Regulated release and functional modulation of junctional adhesion molecule A by disintegrin metalloproteinases

Blood. 2009 May 7;113(19):4799-809. doi: 10.1182/blood-2008-04-152330. Epub 2009 Mar 3.

Abstract

Junctional adhesion molecule A (JAM-A) is a transmembrane adhesive glycoprotein that participates in the organization of endothelial tight junctions and contributes to leukocyte transendothelial migration. We demonstrate here that cultured endothelial cells not only express a cellular 43-kDa variant of JAM-A but also release considerable amounts of a 33-kDa soluble JAM-A variant. This release is enhanced by treatment with proinflammatory cytokines and is associated with the down-regulation of surface JAM-A. Inhibition experiments, loss/gain-of-function experiments, and cleavage experiments with recombinant proteases indicated that cleavage of JAM-A is mediated predominantly by the disintegrin and metalloproteinase (ADAM) 17 and, to a lesser extent, by ADAM10. Cytokine treatment of mice increased JAM-A serum level and in excised murine aortas increased ADAM10/17 activity correlated with enhanced JAM-A release. Functionally, soluble JAM-A blocked migration of cultured endothelial cells, reduced transendothelial migration of isolated neutrophils in vitro, and decreased neutrophil infiltration in a murine air pouch model by LFA-1- and JAM-A-dependent mechanisms. Therefore, shedding of JAM-A by inflamed vascular endothelium via ADAM17 and ADAM10 may not only generate a biomarker for vascular inflammation but could also be instrumental in controlling JAM-A functions in the molecular zipper guiding transendothelial diapedesis of leukocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM Proteins / antagonists & inhibitors
  • ADAM Proteins / physiology*
  • ADAM10 Protein
  • ADAM17 Protein
  • Amyloid Precursor Protein Secretases / antagonists & inhibitors
  • Amyloid Precursor Protein Secretases / physiology*
  • Animals
  • Aorta / cytology
  • Aorta / metabolism
  • Blotting, Western
  • Cell Adhesion / physiology
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Adhesion Molecules / physiology*
  • Cells, Cultured
  • Cytokines / metabolism
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / metabolism
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Humans
  • Immunoenzyme Techniques
  • Immunoglobulins / genetics
  • Immunoglobulins / metabolism*
  • Kidney / cytology
  • Kidney / metabolism
  • Male
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / metabolism
  • Protease Inhibitors / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Cell Surface / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Umbilical Veins / cytology
  • Umbilical Veins / metabolism
  • Urinary Bladder Neoplasms / metabolism
  • Urinary Bladder Neoplasms / pathology

Substances

  • Cell Adhesion Molecules
  • Cytokines
  • F11R protein, human
  • F11r protein, mouse
  • Immunoglobulins
  • Membrane Proteins
  • Protease Inhibitors
  • RNA, Messenger
  • Receptors, Cell Surface
  • Amyloid Precursor Protein Secretases
  • ADAM Proteins
  • ADAM10 Protein
  • Adam10 protein, mouse
  • ADAM17 Protein
  • ADAM17 protein, human
  • Adam17 protein, mouse