Alcohol-induced miR-155 and HDAC11 inhibit negative regulators of the TLR4 pathway and lead to increased LPS responsiveness of Kupffer cells in alcoholic liver disease

J Leukoc Biol. 2017 Aug;102(2):487-498. doi: 10.1189/jlb.3A0716-310R. Epub 2017 Jun 5.

Abstract

Inflammation promotes the progression of alcoholic liver disease. Alcohol sensitizes KCs to gut-derived endotoxin (LPS); however, signaling pathways that perpetuate inflammation in alcoholic liver disease are only partially understood. We found that chronic alcohol feeding in mice induced miR-155, an inflammatory miRNA in isolated KCs. We hypothesized that miR-155 might increase the responsiveness of KCs to LPS via targeting the negative regulators of LPS signaling. Our results revealed that KCs that were isolated from alcohol-fed mice showed a decrease in IRAK-M, SHIP1, and PU.1, and an increase in TNF-α levels. This was specific to KCs, as no significant differences were observed in these genes in hepatocytes. We found a causal effect of miR-155 deficiency on LPS responsiveness, as KCs that were isolated from miR-155 KO mice showed a greater induction of IRAK-M, SHIP1, and suppressor of cytokine signaling 1 after LPS treatment. C/EBPβ, a validated miR-155 target, stimulates IL-10 transcription. We found a higher induction of C/EBPβ and IL-10 in KCs that were isolated from miR-155 KO mice after LPS treatment. Gain- and loss-of-function studies affirmed that alcohol-induced miR-155 directly regulates IRAK-M, SHIP1, suppressor of cytokine signaling 1, and C/EBPβ, as miR-155 inhibition increased and miR-155 overexpression decreased these genes in LPS or alcohol-pretreated wild-type KCs. HDAC11, a regulator of IL-10, was significantly increased and IL-10 was decreased in KCs that were isolated from alcohol-fed mice. Functionally, knockdown of HDAC11 with small interfering RNA resulted in an IL-10 increase in LPS or alcohol-pretreated Mϕ. We found that acetaldehyde and NF-κB pathways regulate HDAC11 levels. Collectively, our results indicate that the alcohol-induced responsiveness of KCs to LPS, in part, is governed by miR-155 and HDAC11.

Keywords: HDAC11; IRAK-M; MyD88; TNF-α; miR-155.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Blotting, Western
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Gene Expression Regulation / immunology*
  • Gene Knockdown Techniques
  • Histone Deacetylases / metabolism*
  • Inflammation / immunology
  • Inflammation / metabolism
  • Kupffer Cells / immunology
  • Kupffer Cells / metabolism*
  • Lipopolysaccharides / immunology
  • Lipopolysaccharides / toxicity
  • Liver Diseases, Alcoholic / immunology
  • Liver Diseases, Alcoholic / metabolism*
  • Liver Diseases, Alcoholic / pathology
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / metabolism*
  • RAW 264.7 Cells
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / immunology
  • Toll-Like Receptor 4 / immunology
  • Toll-Like Receptor 4 / metabolism

Substances

  • Lipopolysaccharides
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Hdac11 protein, mouse
  • Histone Deacetylases