Immunoregulatory Siglec ligands are abundant in human and mouse aorta and are up-regulated by high glucose

Life Sci. 2019 Jan 1:216:189-199. doi: 10.1016/j.lfs.2018.11.049. Epub 2018 Nov 22.

Abstract

Aim: Inflammation is a driving force in development of atherosclerosis, and hyperglycemia is a significant risk factor for angiopathy. Siglec-9, expressed on human neutrophils and macrophages, engages specific glycan ligands on tissues to diminish ongoing inflammation.

Materials and method: Siglec-9 ligands on human aorta were characterized and the effects of high glucose exposure on the expression of ligands for Siglec-9 on human umbilical vein endothelial cells (HUV-EC-C) in vitro and ligands for the comparable siglec (Siglec-E) on mouse aorta in vivo were studied.

Key findings: Siglec-9 ligands were expressed broadly on human aorta, as well as on HUV-EC-C. Siglec-9 ligands on HUV-EC-C were sharply up-regulated under high glucose exposure in vitro, as were Siglec-E ligands on the aortas of hyperglycemic mice. Exposure of HUV-EC-C to high-glucose resulted in consistent inhibitory changes in co-cultured macrophages including increased apoptosis and decreased phagocytosis. Control of Siglec-9 ligand expression on HUV-EC-C was downstream of changes in an enzyme involved in their biosynthesis, UDP-galactose-4-epimerase (GALE) and increased cellular N-acetylgalactosamine. The alteration of GALE was associated with the regulatory microRNA hsa-let-7f.

Significance: We conclude that exposure to high-glucose results in up-regulation of immune inhibitory Siglec-9 sialoglycan ligands on aorta and HUV-EC-C cells downstream of altered GALE and GalNAc expression, resulting in up-regulation of apoptosis and decrease of phagocytic activity of macrophages. Changes in Siglec-9 sialoglycan ligand expression on vascular endothelial cells may be a natural response to the initial steps of atherosclerosis and might be a potential target to regulate inflammation in diabetic angiopathy.

Keywords: Endothelial cells; High glucose; Inflammation; Siglec-9 ligands; UDP-galactose-4-epimerase.

MeSH terms

  • Animals
  • Antigens, CD / immunology
  • Antigens, CD / metabolism*
  • Antigens, Differentiation, B-Lymphocyte / immunology
  • Antigens, Differentiation, B-Lymphocyte / metabolism
  • Aorta / immunology
  • Aorta / metabolism*
  • Apoptosis / immunology*
  • Glucose / metabolism*
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Ligands
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Sialic Acid Binding Immunoglobulin-like Lectins / immunology
  • Sialic Acid Binding Immunoglobulin-like Lectins / metabolism*
  • UDPglucose 4-Epimerase / metabolism
  • Up-Regulation

Substances

  • Antigens, CD
  • Antigens, Differentiation, B-Lymphocyte
  • Ligands
  • SIGLEC9 protein, human
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • Siglece protein, mouse
  • UDPglucose 4-Epimerase
  • Glucose