Association between adherens junctions and tight junctions via Rap1 promotes barrier protective effects of oxidized phospholipids

J Cell Physiol. 2011 Aug;226(8):2052-62. doi: 10.1002/jcp.22543.

Abstract

Previous studies showed that cyclopenthenone-containing products resulting from oxidation of a natural phospholipid, 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine (OxPAPC) exhibit potent barrier-protective effects in the in vitro and in vivo models of lung endothelial cell (EC) barrier dysfunction, and these effects are associated with enhancement of peripheral actin cytoskeleton, cell-cell and cell-substrate contacts driven by activation of Rac and Cdc42 GTPases. Rap1 GTPase is another member of small GTPase family involved in control of cell-cell interactions; however, its involvement in EC barrier-protective effects by OxPAPC remains unknown. This study examined a role of Rap1 in regulation of OxPAPC-induced interactions in adherens junctions (AJ) and tight junctions (TJ) as a novel mechanism of EC barrier preservation in vitro and in vivo. Immunofluorescence analysis, subcellular fractionation, and co-immunoprecipitation assays indicate that OxPAPC promoted accumulation of AJ proteins: VE-cadherin, p120-catenin, and β-catenin; and TJ proteins: ZO-1, occludin, and JAM-A in the cell membrane, and induced novel cross-interactions between AJ and TJ protein complexes, that were dependent on OxPAPC-induced Rap1 activation. Inhibition of Rap1 function suppressed OxPAPC-mediated pulmonary EC barrier enhancement and AJ and TJ interactions in vitro, as well as inhibited protective effects of OxPAPC against ventilator-induced lung injury in vivo. These results show for the first time a role of Rap1-mediated association between adherens junctions and tight junction complexes in the OxPAPC-induced pulmonary vascular EC barrier protection.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adherens Junctions / metabolism*
  • Animals
  • Antigens, CD / metabolism
  • Cadherins / metabolism
  • Catenins / metabolism
  • Cell Adhesion Molecules / metabolism*
  • Cell Line
  • Delta Catenin
  • Endothelial Cells / metabolism
  • Humans
  • Immunoglobulins / metabolism*
  • Lung / metabolism
  • Male
  • Membrane Proteins / metabolism
  • Mice
  • Occludin
  • Phosphatidylcholines / metabolism
  • Phosphoproteins / metabolism
  • Pulmonary Artery / metabolism
  • Receptors, Cell Surface
  • Shelterin Complex
  • Telomere-Binding Proteins / metabolism*
  • Tight Junctions / metabolism*
  • Ventilator-Induced Lung Injury / metabolism
  • Zonula Occludens-1 Protein
  • beta Catenin / metabolism

Substances

  • Antigens, CD
  • Cadherins
  • Catenins
  • Cell Adhesion Molecules
  • F11R protein, human
  • Immunoglobulins
  • Membrane Proteins
  • OCLN protein, human
  • Occludin
  • Ocln protein, mouse
  • Phosphatidylcholines
  • Phosphoproteins
  • Receptors, Cell Surface
  • Shelterin Complex
  • TERF2IP protein, human
  • TJP1 protein, human
  • Telomere-Binding Proteins
  • Tjp1 protein, mouse
  • Zonula Occludens-1 Protein
  • beta Catenin
  • cadherin 5
  • oxidized-L-alpha-1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine
  • Delta Catenin