Trans-dimerization of JAM-A regulates Rap2 and is mediated by a domain that is distinct from the cis-dimerization interface

Mol Biol Cell. 2014 May;25(10):1574-85. doi: 10.1091/mbc.E14-01-0018. Epub 2014 Mar 26.

Abstract

Junctional adhesion molecule-A (JAM-A) is a tight junction-associated signaling protein that regulates epithelial cell proliferation, migration, and barrier function. JAM-A dimerization on a common cell surface (in cis) has been shown to regulate cell migration, and evidence suggests that JAM-A may form homodimers between cells (in trans). Indeed, transfection experiments revealed accumulation of JAM-A at sites between transfected cells, which was lost in cells expressing cis- or predicted trans-dimerization null mutants. Of importance, microspheres coated with JAM-A containing alanine substitutions to residues 43NNP45 (NNP-JAM-A) within the predicted trans-dimerization site did not aggregate. In contrast, beads coated with cis-null JAM-A demonstrated enhanced clustering similar to that observed with wild-type (WT) JAM-A. In addition, atomic force microscopy revealed decreased association forces in NNP-JAM-A compared with WT and cis-null JAM-A. Assessment of effects of JAM-A dimerization on cell signaling revealed that expression of trans- but not cis-null JAM-A mutants decreased Rap2 activity. Furthermore, confluent cells, which enable trans-dimerization, had enhanced Rap2 activity. Taken together, these results suggest that trans-dimerization of JAM-A occurs at a unique site and with different affinity compared with dimerization in cis. Trans-dimerization of JAM-A may thus act as a barrier-inducing molecular switch that is activated when cells become confluent.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Binding Sites / genetics
  • CHO Cells
  • Cell Adhesion / physiology
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Aggregation / physiology
  • Cell Line
  • Cell Membrane / metabolism
  • Cell Movement
  • Cricetulus
  • HEK293 Cells
  • Humans
  • Intercellular Junctions / metabolism
  • Microscopy, Atomic Force
  • Mutation
  • Protein Multimerization / physiology*
  • Protein Structure, Tertiary
  • RNA Interference
  • RNA, Small Interfering
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Signal Transduction
  • Tight Junctions / genetics
  • Tight Junctions / physiology*
  • rap GTP-Binding Proteins / biosynthesis*

Substances

  • Cell Adhesion Molecules
  • F11R protein, human
  • RNA, Small Interfering
  • Receptors, Cell Surface
  • RAP2A protein, human
  • rap GTP-Binding Proteins