Packaging of proteases and proteoglycans in the granules of mast cells and other hematopoietic cells. A cluster of histidines on mouse mast cell protease 7 regulates its binding to heparin serglycin proteoglycans

J Biol Chem. 1995 Aug 18;270(33):19524-31. doi: 10.1074/jbc.270.33.19524.

Abstract

Mouse mast cell protease 7 (mMCP-7) is a tryptase stored in the secretory granules of mast cells. At the granule pH of 5.5, mMCP-7 is fully active and is bound to heparin-containing serglycin proteoglycans. to understand the interaction of mMCP-7 with heparin inside and outside the mast cell, this trytase was first studied by comparative protein modeling. The "pro" form of mMCP-7 was then expressed in insect cells and studied by site-directed mutagenesis. Although mMCP-7 lacks known linear sequences of amino acis that interact with heparin, the three-dimensional model of mMCP-7 revealed an area on the surface of the folded protein away from the substrate-binding site that exhibits a strong positive electrostatic potential at the acidic pH of the granule. In agreement with this calculation, recombinant pro-mMCP-7 bound to a heparin-affinity column at pH 5.5 and readily dissociated from the column at pH > 6.5. Site-directed mutagenesis confirmed the prediction that the conversion of His residues 8,68, and 70 in the positively charged region into Glu prevents the binding of pro-mMCP-7 to heparin. Because the binding requires positively charged His residues, native mMCP-7 is able to dissociate from the protease/proteoglycan macromolecular complex when the complex is exocytosed from bone marrow-derived mast cells into a neutral pH environment. Many hematopoietic effector cells store positively charged proteins in granules that contain serglycin proteoglycans. The heparin/mMCP-7 interaction, which depends on the tertiary structure of the tryptase, may be representative of a general control mechanism by which hematopoietic cells maximize storage of properly folded, enzymatically active proteins in their granules.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Bone Marrow Cells*
  • Cell Line
  • Chymases
  • Cytoplasmic Granules / enzymology
  • Cytoplasmic Granules / metabolism
  • Heparin / metabolism*
  • Histidine / chemistry
  • Histidine / metabolism*
  • Mast Cells / enzymology
  • Mast Cells / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Molecular Sequence Data
  • Protein Binding
  • Proteoglycans / chemistry
  • Proteoglycans / metabolism*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Serine Endopeptidases / chemistry
  • Serine Endopeptidases / metabolism*
  • Spodoptera
  • Tryptases
  • Vesicular Transport Proteins

Substances

  • Proteoglycans
  • Recombinant Proteins
  • Tpsb2 protein, mouse
  • Vesicular Transport Proteins
  • serglycin
  • Histidine
  • Heparin
  • Serine Endopeptidases
  • chymase 2
  • Chymases
  • Tpsab1 protein, mouse
  • Tryptases