MSCs did in FHF. Treatment efficacy of MSCs could be attributed to decreased infiltration and activation of CD4(+) T cells in the liver, inhibition of T helper 1 cells, and induction of regulatory T cells (Tregs). Moreover, decreased DNA copies of P. acnes were detected in the liver of MSC-treated mice. Intriguingly, a distinct liver population of CD11c(+) MHCII(hi) CD80(lo) CD86(lo) regulatory dendritic cells (DCs) was induced by MSCs. Moreover, these DCs induced Treg differentiation through transforming growth factor-β production. Further mechanistic studies demonstrated that MSC-derived prostaglandin E2 and one of its receptors, EP4, played essential roles in the differentiation of CD11c(+) B220(-) DC precursors into regulatory DCs in a phosphoinositide 3-kinase-dependent manner.

Conclusion: MSCs induce regulatory DCs from CD11c(+) B220(-) DC precursors. This study elucidates an immunoregulatory mechanism of MSCs and lays a foundation for application of MSCs in FHF therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell- and Tissue-Based Therapy
  • Dendritic Cells / metabolism
  • Dendritic Cells / pathology*
  • Disease Models, Animal
  • Gram-Positive Bacterial Infections / complications*
  • Lipopolysaccharides / adverse effects
  • Liver / metabolism
  • Liver / pathology
  • Liver Failure, Acute / chemically induced
  • Liver Failure, Acute / microbiology*
  • Liver Failure, Acute / therapy*
  • Mesenchymal Stem Cell Transplantation*
  • Mesenchymal Stem Cells / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Propionibacterium acnes*
  • Receptors, Prostaglandin E, EP4 Subtype / metabolism
  • Signal Transduction
  • T-Lymphocytes, Regulatory / metabolism
  • T-Lymphocytes, Regulatory / pathology
  • Th1 Cells / metabolism
  • Th1 Cells / pathology
  • Transforming Growth Factor beta / metabolism

Substances

  • Lipopolysaccharides
  • Ptger4 protein, mouse
  • Receptors, Prostaglandin E, EP4 Subtype
  • Transforming Growth Factor beta