Disruption of hepatocyte Sialylation drives a T cell-dependent pro-inflammatory immune tone

Glycoconj J. 2020 Jun;37(3):395-407. doi: 10.1007/s10719-020-09918-y. Epub 2020 Mar 28.

Abstract

Through the catalysis of α2,6-linked sialylation, the enzyme ST6Gal1 is thought to play key roles in immune cell communication and homeostasis. Of particular importance, glycans with terminal α2,6-sialic acids are known to negatively regulate B cell receptor signaling and are associated with an immunosuppressive tumor microenvironment that promotes T cell anergy, suggesting that α2,6-sialic acids are a key immune inhibitory signal. Consistent with this model, mice harboring a hepatocyte-specific ablation of ST6Gal1 (H-cKO) develop a progressive and severe non-alcoholic fatty liver disease characterized by steatohepatitis. Using this H-cKO mouse, we have further discovered that loss of hepatocyte α2,6-sialylation not only increases the inflammatory state of the local tissue microenvironment, but also systemic T cell-dependent immune responses. H-cKO mice responded normally to innate and passively induced inflammation, but showed significantly increased morbidity in T cell-dependent house dust mite-antigen (HDM)-induced asthma and myelin oligodendrocyte glycoprotein (MOG) peptide-induced experimental autoimmune encephalomyelitis (EAE). We further discovered that H-cKO mice have a profound shift toward effector/memory T cells even among unchallenged mice, and that macrophages from both the liver and spleen expressed the inhibitory and α2,6-sialic acid-specific glycan binding molecule CD22. These findings align with previously reported pro-inflammatory changes in liver macrophages, and support a model in which the liver microenvironment sets a systemic immune tone that is regulated by tissue α2,6-sialylation and mediated by liver macrophages and systemic T cells.

Keywords: Asthma; EAE; Glycobiology; IgG; Inflammation; Liver; Macrophage; ST6Gal1; Sialic acid; Sialylation; T cell.

Publication types

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

MeSH terms

  • Animals
  • Asthma / etiology
  • Asthma / immunology
  • Colitis / chemically induced
  • Colitis / immunology
  • Disease Models, Animal
  • Hepatocytes / immunology
  • Hepatocytes / metabolism*
  • Immunity, Innate / physiology*
  • Lipopolysaccharides / administration & dosage
  • Lipopolysaccharides / toxicity
  • Liver / immunology
  • Lung / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice, Knockout
  • Peritonitis / chemically induced
  • Peritonitis / immunology
  • Sialic Acid Binding Ig-like Lectin 2 / metabolism
  • Sialyltransferases / genetics
  • Sialyltransferases / metabolism*
  • T-Lymphocytes / immunology*
  • Thioglycolates / toxicity

Substances

  • Cd22 protein, mouse
  • Lipopolysaccharides
  • Sialic Acid Binding Ig-like Lectin 2
  • Thioglycolates
  • Sialyltransferases