Three "hotspots" important for adenosine A 2B receptor activation: A mutational analysis of transmembrane domains 4 and 5 and the second extracellular loop

Purinergic Signalling

Volumn 8, Issue 1, 2012, Pages 23-38

  Peeters, Miriam C ^a   Li, Qilan ^a   van Westen, Gerard J P ^a   Ijzerman, Ad P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Adenosine A 2B receptor; Constitutive activity; G protein coupled receptor; Random mutagenesis; S. cerevisiae

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1, 2, 4 TRIAZOLO [2, 3 A] [1, 3, 5] TRIAZIN 5 YLAMINO] ETHYL] PHENOL; ADENOSINE A2B RECEPTOR; CYSTEINE; EXTRACELLULAR LOOP 2; TRANSMEMBRANE DOMAINS 4; TRANSMEMBRANE DOMAINS 5; UNCLASSIFIED DRUG;

AGAR MEDIUM; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; FUNGUS CULTURE; FUNGUS GROWTH; GAIN OF FUNCTION MUTATION; GENETIC TRANSFORMATION; IMMUNOBLOTTING; LIGAND BINDING; LIQUID CULTURE; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; RECEPTOR INTRINSIC ACTIVITY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84857688066     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-011-9251-x     Document Type: Article

References (46)

1. Fredholm BB, IJzerman AP, Jacobson KA, Linden J, Muller CE (2011) International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol Rev 63(1): 1-34. doi:10.1124/pr.110.003285.
2. Beukers M, van Oppenraaij J, van der Hoorn P, Blad C, den Dulk H, Brouwer J, IJzerman A (2004) Random mutagenesis of the human adenosine A2B receptor followed by growth selection in yeast. Identification of constitutively active and gain of function mutations. Mol Pharmacol 65(3): 702-710.
3. Peeters MC, van Westen GJ, Guo D, Wisse LE, Muller CE, Beukers MW, IJzerman AP (2011) GPCR structure and activation: an essential role for the first extracellular loop in activating the adenosine A2B receptor. FASEB J 25(2): 632-643. doi:10.1096/fj.10-164319.
4. Ahuja S, Hornak V, Yan EC, Syrett N, Goncalves JA, Hirshfeld A, Ziliox M, Sakmar TP, Sheves M, Reeves PJ, Smith SO, Eilers M (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat Struct Mol Biol 16(2): 168-175.
5. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY, Lane JR, IJzerman AP, Stevens RC (2008) The 2. 6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322(5905): 1211-1217.
6. Xu F, Wu H, Katritch V, Han GW, Jacobson KA, Gao ZG, Cherezov V, Stevens RC (2011) Structure of an agonist-bound human A2A adenosine receptor. Science. doi:10.1126/science.1202793.
7. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, Leslie AG, Tate CG (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474(7352): 521-525. doi:10.1038/nature10136.
8. Klco J, Wiegand C, Narzinski K, Baranski T (2005) Essential role for the second extracellular loop in C5a receptor activation. Nat Struct Mol Biol 12(4): 320-326.
9. Massotte D, Kieffer BL (2005) The second extracellular loop: a damper for G protein-coupled receptors? Nat Struct Mol Biol 12(4): 287-288.
10. Peeters MC, van Westen GJ, Li Q, IJzerman AP (2011) Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation. Trends Pharmacol Sci 32(1): 35-42. doi:10.1016/j.tips.2010.10.001.
11. Jaakola VP, IJzerman AP (2010) The crystallographic structure of the human adenosine A(2A) receptor in a high-affinity antagonist-bound state: implications for GPCR drug screening and design. Curr Opin Struct Biol 20: 1-14.
12. Smit M, Vischer H, Bakker R, Jongejan A, Timmerman H, Pardo L, Leurs R (2007) Pharmacogenomic and structural analysis of constitutive G protein-coupled receptor activity. Annu Rev Pharmacol Toxicol 47: 53-87.
