Allosteric interactions across native adenosine-A 3 receptor homodimers: Quantification using single-cell ligand-binding kinetics

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3465-3476

  May, Lauren T ^a,b   Bridge, Lloyd J ^a   Stoddart, Leigh A ^a   Briddon, Stephen J ^a   Hill, Stephen J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Cooperativity; Dissociation; GPCRs

Indexed keywords

ADENOSINE A1 RECEPTOR; ADENOSINE A3 RECEPTOR; G PROTEIN COUPLED RECEPTOR; HOMODIMER;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CHO CELL; FEMALE; KINETICS; LIGAND BINDING; MOLECULAR INTERACTION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE CELL ANALYSIS;

ADENOSINE; ADENOSINE-5'-(N-ETHYLCARBOXAMIDE); ALLOSTERIC REGULATION; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION; HUMANS; KINETICS; PROTEIN BINDING; RECEPTOR, ADENOSINE A3; XANTHINES;

EID: 80053906571     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-186296     Document Type: Article

References (47)

1. Bortolato, A., Mobarec, J. C., Provasi, D., and Filizola, M. (2009) Progress in elucidating the structural and dynamic character of G protein-coupled receptor oligomers for use in drug discovery. Curr. Pharm. Des. 15, 4017-4025
2. Overington, J. P., Al-Lazikani, B., and Hopkins, A. L. (2006) How many drug targets are there? Nat. Rev. Drug Discov. 5, 993-996 (Pubitemid 44835126)
3. Kenakin, T., and Onaran, O. (2002) The ligand paradox between affinity and efficacy: can you be there and not make a difference? Trends Pharmacol. Sci. 23, 275-280 (Pubitemid 34655733)
4. Birdsall, N. J., and Lazareno, S. (2005) Allosterism at muscarinic receptors: ligands and mechanisms. Mini Rev. Med. Chem. 5, 523-543 (Pubitemid 40754167)
5. Christopoulos, A. (2002) Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nat. Rev. Drug Discov. 1, 198-210
6. May, L. T., Leach, K., Sexton, P. M., and Christopoulos, A. (2007) Allosteric modulation of G protein-coupled receptors. Annu. Rev. Pharmacol. Toxicol. 47, 1-51 (Pubitemid 46277033)
7. Kenakin, T. (2007) Collateral efficacy in drug discovery: taking advantage of the good (allosteric) nature of 7TM receptors. Trends Pharmacol. Sci. 28, 407-415
8. Whalen, E. J., Rajagopal, S., and Lefkowitz, R. J. (2011) Therapeutic potential of beta-arrestin- and G protein-biased agonists. Trends Mol. Med. 17, 126-139
9. Rajagopal, S., Rajagopal, K., and Lefkowitz, R. J. (2010) Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat. Rev. Drug Discov. 9, 373-386
10. Casado, V., Cortes, A., Mallol, J., Perez-Capote, K., Ferre, S., Lluis, C., Franco, R., and Canela, E. I. (2009) GPCR homomers and heteromers: a better choice as targets for drug development than GPCR monomers? Pharmacol. Ther. 124, 248-257
11. Springael, J. Y., Urizar, E., Costagliola, S., Vassart, G., and Parmentier, M. (2007) Allosteric properties of G protein-coupled receptor oligomers. Pharmacol. Ther. 115, 410-418 (Pubitemid 47362379)
12. Smith, N. J., and Milligan, G. (2010) Allostery at G proteincoupled receptor homo- and heteromers: uncharted pharmacological landscapes. Pharmacol. Rev. 62, 701-725
13. Attwood, T. K., and Findlay, J. B. (1994) Fingerprinting G-protein- coupled receptors. Protein Eng. 7, 195-203
14. Kolakowski, L. F., Jr. (1994) GCRDb: a G-protein-coupled receptor database. Receptors Channels 2, 1-7
15. Pin, J. P., Galvez, T., and Prezeau, L. (2003) Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol. Ther. 98, 325-354 (Pubitemid 36638547)
