The role of a sodium ion binding site in the allosteric modulation of the A2A adenosine G protein-coupled receptor

Structure

Volumn 21, Issue 12, 2013, Pages 2175-2185

  Gutiérrez De Terán, Hugo ^a,b,c   Massink, Arnault ^d   Rodríguez, David ^a,e   Liu, Wei ^b   Han, Gye Won ^b   Joseph, Jeremiah S ^b   Katritch, Ilia ^b   Heitman, Laura H ^d   Xia, Lizi ^d   Ijzerman, Adriaan P ^d   Cherezov, Vadim ^b   Katritch, Vsevolod ^b   Stevens, Raymond C ^b  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d LEIDEN UNIVERSITY   (Netherlands)

^e STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 5 (N,N HEXAMETHYLENE)AMILORIDE; ADENOSINE A2A RECEPTOR; AMILORIDE; AMILORIDE DERIVATIVE; G PROTEIN COUPLED RECEPTOR; SODIUM ION; UK 432097;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG EFFECT; DRUG RECEPTOR BINDING; EMBRYO; EXPERIMENTAL STUDY; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; RECEPTOR AFFINITY; SIMULATION; THERMOSTABILITY;

ADENOSINE A2 RECEPTOR AGONISTS; ADENOSINE A2 RECEPTOR ANTAGONISTS; ALLOSTERIC REGULATION; ALLOSTERIC SITE; AMILORIDE; AMINO ACID SEQUENCE; CATIONS, MONOVALENT; HEK293 CELLS; HOT TEMPERATURE; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STABILITY; RADIOLIGAND ASSAY; RECEPTOR, ADENOSINE A2A; SODIUM;

EID: 84889573352     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.09.020     Document Type: Article

References (64)

