Impairment of Hematopoietic Precursor Cell Activation during the Granulopoietic Response to Bacteremia in Mice with Chronic-Plus-Binge Alcohol Administration

Infect Immun. 2017 Oct 18;85(11):e00369-17. doi: 10.1128/IAI.00369-17. Print 2017 Nov.

Abstract

Alcohol abuse impairs immune defense. To study the effect of chronic-plus-binge alcohol exposure on the granulopoietic response, acute alcohol intoxication (intraperitoneal injection of 5 g alcohol/kg body weight) was introduced to mice chronically fed on the Lieber-DeCarli low-fat liquid alcohol diet for 5 weeks. Bacteremia was induced by intravenous injection of Escherichia coli Bacteremia caused a remarkable increase in marrow lin- c-kit+ Sca-1+ cells. Activation of cell proliferation supported the increase in marrow lin- c-kit+ Sca-1+ cells. Alcohol administration inhibited this activation of lin- c-kit+ Sca-1+ cells. The bone marrow of pair-fed control mice receiving intraperitoneal saline stored a large number of mature granulocytes expressing a high level of Gr1 (Gr1hi cells). The proportion of Gr1hi cells and the total number of Gr1+ cells were markedly reduced in the bone marrow, along with an increase in the ratio of Gr1+ granulocytes in peripheral white blood cells following bacteremia. E. coli infection stimulated proliferation of granulopoietic precursor cells, resulting in a marked increase in the ratio of immature Gr1lo cells in the bone marrow. Alcohol administration itself triggered marrow release of Gr1+ cells, resulting in reduction of the marrow granulocyte reserve with an elevation of granulocytes in the circulation. Alcohol also impaired activation of granulopoietic precursor proliferation following bacteremia. Alcohol disrupted lipopolysaccharide (LPS)-TLR4-ERK1/2-cyclin D1 signaling and inhibited upregulation of Sca-1 and C/EBPβ expression by lineage-negative marrow cells in response to bacteremia. These results indicate that chronic-plus-binge alcohol exposure inhibits the granulopoietic response by disrupting key cell signaling for hematopoietic precursor cell activation and commitment to granulocyte lineage development.

Keywords: Alcohol; bacteremia; cell signaling; granulocytes; granulopoietic response; stem cells.

MeSH terms

  • Animals
  • Antigens, Ly / genetics
  • Antigens, Ly / immunology
  • Bacteremia / genetics
  • Bacteremia / immunology*
  • Bacteremia / pathology
  • Binge Drinking / genetics
  • Binge Drinking / immunology*
  • Binge Drinking / pathology
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / pathology
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / immunology
  • Cyclin D1 / genetics
  • Cyclin D1 / immunology
  • Disease Models, Animal
  • Escherichia coli / growth & development
  • Escherichia coli / immunology
  • Escherichia coli Infections / genetics
  • Escherichia coli Infections / immunology*
  • Escherichia coli Infections / pathology
  • Ethanol / pharmacology*
  • Gene Expression Regulation / drug effects*
  • Gene Expression Regulation / immunology
  • Granulocytes / drug effects
  • Granulocytes / immunology
  • Granulocytes / pathology
  • Hematopoiesis / drug effects*
  • Hematopoiesis / genetics
  • Hematopoiesis / immunology
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / immunology
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / immunology
  • Nucleotidyltransferases / deficiency
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / immunology
  • Proto-Oncogene Proteins c-kit / genetics
  • Proto-Oncogene Proteins c-kit / immunology
  • Signal Transduction / drug effects*
  • Signal Transduction / immunology
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology

Substances

  • Antigens, Ly
  • CCAAT-Enhancer-Binding Protein-beta
  • Ccnd1 protein, mouse
  • Cebpb protein, mouse
  • Ly6G antigen, mouse
  • Ly6a protein, mouse
  • Membrane Proteins
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Cyclin D1
  • Ethanol
  • Proto-Oncogene Proteins c-kit
  • Mapk1 protein, mouse
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Nucleotidyltransferases
  • lincosaminide O-nucleotidyltransferase