The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity

J Cell Sci. 2003 Oct 1;116(Pt 19):3879-91. doi: 10.1242/jcs.00704.

Abstract

Tight junctions play a central role in the establishment of cell polarity in vertebrate endothelial and epithelial cells. A ternary protein complex consisting of the cell polarity proteins PAR-3 and PAR-6 and the atypical protein kinase C localizes at tight junctions and is crucial for tight junction formation. We have recently shown that PAR-3 directly associates with the junctional adhesion molecule (JAM), which suggests that the ternary complex is targeted to tight junctions of epithelial cells through PAR-3 binding to JAM. The expression of JAM-related proteins by endothelial cells prompted us to test whether recruitment of the ternary complex in endothelial cells can occur through binding to JAM-2, JAM-3, endothelial cell-selective adhesion molecule (ESAM) or coxsackie- and adenovirus receptor (CAR). Here we show that the two JAM-related proteins JAM-2 and JAM-3 directly associate with PAR-3. The association between PAR-3 and JAM-2/-3 is mediated through the first PDZ domain of PAR-3. In agreement with the predominant expression of JAM-2 and JAM-3 in endothelial cells, we found that PAR-3 is expressed by endothelial cells in vivo and is localized at cell contacts of cultured endothelial cells. PAR-3 associates with JAM-2/-3 but not with the JAM-related Ig-superfamily members ESAM or CAR. In addition, we show that the tight junction-associated protein ZO-1 associates with JAM-2/-3 in a PDZ domain-dependent manner. Using ectopic expression of JAM-2 in CHO cells, we show that the junctional localization of JAM-2 is regulated by serine phosphorylation and that its clustering at cell-cell contacts recruits endogenous PAR-3 and ZO-1. Our findings suggest that JAM-2 affects endothelial cell junctions by its regulated clustering at intercellular contacts, and they support a role for JAM-2, and possibly JAM-3, in tight junction formation of endothelial cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • CHO Cells
  • COS Cells
  • Carrier Proteins / metabolism*
  • Cell Adhesion Molecules / metabolism*
  • Cell Cycle Proteins
  • Cell Polarity / physiology*
  • Cells, Cultured
  • Chlorocebus aethiops
  • Cloning, Molecular
  • Cricetinae
  • Cricetulus
  • Endothelial Cells / metabolism*
  • Epithelial Cells / metabolism
  • Humans
  • Immunoglobulins / metabolism*
  • Immunohistochemistry
  • Membrane Proteins / metabolism*
  • Mice
  • Phosphorylation
  • Protein Binding
  • Protein Structure, Tertiary
  • Serine / metabolism
  • Tight Junctions / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Cell Adhesion Molecules
  • Cell Cycle Proteins
  • Esam protein, mouse
  • Immunoglobulins
  • JAM3 protein, human
  • Jam3 protein, mouse
  • Membrane Proteins
  • Pard3 protein, mouse
  • Serine