Essential role and therapeutic targeting of the glomerular endothelial glycocalyx in lupus nephritis

JCI Insight. 2020 Oct 2;5(19):e131252. doi: 10.1172/jci.insight.131252.

Abstract

Lupus nephritis (LN) is a major organ complication and cause of morbidity and mortality in patients with systemic lupus erythematosus (SLE). There is an unmet medical need for developing more efficient and specific, mechanism-based therapies, which depends on improved understanding of the underlying LN pathogenesis. Here we present direct visual evidence from high-power intravital imaging of the local kidney tissue microenvironment in mouse models showing that activated memory T cells originated in immune organs and the LN-specific robust accumulation of the glomerular endothelial glycocalyx played central roles in LN development. The glomerular homing of T cells was mediated via the direct binding of their CD44 to the hyaluronic acid (HA) component of the endothelial glycocalyx, and glycocalyx-degrading enzymes efficiently disrupted homing. Short-course treatment with either hyaluronidase or heparinase III provided long-term organ protection as evidenced by vastly improved albuminuria and survival rate. This glycocalyx/HA/memory T cell interaction is present in multiple SLE-affected organs and may be therapeutically targeted for SLE complications, including LN.

Keywords: Lupus; Nephrology; T cells; endothelial cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Endothelium, Vascular / immunology*
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • Female
  • Glycocalyx / metabolism*
  • Hyaluronic Acid / metabolism
  • Hyaluronoglucosaminidase / administration & dosage*
  • Immunologic Memory / immunology
  • Kidney Glomerulus / immunology*
  • Kidney Glomerulus / metabolism
  • Kidney Glomerulus / pathology
  • Lupus Nephritis / immunology
  • Lupus Nephritis / metabolism
  • Lupus Nephritis / pathology
  • Lupus Nephritis / prevention & control*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Polysaccharide-Lyases / administration & dosage*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology

Substances

  • Hyaluronic Acid
  • Hyaluronoglucosaminidase
  • Polysaccharide-Lyases
  • heparitinsulfate lyase