Introduction. The adenosine A1 receptor (A1AR) represents a potential therapeutic target for a variety of central and peripheral disorders (Jacobson et al, 2006). There are now examples of diverse classes of ligands that interact with the A1AR by targeting the orthosteric site, a topographically distinct allosteric site, or concomitantly bridging both sites via a “bitopic” mechanism (May et al, 2008; Valant et al, 2012). Therapeutic applications targeting the A1AR would benefit immensely from the rational design of more potent, selective and efficacious A1AR ligands, however this approach requires greater structural knowledge of the A1AR orthosteric and allosteric binding sites.
Aim. To probe the key residues involved in conferring A1AR orthosteric, allosteric and bitopic ligand affinity, efficacy and allosteric cooperativity.
Methods. Homology modelling of the A1AR, based on the agonist-bound adenosine A2A receptor crystal structure, predicted key residues involved in allosteric and bitopic ligand binding. Individual alanine substitutions of the residues were introduced and each mutant was stably expressed in a FlpINCHO cell line. The influence of receptor mutations on orthosteric (NECA), allosteric (PD81723), and bitopic (VCP746) ligand affinity, efficacy and cooperativity was investigated using assays of radioligand binding and ERK1/2 phosphorylation.
Results. The extracellular mutations, T257A, H264A and E172A, significantly enhanced the affinity of VCP746 but decreased or had no effect on NECA affinity (n=4; p<0.05). Transmembrane mutations, V87A, Q92A, N184A, significantly decreased the positive cooperativity between NECA and PD81723 (n=4; p<0.05).
Discussion. T257, H264 and E172 likely form a hydrogen bond network between extracellular loops 2 and 3. Breaking this network may open up an extracellular cavity to facilitate VCP746 binding (see Figure). Residues involved in conferring allosteric cooperativity cluster around a region proximal to the orthosteric site. The novel structural knowledge gained from these studies will inform ongoing structure-activity studies and rational drug design efforts at this therapeutically relevant receptor family.