Internalization and sequestration of the human prostacyclin receptor

J Biol Chem. 2000 Oct 13;275(41):32037-45. doi: 10.1074/jbc.M003873200.

Abstract

Prostacyclin (PGI(2)), the major product of cyclooxygenase in macrovascular endothelium, mediates its biological effects through its cell surface G protein-coupled receptor, the IP. PKC-mediated phosphorylation of human (h) IP is a critical determinant of agonist-induced desensitization (Smyth, E. M., Hong Li, W., and FitzGerald, G. A. (1998) J. Biol. Chem. 273, 23258-23266). The regulatory events that follow desensitization are unclear. We have examined agonist-induced sequestration of hIP. Human IP, tagged at the N terminus with hemagglutinin (HA) and fused at the C terminus to the green fluorescent protein (GFP), was coupled to increased cAMP (EC(50) = 0.39 +/- 0.09 nm) and inositol phosphate (EC(50) = 86. 6 +/- 18.3 nm) generation when overexpressed in HEK 293 cells. Iloprost-induced sequestration of HAhIP-GFP, followed in real time by confocal microscopy, was partially colocalized to clathrin-coated vesicles. Iloprost induced a time- and concentration-dependent loss of cell surface HA, indicating receptor internalization, which was prevented by inhibitors of clathrin-mediated trafficking and partially reduced by cotransfection of cells with a dynamin dominant negative mutant. Sequestration (EC(50) = 27.6 +/- 5.7 nm) was evident at those concentrations of iloprost that induce PKC-dependent desensitization. Neither the PKC inhibitor GF109203X nor mutation of Ser-328, the site for PKC phosphorylation, altered receptor sequestration indicating that, unlike desensitization, internalization is PKC-independent. Deletion of the C terminus prevented iloprost-induced internalization, demonstrating the critical nature of this region for sequestration. Internalization was unaltered by cotransfection of cells with G protein-coupled receptor kinases (GRK)-2, -3, -5, -6, arrestin-2, or an arrestin-2 dominant negative mutant, indicating that GRKs and arrestins do not play a role in hIP trafficking. The hIP is sequestered in response to agonist activation via a PKC-independent pathway that is distinct from desensitization. Trafficking is dependent on determinants located in the C terminus, is GRK/arrestin-independent, and proceeds in part via a dynamin-dependent clathrin-coated vesicular endocytotic pathway although other dynamin-independent pathways may also be involved.

Publication types

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

MeSH terms

  • Arrestins / genetics
  • Arrestins / metabolism
  • Cell Line
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Clathrin-Coated Vesicles / drug effects
  • Clathrin-Coated Vesicles / metabolism
  • Cyclic AMP / metabolism
  • Cyclic AMP / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Down-Regulation* / drug effects
  • Dynamins
  • Endocytosis* / drug effects
  • Epoprostenol / metabolism
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism
  • Heterotrimeric GTP-Binding Proteins / metabolism
  • Humans
  • Iloprost / pharmacology
  • Indoles / pharmacology
  • Inositol Phosphates / metabolism
  • Maleimides / pharmacology
  • Microscopy, Fluorescence
  • Mutation / genetics
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Receptors, Epoprostenol
  • Receptors, Prostaglandin / agonists
  • Receptors, Prostaglandin / genetics
  • Receptors, Prostaglandin / metabolism*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / immunology
  • Transfection

Substances

  • Arrestins
  • Indoles
  • Inositol Phosphates
  • Maleimides
  • Receptors, Epoprostenol
  • Receptors, Prostaglandin
  • Recombinant Fusion Proteins
  • Epoprostenol
  • Cyclic AMP
  • Protein Serine-Threonine Kinases
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C
  • GTP Phosphohydrolases
  • Heterotrimeric GTP-Binding Proteins
  • Dynamins
  • Iloprost
  • bisindolylmaleimide I