Hepatic expression of lipopolysaccharide-binding protein (Lbp) is induced by the gut microbiota through Myd88 and impairs glucose tolerance in mice independent of obesity

Mol Metab. 2020 Jul:37:100997. doi: 10.1016/j.molmet.2020.100997. Epub 2020 Apr 16.

Abstract

Objective: Gut-derived inflammatory factors can impair glucose homeostasis, but the underlying mechanisms are not fully understood. In this study, we investigated how hepatic gene expression is regulated by gut colonization status through myeloid differentiation primary response 88 (MYD88) and how one of the regulated genes, lipopolysaccharide-binding protein (Lbp), affects insulin signaling and systemic glucose homeostasis.

Methods: Liver transcriptomics analysis was conducted on four groups of mice fed a chow diet: conventionally raised (CONV-R) wild-type, germ-free (GF) wild-type, CONV-R Myd88 KO, and GF Myd88 KO. Primary hepatocytes were exposed to combinations of lipopolysaccharide (LPS), LBP, and the LBP-blocking peptide LBPK95A, and the effect on insulin signaling was determined. To assess how LBP affects glucose metabolism in vivo, two mouse models were applied: treatment with LBPK95A and hepatic knockdown of Lbp using CRISPR-CAS9.

Results: We showed that the colonization status regulates gene expression in the liver and that a subset of these genes, including Lbp, is regulated through MYD88. Furthermore, we demonstrated that LBP impairs insulin signaling in hepatocytes in the presence of low levels of LPS and that the effect of LBP is abolished by LBPK95A. We showed that both systemic pharmacological blocking of LBP by LBPK95A and CRISPR-CAS9-mediated downregulation of hepatic Lbp improve glucose homeostasis.

Conclusions: Our results demonstrate that the gut microbiota regulates hepatic expression of Lbp through MYD88-dependent signaling. LBP potentiates LPS inhibition of insulin signaling in vitro and impairs systemic glucose homeostasis in vivo.

Keywords: CRISR-CAS9; Glucose metabolism; Gut microbiota; Lipopolysaccharide-binding protein; Liver; MYD88.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute-Phase Proteins / genetics
  • Acute-Phase Proteins / metabolism*
  • Animals
  • Carbohydrate Metabolism / physiology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Gastrointestinal Microbiome / genetics
  • Gastrointestinal Microbiome / physiology
  • Gene Expression
  • Glucose / metabolism*
  • Glucose Tolerance Test
  • Hepatocytes / metabolism
  • Inflammation / metabolism
  • Lipopolysaccharides / metabolism
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Myeloid Differentiation Factor 88 / metabolism*
  • Myeloid Differentiation Factor 88 / pharmacology
  • Myeloid Differentiation Factor 88 / physiology
  • Obesity / metabolism
  • Obesity / physiopathology
  • Signal Transduction

Substances

  • Acute-Phase Proteins
  • Carrier Proteins
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • lipopolysaccharide-binding protein
  • Glucose