A hydrophobic patch on proteinase 3, the target of autoantibodies in Wegener granulomatosis, mediates membrane binding via NB1 receptors

J Biol Chem. 2008 Dec 19;283(51):35976-82. doi: 10.1074/jbc.M806754200. Epub 2008 Oct 14.

Abstract

Proteinase 3 (PR3), the target antigen of antineutrophil cytoplasm autoantibodies, which are found in patients with Wegener granulomatosis, is a neutrophil serine protease localized within cytoplasmic granules. Recently, the human neutrophil antigen NB1 was identified as a specific neutrophil cell surface receptor of PR3. We hypothesized that the unique hydrophobic cluster of PR3 that is not present on human neutrophil elastase and cathepsin G and presumably is also missing in other human PR3 homologs accounts for its binding to the NB1 receptor expressed on the cellular surface of NB1 cells. Instead of generating and testing various artificial human PR3 mutants, we cloned and expressed the very closely related gibbon (Hylobates pileatus) PR3 homolog, which did not bind to the human NB1 receptor. Moreover, a human-gibbon hybrid constructed from the N- and C-terminal half of the human and gibbon PR3, respectively, also did not interact with human NB1. The C-terminal half of gibbon PR3 differs only by 9 residues from human PR3, among which four closely spaced hydrophobic residues are substituted in a nonconservative manner (F166L, W218R, G219A, and L223H). The NB1-bound PR3 was active and was cleared from the surface by alpha-1-protease inhibitor. Conformational distortion of the hydrophobic 217-225 loop by alpha-1-protease inhibitor most likely triggers rapid solubilization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Antineutrophil Cytoplasmic / genetics
  • Antibodies, Antineutrophil Cytoplasmic / immunology
  • Antibodies, Antineutrophil Cytoplasmic / metabolism
  • Cathepsin G
  • Cathepsins / genetics
  • Cathepsins / immunology
  • Cathepsins / metabolism
  • Cell Line
  • GPI-Linked Proteins
  • Granulomatosis with Polyangiitis / genetics
  • Granulomatosis with Polyangiitis / immunology
  • Granulomatosis with Polyangiitis / metabolism*
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Hylobates
  • Isoantigens / genetics
  • Isoantigens / immunology
  • Isoantigens / metabolism*
  • Leukocyte Elastase / genetics
  • Leukocyte Elastase / immunology
  • Leukocyte Elastase / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology
  • Membrane Glycoproteins / metabolism*
  • Myeloblastin / genetics
  • Myeloblastin / immunology
  • Myeloblastin / metabolism*
  • Protein Binding
  • Protein Structure, Secondary / genetics
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / immunology
  • Receptors, Cell Surface / metabolism*
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / immunology
  • Serine Endopeptidases / metabolism
  • Species Specificity

Substances

  • Antibodies, Antineutrophil Cytoplasmic
  • CD177 protein, human
  • GPI-Linked Proteins
  • Isoantigens
  • Membrane Glycoproteins
  • Receptors, Cell Surface
  • Cathepsins
  • Serine Endopeptidases
  • CTSG protein, human
  • Cathepsin G
  • Leukocyte Elastase
  • Myeloblastin