13. Brown A, Dyos S, Whiteway M, White J, Watson M, Marzioch M, Clare J, Cousens D, Paddon C, Plumpton C, Romanos M, Dowell S (2000) Functional coupling of mammalian receptors to the yeast mating pathway using novel yeast/mammalian G protein alpha-subunit chimeras. Yeast 16(1): 11-22.
14. Stewart GD, Valant C, Dowell SJ, Mijaljica D, Devenish RJ, Scammells PJ, Sexton PM, Christopoulos A (2009) Determination of adenosine A1 receptor agonist and antagonist pharmacology using Saccharomyces cerevisiae: implications for ligand screening and functional selectivity. J Pharmacol Exp Ther 331(1): 277-286.
15. Fromant M, Blanquet S, Plateau P (1995) Direct random mutagenesis of gene-sized DNA fragments using polymerase chain reaction. Anal Biochem 224(1): 347-353.
16. Beukers M, IJzerman A (2005) Techniques: how to boost GPCR mutagenesis studies using yeast. Trends Pharmacol Sci 26(10): 533-539.
17. Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20(6): 1425.
18. Eckle T, Krahn T, Grenz A, Kohler D, Mittelbronn M, Ledent C, Jacobson MA, Osswald H, Thompson LF, Unertl K, Eltzschig HK (2007) Cardioprotection by ecto-5′-nucleotidase (CD73) and A2B adenosine receptors. Circulation 115(12): 1581-1590.
19. Li Q, Ye K, Blad CC, den Dulk H, Brouwer J, IJzerman AP, Beukers MW (2007) ZM241385, DPCPX, MRS1706 are inverse agonists with different relative intrinsic efficacies on constitutively active mutants of the human adenosine A2B receptor. J Pharmacol Exp Ther 320(2): 637-645.
20. Borrmann T, Hinz S, Bertarelli DC, Li W, Florin NC, Scheiff AB, Muller CE (2009) 1-alkyl-8-(piperazine-1-sulfonyl)phenylxanthines: development and characterization of adenosine A2B receptor antagonists and a new radioligand with subnanomolar affinity and subtype specificity. J Med Chem 52(13): 3994-4006.
21. Ballesteros JA, Weinstein H (1995) Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors. Meth Neurosci 25: 366-428.
22. Vroling B, Sanders M, Baakman C, Borrmann A, Verhoeven S, Klomp J, Oliveira L, de Vlieg J, Vriend G (2011) GPCRDB: information system for G protein-coupled receptors. Nucleic Acids Res 39(Database issue): D309-D319. doi:10.1093/nar/gkq1009.
23. de Zwart M, Vollinga RC, Beukers MW, Sleegers DF, Kunzel JKVD, de Groote M, IJzerman AP (1999) Potent antagonists for the human adenosine A(2B) receptor. Derivatives of the triazolotriazine adenosine receptor antagonist ZM241385 with high affinity. Drug Dev Res 48(3): 95-103.
24. Ongini E, Dionisotti S, Gessi S, Irenius E, Fredholm BB (1999) Comparison of CGS 15943, ZM 241385 and SCH 58261 as antagonists at human adenosine receptors. Naunyn Schmiedebergs Arch Pharmacol 359(1): 7-10.
25. Wu B, Chien EYT, Mol CD, Fenalti G, Liu W, Katritch V, Abagyan R, Brooun A, Wells P, Bi FC, Hamel DJ, Kuhn P, Handel TM, Cherezov V, Stevens RC (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330(6007): 1066-1071.
26. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Yao XJ, Weis WI, Stevens RC, Kobilka BK (2007) GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318(5854): 1266-1273.
27. Storjohann L, Holst B, Schwartz TW (2008) A second disulfide bridge from the N-terminal domain to extracellular loop 2 dampens receptor activity in GPR39. Biochemistry 47(35): 9198-9207.
28. de Graaf C, Foata N, Engkvist O, Rognan D (2008) Molecular modeling of the second extracellular loop of G-protein coupled receptors and its implication on structure-based virtual screening. Proteins 71(2): 599-620.
29. Wang J, Luthey-Schulten ZA, Suslick KS (2003) Is the olfactory receptor a metalloprotein? Proc Natl Acad Sci USA 100(6): 3035-3039. doi:10.1073/pnas.262792899.
