Alcohol-related changes in the intestinal microbiome influence neutrophil infiltration, inflammation and steatosis in early alcoholic hepatitis in mice

PLoS One. 2017 Mar 28;12(3):e0174544. doi: 10.1371/journal.pone.0174544. eCollection 2017.

Abstract

Background: Alcohol-induced intestinal dysbiosis disrupts homeostatic gut-liver axis function and is essential in the development of alcoholic liver disease. Here, we investigate changes in enteric microbiome composition in a model of early alcoholic steatohepatitis and dissect the pathogenic role of intestinal microbes in alcohol-induced liver pathology.

Materials and methods: Wild type mice received a 10-day diet that was either 5% alcohol-containing or an isocaloric control diet plus a single binge. 16S rDNA sequencing defined the bacterial communities in the cecum of alcohol- and pair-fed animals. Some mice were treated with an antibiotic cocktail prior to and throughout alcohol feeding. Liver neutrophils, cytokines and steatosis were evaluated.

Results: Acute-on-chronic alcohol administration induced shifts in various bacterial phyla in the cecum, including increased Actinobacteria and a reduction in Verrucomicrobia driven entirely by a reduction in the genus Akkermansia. Antibiotic treatment reduced the gut bacterial load and circulating bacterial wall component lipopolysaccharide (LPS). We found that bacterial load suppression prevented alcohol-related increases in the number of myeloperoxidase- (MPO) positive infiltrating neutrophils in the liver. Expression of liver mRNA tumor necrosis factor alpha (Tnfα), C-X-C motif chemokine ligand 1 (Cxcl1) and circulating protein monocyte chemoattractant protein-1 (MCP-1) were also reduced in antibiotic-treated alcohol-fed mice. Alcohol-induced hepatic steatosis measured by Oil-Red O staining was significantly reduced in antibiotic treated mice. Genes regulating lipid production and storage were also altered by alcohol and antibiotic treatment. Interestingly, antibiotic treatment did not protect from alcohol-induced increases in serum aminotransferases (ALT/AST).

Conclusions: Our data indicate that acute-on-chronic alcohol feeding alters the microflora at multiple taxonomic levels and identifies loss of Akkermansia as an early marker of alcohol-induced gut dysbiosis. We conclude that gut microbes influence liver inflammation, neutrophil infiltration and liver steatosis following alcohol consumption and these data further emphasize the role of the gut-liver axis in early alcoholic liver disease.

MeSH terms

  • Animals
  • Anti-Bacterial Agents / administration & dosage
  • Anti-Bacterial Agents / pharmacology
  • Bacteria / classification
  • Bacteria / drug effects
  • Bacteria / genetics
  • Central Nervous System Depressants / administration & dosage
  • Central Nervous System Depressants / toxicity
  • Ethanol / administration & dosage
  • Ethanol / toxicity
  • Fatty Liver / chemically induced
  • Fatty Liver / genetics*
  • Fatty Liver, Alcoholic / etiology
  • Fatty Liver, Alcoholic / genetics
  • Female
  • Gastrointestinal Microbiome / drug effects
  • Gastrointestinal Microbiome / genetics*
  • Gene Expression / drug effects
  • Hepatitis, Alcoholic / etiology
  • Hepatitis, Alcoholic / genetics*
  • Inflammation / chemically induced
  • Inflammation / genetics*
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Mice, Inbred C57BL
  • Neutrophil Infiltration / drug effects
  • Neutrophil Infiltration / genetics*
  • RNA, Ribosomal, 16S / genetics
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Anti-Bacterial Agents
  • Central Nervous System Depressants
  • RNA, Ribosomal, 16S
  • Ethanol