beta-arrestin Dependent Spontaneous 1a-Adrenoceptor Endocytosis causes Intracellular Transportation of -blockers via Recycling Compartments

Authors:
Pediani JD, Colston JF, Caldwell D, Milligan G, Daly CJ, McGrath JC
In:
Source: Mol Pharmacol
Publication Date: (2005)
Issue: 67(4): 992-1004
Research Area:
Cancer Research/Cell Biology
Cells used in publication:
Embryonic fibroblast, mouse (MEF) immort
Species: mouse
Tissue Origin: embryo
Platform:
Nucleofector® I/II/2b
Abstract
The antagonist ligand BODIPY-FL-prazosin (QAPB) fluoresces when bound to bovine alpha1a-adrenoceptors (ARs). Data indicates that the receptor-ligand complex is spontaneously internalized by beta-arrestin-dependent endocytosis. Internalization of the ligand did not occur in beta-arrestin-deficient cells, was blocked or reversed by another alpha1 ligand, phentolamine, indicating it to reflect binding to the orthosteric recognition site, and was prevented by blocking clathrin-mediated endocytosis. The ligand showed rapid, diffuse, low-intensity, surface binding, superseded by punctate intracellular binding that developed to equilibrium in 50-60 min, and was reversible on ligand removal, indicating a dynamic equilibrium. In cells expressing a human alpha1a-AR-EGFP2 fusion protein, BODIPY-R-558/568-prazosin (RQAPB) co-localized with the fusion, indicating that the ligand gained access to all compartments containing the receptor and, conversely, that the receptor has affinity for the ligand at all of these sites. The distribution of QAPB binding sites was similar for receptors with or without EGFP2, validating the fusion protein as an indicator of receptor location. The ligand partially co-localized with beta-arrestin in recycling and late endosomes indicating receptor transit without destruction. Organelles containing receptors showed considerable movement consistent with a transportation function. This was absent in beta-arrestin-deficient cells indicating that both constitutive receptor internalization and subsequent intracellular transportation are beta-arrestin-dependent. Calculations of relative receptor number suggest that at steady state less than 30% of receptors reside on the cell surface and that recyling is extremely rapid. We conclude that alpha1a-ARs recycle rapidly by an agonist-independent, constitutive, beta-arrestin-dependent process and that this can transport "alpha-blockers" into cells carrying these receptors.