30. Warne T, Moukhametzianov R, Baker JG, Nehme R, Edwards PC, Leslie AG, Schertler GF, Tate CG (2011) The structural basis for agonist and partial agonist action on a beta(1)-adrenergic receptor. Nature 469(7329): 241-244. doi:10.1038/nature09746.
31. Park JH, Scheerer P, Hofmann KP, Choe HW, Ernst OP (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454(7201): 183-187.
32. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, Devree BT, Rosenbaum DM, Thian FS, Kobilka TS, Schnapp A, Konetzki I, Sunahara RK, Gellman SH, Pautsch A, Steyaert J, Weis WI, Kobilka BK (2011) Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 469(7329): 175-180. doi:10.1038/nature09648.
33. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VR, Sanishvili R, Fischetti RF, Schertler GF, Weis WI, Kobilka BK (2007) Crystal structure of the human beta(2) adrenergic G-protein-coupled receptor. Nature 450(7168): 383-387.
34. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289(5480): 739-745.
35. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, Henderson R, Leslie AG, Tate CG, Schertler GF (2008) Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454(7203): 486-491.
36. Kobilka BK, Deupi X (2007) Conformational complexity of G-protein-coupled receptors. Trends Pharmacol Sci 28(8): 397-406.
37. Ahuja S, Smith SO (2009) Multiple switches in G protein-coupled receptor activation. Trends Pharmacol Sci 30(9): 494-502.
38. Baranski T, Herzmark P, Lichtarge O, Gerber B, Trueheart J, Meng E, Iiri T, Sheikh S, Bourne H (1999) C5a receptor activation. Genetic identification of critical residues in four transmembrane helices. J Biol Chem 274(22): 15757-15765.
39. Geva A, Lassere TB, Lichtarge O, Pollitt SK, Baranski TJ (2000) Genetic mapping of the human C5a receptor. Identification of transmembrane amino acids critical for receptor function. J Biol Chem 275(45): 35393-35401. doi:10.1074/jbc.M005602200.
40. Jaakola VP, Lane JR, Lin JY, Katritch V, IJzerman AP, Stevens RC (2010) Ligand binding and subtype selectivity of the human A(2A) adenosine receptor: identification and characterization of essential amino acid residues. J Biol Chem 285(17): 13032-13044. doi:10.1074/jbc.M109.096974.
41. Del Tredici AL, Schiffer HH, Burstein ES, Lameh J, Mohell N, Hacksell U, Brann MR, Weiner DM (2004) Pharmacology of polymorphic variants of the human 5-HT1A receptor. Biochem Pharmacol 67(3): 479-490. doi:10.1016/j.bcp.2003.09.030.
42. Granas C, Nordvall G, Larhammar D (1998) Site-directed mutagenesis of the human 5-HT1B receptor. Eur J Pharmacol 349(2-3): 367-375.
43. Sherbiny FF, Schiedel AC, Maass A, Muller CE (2009) Homology modelling of the human adenosine A2B receptor based on X-ray structures of bovine rhodopsin, the beta2-adrenergic receptor and the human adenosine A2A receptor. J Comput Aided Mol Des 23(11): 807-828. doi:10.1007/s10822-009-9299-7.
44. Schiedel AC, Hinz S, Thimm D, Sherbiny F, Borrmann T, Maass A, Muller CE (2011) The four cysteine residues in the second extracellular loop of the human adenosine A(2B) receptor: role in ligand binding and receptor function. Biochem Pharmacol. doi:10.1016/j.bcp.2011.05.008.
45. Arseven OK, Wilkes WP, Jameson JL, Kopp P (2000) Substitutions of tyrosine 601 in the human thyrotropin receptor result in increase or loss of basal activation of the cyclic adenosine monophosphate pathway and disrupt coupling to Gq/11. Thyroid 10(1): 3-10. doi:10.1089/10507250050137879.
46. Sansuk K, Deupi X, Torrecillas I, Jongejan A, Nijmeijer S, Bakker R, Pardo L, Leurs R (2011) A structural insight into the reorientation of transmembrane domains 3 and 5 during family A GPCR activation. Mol Pharmacol 79(2): 262-269. doi:10.1124/mol.110.066068.