Immunopathological analysis of the expression of glomerular exostosin 1 and exostosin 2 in Japanese patients with lupus nephritis

Virchows Arch. 2021 Nov;479(5):997-1005. doi: 10.1007/s00428-021-03164-9. Epub 2021 Jul 24.

Abstract

Exostosin 1 and exostosin 2 (EXT1/EXT2) on glomerular basement membrane (GBM) were recently reported as novel putative antigens in secondary membranous nephropathy with autoimmune disease. However, the clinical significance of glomerular EXT1/EXT2 remains elusive in patients with lupus nephritis (LN). The immunofluorescence staining pattern of glomerular EXT1/EXT2 is also undetermined in membranous LN (MLN) or proliferative LN (PLN). We cross-sectionally analyzed patients with MLN (pure class V, n = 11) and PLN (class III, IV, and mixed class III/IV + V, n = 22) who underwent renal biopsies between 2010 and 2020 at Showa University Hospital. Glomerular EXT1/EXT2 expressions were evaluated by immunofluorescence. T-helper (Th) cell-related serum inflammatory cytokines were measured using enzyme-linked immunosorbent assay. The positivity for both EXT1/EXT2 was higher in patients with MLN than PLN (90.9% vs 63.6%, P = 0.212). MLN showed global and bright granular EXT1/EXT2 expressions along GBM, while PLN showed segmental and moderate expressions on GBM. Additionally, glomerular EXT1/EXT2 positivity was not associated with the degree of proteinuria or renal function in MLN and PLN patients, but the levels of serum anti-dsDNA antibody and circulating immune complexes were lower in patients with EXT1/EXT2-positive MLN than EXT1/EXT2-negative PLN. Moreover, serum complement levels and IL-4/IFN-γ ratios were elevated in EXT1/EXT2-positive MLN than EXT1/EXT2-negative PLN. Collectively, immunofluorescence staining for glomerular EXT1/EXT2 had characteristic patterns between MLN and PLN. Glomerular EXT1/EXT2 expressions tended to be high in Th2-dominant MLN patients without severe hypocomplementemia and elevated autoantibodies. Thus, EXT1/EXT2 might be involved in the unique developmental mechanism of MLN.

Keywords: Exostosin 1; Exostosin 2; Membranous lupus nephritis; Proliferative lupus nephritis; T-helper type 2.

MeSH terms

  • Adult
  • Antibodies, Antinuclear / blood
  • Antigen-Antibody Complex / blood
  • Biomarkers / blood
  • Biopsy
  • Cross-Sectional Studies
  • Cytokines / blood
  • Female
  • Humans
  • Immunohistochemistry*
  • Inflammation Mediators / blood
  • Japan
  • Kidney Glomerulus / chemistry*
  • Kidney Glomerulus / pathology
  • Lupus Nephritis / immunology
  • Lupus Nephritis / metabolism*
  • Lupus Nephritis / pathology
  • Male
  • Middle Aged
  • N-Acetylglucosaminyltransferases / analysis*
  • Predictive Value of Tests
  • T-Lymphocytes, Helper-Inducer / immunology
  • T-Lymphocytes, Helper-Inducer / metabolism

Substances

  • Antibodies, Antinuclear
  • Antigen-Antibody Complex
  • Biomarkers
  • Cytokines
  • Inflammation Mediators
  • N-Acetylglucosaminyltransferases
  • exostosin-1
  • exostosin-2