16. Birdsall, N. J. (2010) Class A GPCR heterodimers: evidence from binding studies. Trends Pharmacol. Sci. 31, 499-508
17. Milligan, G. (2009) G protein-coupled receptor heterodimerization: contribution to pharmacology and function. Br. J. Pharmacol. 158, 5-14
18. Pin, J. P., Neubig, R., Bouvier, M., Devi, L., Filizola, M., Javitch, J. A., Lohse, M. J., Milligan, G., Palczewski, K., Parmentier, M., and Spedding, M. (2007) International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol. Rev. 59, 5-13 (Pubitemid 46335687)
19. Kuszak, A. J., Pitchiaya, S., Anand, J. P., Mosberg, H. I., Walter, N. G., and Sunahara, R. K. (2009) Purification and functional reconstitution of monomeric mu-opioid receptors: allosteric modulation of agonist binding by Gi2. J. Biol. Chem. 284, 26732-26741
20. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. U. S. A. 104, 7682-7687 (Pubitemid 47185966)
21. Whorton, M. R., Jastrzebska, B., Park, P. S., Fotiadis, D., Engel, A., Palczewski, K., and Sunahara, R. K. (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J. Biol. Chem. 283, 4387-4394
22. Armstrong, D., and Strange, P. G. (2001) Dopamine D2 receptor dimer formation: evidence from ligand binding. J. Biol. Chem. 276, 22621-22629
23. Brea, J., Castro, M., Giraldo, J., Lopez-Gimenez, J. F., Padin, J. F., Quintian, F., Cadavid, M. I., Vilaro, M. T., Mengod, G., Berg, K. A., Clarke, W. P., Vilardaga, J. P., Milligan, G., and Loza, M. I. (2009) Evidence for distinct antagonist-revealed functional states of 5-hydroxytryptamine(2A) receptor homodimers. Mol. Pharmacol. 75, 1380-1391
24. Chidiac, P., Green, M. A., Pawagi, A. B., and Wells, J. W. (1997) Cardiac muscarinic receptors. Cooperativity as the basis for multiple states of affinity. Biochemistry 36, 7361-7379 (Pubitemid 27262359)
25. Christopoulos, A., and Kenakin, T. (2002) G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 54, 323-374 (Pubitemid 34575719)
26. Durroux, T. (2005) Principles: a model for the allosteric interactions between ligand binding sites within a dimeric GPCR. Trends Pharmacol. Sci. 26, 376-384
27. Franco, R., Casado, V., Mallol, J., Ferrada, C., Ferre, S., Fuxe, K., Cortes, A., Ciruela, F., Lluis, C., and Canela, E. I. (2006) The two-state dimer receptor model: a general model for receptor dimers. Mol. Pharmacol. 69, 1905-1912 (Pubitemid 43894307)
28. Franco, R., Casado, V., Mallol, J., Ferre, S., Fuxe, K., Cortes, A., Ciruela, F., Lluis, C., and Canela, E. I. (2005) Dimer-based model for heptaspanning membrane receptors. Trends Biochem. Sci. 30, 360-366 (Pubitemid 40942030)
29. Rovira, X., Pin, J. P., and Giraldo, J. (2010) The asymmetric/ symmetric activation of GPCR dimers as a possible mechanistic rationale for multiple signalling pathways. Trends Pharmacol. Sci. 31, 15-21
30. Rovira, X., Vivo, M., Serra, J., Roche, D., Strange, P. G., and Giraldo, J. (2009) Modelling the interdependence between the stoichiometry of receptor oligomerization and ligand binding for a coexisting dimer/tetramer receptor system. Br. J. Pharmacol. 156, 28-35
31. Wreggett, K. A., and Wells, J. W. (1995) Cooperativity manifest in the binding properties of purified cardiac muscarinic receptors. J. Biol. Chem. 270, 22488-22499
32. May, L. T., Briddon, S. J., and Hill, S. J. (2010) Antagonist selective modulation of adenosine A1 and A3 receptor pharmacology by the food dye Brilliant Black BN: evidence for allosteric interactions. Mol. Pharmacol. 77, 678-686