1. A.I. Alexandrov, M. Mileni, E.Y. Chien, M.A. Hanson, and R.C. Stevens Microscale fluorescent thermal stability assay for membrane proteins Structure 16 2008 351 359
2. T.E. Angel, M.R. Chance, and K. Palczewski Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors Proc. Natl. Acad. Sci. USA 106 2009 8555 8560
3. J.A. Ballesteros, and H. Weinstein Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors Methods Neurosci. 25 1995 366 428
4. H. Barbhaiya, R. McClain, A. Ijzerman, and S.A. Rivkees Site-directed mutagenesis of the human A1 adenosine receptor: influences of acidic and hydroxy residues in the first four transmembrane domains on ligand binding Mol. Pharmacol. 50 1996 1635 1642
5. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, and J. Hermans Interaction models for water in relation to protein hydration B. Pullman, Intermolecular Forces 1981 D. Reidel Publishing Company Dordretch 331 342
6. O. Berger, O. Edholm, and F. Jähnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
7. N. Chakrabarti, C. Neale, J. Payandeh, E.F. Pai, and R. Pomès An iris-like mechanism of pore dilation in the CorA magnesium transport system Biophys. J. 98 2010 784 792
8. V. Cherezov Lipidic cubic phase technologies for membrane protein structural studies Curr. Opin. Struct. Biol. 21 2011 559 566
9. J.A. Christopher, J. Brown, A.S. Doré, J.C. Errey, M. Koglin, F.H. Marshall, D.G. Myszka, R.L. Rich, C.G. Tate, and B. Tehan Biophysical fragment screening of the β1-adrenergic receptor: identification of high affinity arylpiperazine leads using structure-based drug design J. Med. Chem. 56 2013 3446 3455
10. A. Christopoulos Allosteric binding sites on cell-surface receptors: novel targets for drug discovery Nat. Rev. Drug Discov. 1 2002 198 210
11. M. Congreve, S.P. Andrews, A.S. Doré, K. Hollenstein, E. Hurrell, C.J. Langmead, J.S. Mason, I.W. Ng, B. Tehan, and A. Zhukov Discovery of 1,2,4-triazine derivatives as adenosine A(2A) antagonists using structure based drug design J. Med. Chem. 55 2012 1898 1903
12. M. Congreve, C.J. Langmead, J.S. Mason, and F.H. Marshall Progress in structure based drug design for G protein-coupled receptors J. Med. Chem. 54 2011 4283 4311
13. P.J. Conn, A. Christopoulos, and C.W. Lindsley Allosteric modulators of GPCRs: a novel approach for the treatment of CNS disorders Nat. Rev. Drug Discov. 8 2009 41 54
14. A.S. Doré, N. Robertson, J.C. Errey, I. Ng, K. Hollenstein, B. Tehan, E. Hurrell, K. Bennett, M. Congreve, and F. Magnani Structure of the adenosine A(2A) receptor in complex with ZM241385 and the xanthines XAC and caffeine Structure 19 2011 1283 1293
15. R.O. Dror, D.H. Arlow, D.W. Borhani, M.O. Jensen, S. Piana, and D.E. Shaw Identification of two distinct inactive conformations of the beta2-adrenergic receptor reconciles structural and biochemical observations Proc. Natl. Acad. Sci. USA 106 2009 4689 4694
16. J.S. Fraser, H. van den Bedem, A.J. Samelson, P.T. Lang, J.M. Holton, N. Echols, and T. Alber Accessing protein conformational ensembles using room-temperature X-ray crystallography Proc. Natl. Acad. Sci. USA 108 2011 16247 16252
17. Z.G. Gao, and A.P. Ijzerman Allosteric modulation of A(2A) adenosine receptors by amiloride analogues and sodium ions Biochem. Pharmacol. 60 2000 669 676
18. Z.G. Gao, and K.A. Jacobson Keynote review: allosterism in membrane receptors Drug Discov. Today 11 2006 191 202
19. Z.G. Gao, Q. Jiang, K.A. Jacobson, and A.P. Ijzerman Site-directed mutagenesis studies of human A(2A) adenosine receptors: involvement of glu(13) and his(278) in ligand binding and sodium modulation Biochem. Pharmacol. 60 2000 661 668
20. Z.G. Gao, S.K. Kim, A.S. Gross, A. Chen, J.B. Blaustein, and K.A. Jacobson Identification of essential residues involved in the allosteric modulation of the human A(3) adenosine receptor Mol. Pharmacol. 63 2003 1021 1031
21. Z.G. Gao, N. Melman, A. Erdmann, S.G. Kim, C.E. Müller, A.P. IJzerman, and K.A. Jacobson Differential allosteric modulation by amiloride analogues of agonist and antagonist binding at A(1) and A(3) adenosine receptors Biochem. Pharmacol. 65 2003 525 534
