CX3CR1-expressing inflammatory dendritic cells contribute to the progression of steatohepatitis

Clin Sci (Lond). 2015 Nov;129(9):797-808. doi: 10.1042/CS20150053. Epub 2015 Jun 25.

Abstract

Liver monocytes play a major role in the development of NASH (non-alcoholic steatohepatitis). In inflamed tissues, monocytes can differentiate in both macrophages and dendritic cells. In the present study, we investigated the role of moDCs (monocyte-derived inflammatory dendritic cells) in experimental steatohepatitis induced in C57BL/6 mice by feeding on a MCD (methionine/choline-deficient) diet. The evolution of steatohepatitis was characterized by an increase in hepatic CD45+ / CD11b+ myeloid cells displaying the monocyte/macrophage marker F4-80(+). In the early phases (4 weeks of treatment), Ly6C(high)/CD11b(+)/F4-80(+) inflammatory macrophages predominated. However, their frequency did not grow further with the disease progression (8 weeks of treatment), when a 4-fold expansion of CD11b(+)/F4-80(+) cells featuring the fractalkine receptor (CX3CR1) was evident. These CX3CR1+ cells were also characterized by the combined expression of inflammatory monocyte (Ly6C, CD11b) and dendritic cell (CD11c, MHCII) markers as well as by a sustained TNFα (tumour necrosis factor α) production, suggesting monocyte differentiation into inflammatory moDCs. The expansion of TNFα-producing CX3CR1+ moDCs was associated with an elevation in hepatic and circulating TNFα level and with the worsening of parenchymal injury. Hydrogen sulfide (H2S) has been shown to interfere with CX3CR1 up-regulation in monocyte-derived cells exposed to pro-inflammatory stimuli. Treating 4-week-MCD-fed mice with the H2S donor NaHS while continuing on the same diet prevented the accumulation of TNFα-producing CX3CR1+ moDCs without interfering with hepatic macrophage functions. Furthermore, NaHS reduced hepatic and circulating TNFα levels and ameliorated transaminase release and parenchymal injury. Altogether, these results show that inflammatory CX3CR1+ moDCs contributed in sustaining inflammation and liver injury during steatohepatitis progression.

Keywords: CX3CR1; chronic inflammation; dendritic cells; liver fibrosis; macrophages; non-alcoholic fatty liver disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / immunology
  • Actins / metabolism
  • Animals
  • Antigens, Differentiation / genetics
  • Antigens, Differentiation / immunology
  • Antigens, Differentiation / metabolism
  • Antigens, Ly / genetics
  • CD11b Antigen / genetics
  • CD11b Antigen / immunology
  • CD11b Antigen / metabolism
  • CX3C Chemokine Receptor 1
  • Choline Deficiency
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Diet / adverse effects
  • Disease Progression
  • Flow Cytometry
  • Gene Expression / immunology
  • Immunohistochemistry
  • Inflammation / genetics
  • Inflammation / immunology*
  • Liver / drug effects
  • Liver / immunology
  • Liver / metabolism
  • Methionine / deficiency
  • Mice, Inbred C57BL
  • Monocytes / immunology
  • Monocytes / metabolism
  • Non-alcoholic Fatty Liver Disease / etiology
  • Non-alcoholic Fatty Liver Disease / genetics
  • Non-alcoholic Fatty Liver Disease / immunology*
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / immunology*
  • Receptors, Chemokine / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sulfides / metabolism
  • Sulfides / pharmacology
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / immunology
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Actins
  • Antigens, Differentiation
  • Antigens, Ly
  • CD11b Antigen
  • CX3C Chemokine Receptor 1
  • Cx3cr1 protein, mouse
  • Ly-6C antigen, mouse
  • Receptors, Chemokine
  • Sulfides
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • monocyte-macrophage differentiation antigen
  • Methionine
  • sodium bisulfide