33. May, L. T., Self, T. J., Briddon, S. J., and Hill, S. J. (2010) The effect of allosteric modulators on the kinetics of agonist-G protein-coupled receptor interactions in single living cells. Mol. Pharmacol. 78, 511-523
34. Christopoulos, A., Lanzafame, A., Ziegler, A., and Mitchelson, F. (1997) Kinetic studies of co-operativity at atrial muscarinic M2 receptors with an "infinite dilution" procedure. Biochem. Pharmacol. 53, 795-800 (Pubitemid 27145784)
35. Cordeaux, Y., Briddon, S. J., Megson, A. E., McDonnell, J., Dickenson, J. M., and Hill, S. J. (2000) Influence of receptor number on functional responses elicited by agonists acting at the human adenosine A(1) receptor: evidence for signaling pathway-dependent changes in agonist potency and relative intrinsic activity. Mol. Pharmacol. 58, 1075-1084
36. Cordeaux, Y., Briddon, S. J., Alexander, S. P., Kellam, B., and Hill, S. J. (2008) Agonist-occupied A3 adenosine receptors exist within heterogeneous complexes in membrane microdomains of individual living cells. FASEB J. 22, 850-860 (Pubitemid 351350620)
37. Rose, R. H., Briddon, S. J., and Holliday, N. D. (2010) Bimolecular fluorescence complementation: lighting up seven transmembrane domain receptor signalling networks. Br. J. Pharmacol. 159, 738-750
38. Briddon, S. J., Gandia, J., Amaral, O. B., Ferre, S., Lluis, C., Franco, R., Hill, S. J., and Ciruela, F. (2008) Plasma membrane diffusion of G protein-coupled receptor oligomers. Biochim. Biophys. Acta 1783, 2262-2268
39. Middleton, R. J., Briddon, S. J., Cordeaux, Y., Yates, A. S., Dale, C. L., George, M. W., Baker, J. G., Hill, S. J., and Kellam, B. (2007) New fluorescent adenosine A1-receptor agonists that allow quantification of ligand-receptor interactions in microdomains of single living cells. J. Med. Chem. 50, 782-793 (Pubitemid 46335649)
40. Ballesteros, J. A., and Weinstein, H. (1995) Integrated methods for the construction of three dimensional models and computational probing of structure function relations in G protein-coupled receptors. Methods Neurosci. 25, 366-428
41. Gao, Z. G., Chen, A., Barak, D., Kim, S. K., Muller, C. E., and Jacobson, K. A. (2002) Identification by site-directed mutagenesis of residues involved in ligand recognition and activation of the human A3 adenosine receptor. J. Biol. Chem. 277, 19056-19063 (Pubitemid 34952470)
42. Han, Y., Moreira, I. S., Urizar, E., Weinstein, H., and Javitch, J. A. (2009) Allosteric communication between protomers of dopamine class A GPCR dimers modulates activation. Nat. Chem. Biol. 5, 688-695
43. Agnati, L. F., Ferre, S., Lluis, C., Franco, R., and Fuxe, K. (2003) Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol. Rev. 55, 509-550
44. Bouvier, M. (2001) Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2, 274-286
45. Gao, Z. G., and Jacobson, K. A. (2008) Translocation of arrestin induced by human A(3) adenosine receptor ligands in an engineered cell line: comparison with G protein-dependent pathways. Pharmacol. Res. 57, 303-311
46. Jacobson, K. A., and Gao, Z. G. (2006) Adenosine receptors as therapeutic targets. Nat. Rev. Drug Discov. 5, 247-264 (Pubitemid 43336037)
47. Hasko, G., Linden, J., Cronstein, B., and Pacher, P. (2008) Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat. Rev. Drug Discov. 7, 759-770