22. A. Garritsen, A.P. Ijzerman, M.T. Tulp, E.J. Cragoe Jr., and W. Soudijn Receptor binding profiles of amiloride analogues provide no evidence for a link between receptors and the Na+/H+ exchanger, but indicate a common structure on receptor proteins J. Recept. Res. 11 1991 891 907
23. A. Göblyös, and A.P. Ijzerman Allosteric modulation of adenosine receptors Biochim. Biophys. Acta 1808 2011 1309 1318
24. H. Gutiérrez-de-Terán, X. Bello, and D. Rodríguez Characterization of the dynamic events of GPCRs by automated computational simulations Biochem. Soc. Trans. 41 2013 205 212
25. M.M. Harding Small revisions to predicted distances around metal sites in proteins Acta Crystallogr. D Biol. Crystallogr. 62 2006 678 682
26. L.H. Heitman, K. Ye, J. Oosterom, and A.P. Ijzerman Amiloride derivatives and a nonpeptidic antagonist bind at two distinct allosteric sites in the human gonadotropin-releasing hormone receptor Mol. Pharmacol. 73 2008 1808 1815
27. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
28. T. Hino, T. Arakawa, H. Iwanari, T. Yurugi-Kobayashi, C. Ikeda-Suno, Y. Nakada-Nakura, O. Kusano-Arai, S. Weyand, T. Shimamura, and N. Nomura G-protein-coupled receptor inactivation by an allosteric inverse-agonist antibody Nature 482 2012 237 240
29. S.R. Hoare, M.C. Coldwell, D. Armstrong, and P.G. Strange Regulation of human D(1), d(2(long)), d(2(short)), D(3) and D(4) dopamine receptors by amiloride and amiloride analogues Br. J. Pharmacol. 130 2000 1045 1059
30. D.A. Horstman, S. Brandon, A.L. Wilson, C.A. Guyer, E.J. Cragoe Jr., and L.E. Limbird An aspartate conserved among G-protein receptors confers allosteric regulation of alpha 2-adrenergic receptors by sodium J. Biol. Chem. 265 1990 21590 21595
31. M.J. Howard, R.J. Hughes, H.J. Motulsky, M.D. Mullen, and P.A. Insel Interactions of amiloride with alpha- and beta-adrenergic receptors: amiloride reveals an allosteric site on alpha 2-adrenergic receptors Mol. Pharmacol. 32 1987 53 58
32. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
33. V.-P. Jaakola, M.T. Griffith, M.A. Hanson, V. Cherezov, E.Y.T. Chien, J.R. Lane, A.P. Ijzerman, and R.C. Stevens The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist Science 322 2008 1211 1217
34. K.A. Jacobson, Z.G. Gao, A. Göblyös, and A.P. Ijzerman Allosteric modulation of purine and pyrimidine receptors Adv. Pharmacol. 61 2011 187 220
35. G.A. Kaminski, R.A. Friesner, J. Tirado-Rives, and W.L. Jorgensen Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides J. Phys. Chem. B 105 2001 6474 6487
36. V. Katritch, V. Cherezov, and R.C. Stevens Structure-function of the G protein-coupled receptor superfamily Annu. Rev. Pharmacol. Toxicol. 53 2013 531 556
37. G. Lebon, T. Warne, P.C. Edwards, K. Bennett, C.J. Langmead, A.G. Leslie, and C.G. Tate Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation Nature 474 2011 521 525
38. W. Liu, E. Chun, A.A. Thompson, P. Chubukov, F. Xu, V. Katritch, G.W. Han, C.B. Roth, L.H. Heitman, and A.P. IJzerman Structural basis for allosteric regulation of GPCRs by sodium ions Science 337 2012 232 236
39. A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, J.M. Mathiesen, R.K. Sunahara, L. Pardo, W.I. Weis, B.K. Kobilka, and S. Granier Crystal structure of the μ-opioid receptor bound to a morphinan antagonist Nature 485 2012 321 326
40. T. Mirzadegan, G. Benkö, S. Filipek, and K. Palczewski Sequence analyses of G-protein-coupled receptors: similarities to rhodopsin Biochemistry 42 2003 2759 2767
41. R.R. Neubig, M. Spedding, T. Kenakin, A. Christopoulos International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification. XXXVIII. Update on terms and symbols in quantitative pharmacology Pharmacol. Rev. 55 2003 597 606
42. K.A. Neve, M.G. Cumbay, K.R. Thompson, R. Yang, D.C. Buck, V.J. Watts, C.J. DuRand, and M.M. Teeter Modeling and mutational analysis of a putative sodium-binding pocket on the dopamine D2 receptor Mol. Pharmacol. 60 2001 373 381
