Exostosin 1/Exostosin 2-Associated Membranous Nephropathy

J Am Soc Nephrol. 2019 Jun;30(6):1123-1136. doi: 10.1681/ASN.2018080852. Epub 2019 May 6.

Abstract

Background: In membranous nephropathy (MN), which is characterized by deposition of immune complexes along the glomerular basement membrane (GBM), phospholipase A2 receptor (PLA2R) and thrombospondin type 1 domain-containing 7A are target antigens in approximately 70% and 1%-5% of cases of primary MN, respectively. In other cases of primary MN and in secondary MN, the target antigens are unknown.

Methods: We studied 224 cases of biopsy-proven PLA2R-negative MN and 102 controls (including 47 cases of PLA2R-associated MN) in pilot and discovery cohorts. We also evaluated 48 cases of PLA2R-negative presumed primary MN and lupus MN in a validation cohort. We used laser microdissection and mass spectrometry to identify new antigens, which were localized by immunohistochemistry.

Results: Mass spectrometry detected exostosin 1 (EXT1) and exostosin 2 (EXT2) in 21 cases of PLA2R-negative MN, but not in PLA2R-associated MN and control cases. Immunohistochemistry staining revealed bright granular GBM staining for EXT1 and EXT2. Clinical and biopsy findings showed features of autoimmune disease, including lupus, in 80.7% of the 26 EXT1/EXT2-associated MN cases we identified. In the validation cohort, we confirmed that EXT1/EXT2 staining was detected in pure class 5 lupus nephritis (eight of 18 patients) and in presumed primary MN associated with signs of autoimmunity (three of 16 patients); only one of the 14 cases of mixed class 5 and 3/4 lupus nephritis was positive for EXT1/EXT2. Tests in seven patients with EXT1/EXT2-associated MN found no circulating anti-exostosin antibodies.

Conclusions: A subset of MN is associated with accumulation of EXT1 and EXT2 in the GBM. Autoimmune disease is common in this group of patients.

Keywords: Immunology and pathology; membranous nephropathy; nephrotic syndrome.

Publication types

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

MeSH terms

  • Adult
  • Autoantibodies / immunology
  • Biopsy, Needle
  • Blotting, Western
  • Case-Control Studies
  • Disease Progression
  • Female
  • Follow-Up Studies
  • Glomerulonephritis, Membranous / immunology*
  • Glomerulonephritis, Membranous / pathology*
  • Humans
  • Immunohistochemistry
  • Male
  • Mass Spectrometry
  • N-Acetylglucosaminyltransferases / immunology*
  • Pilot Projects
  • Receptors, Phospholipase A2 / metabolism*
  • Reference Values
  • Risk Assessment
  • Severity of Illness Index

Substances

  • Autoantibodies
  • PLA2R1 protein, human
  • Receptors, Phospholipase A2
  • N-Acetylglucosaminyltransferases
  • exostosin-1
  • exostosin-2