43. J. Nie, and D.L. Lewis Structural domains of the CB1 cannabinoid receptor that contribute to constitutive activity and G-protein sequestration J. Neurosci. 21 2001 8758 8764
44. S. Nose, and M.L. Klein Constant pressure molecular-dynamics for molecular-systems Mol. Physiol. 50 1983 1055 1076
45. L. Pardo, X. Deupi, N. Dölker, M.L. López-Rodríguez, and M. Campillo The role of internal water molecules in the structure and function of the rhodopsin family of G protein-coupled receptors ChemBioChem 8 2007 19 24
46. J.H. Park, P. Scheerer, K.P. Hofmann, H.-W. Choe, and O.P. Ernst Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454 2008 183 187
47. P.J. Pauwels Competitive and silent antagonism of recombinant 5-HT1B receptors by amiloride Gen. Pharmacol. 29 1997 749 751
48. C.B. Pert, G. Pasternak, and S.H. Snyder Opiate agonists and antagonists discriminated by receptor binding in brain Science 182 1973 1359 1361
49. C.D. Proulx, B.J. Holleran, A.A. Boucard, E. Escher, G. Guillemette, and R. Leduc Mutational analysis of the conserved Asp2.50 and ERY motif reveals signaling bias of the urotensin II receptor Mol. Pharmacol. 74 2008 552 561
50. S.G. Rasmussen, B.T. DeVree, Y. Zou, A.C. Kruse, K.Y. Chung, T.S. Kobilka, F.S. Thian, P.S. Chae, E. Pardon, and D. Calinski Crystal structure of the β2 adrenergic receptor-Gs protein complex Nature 477 2011 549 555
51. D. Rodríguez, A. Piñeiro, and H. Gutiérrez-de- Terán Molecular dynamics simulations reveal insights into key structural elements of adenosine receptors Biochemistry 50 2011 4194 4208
52. D.M. Rosenbaum, V. Cherezov, M.A. Hanson, S.G.F. Rasmussen, F.S. Thian, T.S. Kobilka, H.-J. Choi, X.-J. Yao, W.I. Weis, R.C. Stevens, and B.K. Kobilka GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function Science 318 2007 1266 1273
53. J. Sambrook, and E.F. Fritsch Molecular Cloning: A Laboratory Manual Second Edition 1989 Cold Spring Harbor Laboratory Cold Spring Harbor, NY
54. L.L.C. Schrödinger MacroModel 9.7 User Manual 2009 Schrödinger L.L.C. New York, NY
55. T.W. Schwartz, T.M. Frimurer, B. Holst, M.M. Rosenkilde, and C.E. Elling Molecular mechanism of 7TM receptor activation - a global toggle switch model Annu. Rev. Pharmacol. Toxicol. 46 2006 481 519
56. J. Selent, F. Sanz, M. Pastor, and G. De Fabritiis Induced effects of sodium ions on dopaminergic G-protein coupled receptors PLoS Comput. Biol. 6 2010 e1000884
57. L. Shi, and J.A. Javitch The binding site of aminergic G protein-coupled receptors: the transmembrane segments and second extracellular loop Annu. Rev. Pharmacol. Toxicol. 42 2002 437 467
58. P.K. Smith, R.I. Krohn, G.T. Hermanson, A.K. Mallia, F.H. Gartner, M.D. Provenzano, E.K. Fujimoto, N.M. Goeke, B.J. Olson, and D.C. Klenk Measurement of protein using bicinchoninic acid Anal. Biochem. 150 1985 76 85
59. S.H. Snyder, and G.W. Pasternak Historical review: Opioid receptors Trends Pharmacol. Sci. 24 2003 198 205
60. C.G. Tate, and G.F. Schertler Engineering G protein-coupled receptors to facilitate their structure determination Curr. Opin. Struct. Biol. 19 2009 386 395
61. B.S. Tsai, and R.J. Lefkowitz Agonist-specific effects of monovalent and divalent cations on adenylate cyclase-coupled alpha adrenergic receptors in rabbit platelets Mol. Pharmacol. 14 1978 540 548
62. M.B. Ulmschneider, C. Bagnéris, E.C. McCusker, P.G. Decaen, M. Delling, D.E. Clapham, J.P. Ulmschneider, and B.A. Wallace Molecular dynamics of ion transport through the open conformation of a bacterial voltage-gated sodium channel Proc. Natl. Acad. Sci. USA 110 2013 6364 6369
63. T. Warne, P.C. Edwards, A.G. Leslie, and C.G. Tate Crystal structures of a stabilized β1-adrenoceptor bound to the biased agonists bucindolol and carvedilol Structure 20 2012 841 849
64. F. Xu, H. Wu, V. Katritch, G.W. Han, K.A. Jacobson, Z.G. Gao, V. Cherezov, and R.C. Stevens Structure of an agonist-bound human A2A adenosine receptor Science 332 2011 322 327