Binding of fluorinated phenylalanine α-factor analogues to Ste2p: Evidence for a cation-φ binding interaction between a peptide ligand and its cognate G protein-coupled receptor

Biochemistry

Volumn 49, Issue 24, 2010, Pages 5007-5015

  Tantry, Subramanyam ^a   Ding, Fa Xiang ^a   Dumont, Mark ^b   Becker, Jeffrey M ^c   Naider, Fred ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING INTERACTION; BIOLOGICAL ACTIVITIES; CONFORMATIONAL CHANGE; DERIVATIZATION OF; FLOW-CYTOMETER; G PROTEIN COUPLED RECEPTORS; GROWTH ARREST; HETEROTRIMERIC G PROTEINS; PEPTIDE LIGAND; SIGNAL TRANSDUCTION SYSTEM; SOLID PHASE PEPTIDE SYNTHESIS; TRANSMEMBRANES; YEAST CELL;

AMINO ACIDS; GROWTH KINETICS; ORGANIC ACIDS; PEPTIDES; PHOSPHATASES; POSITIVE IONS; SIGNAL TRANSDUCTION; YEAST;

BINDING ENERGY;

G PROTEIN COUPLED RECEPTOR; MATING HORMONE ALPHA FACTOR; STE2P RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; NONHUMAN; PRIORITY JOURNAL; SOLID PHASE SYNTHESIS; YEAST CELL;

BINDING, COMPETITIVE; FLUORINE; PEPTIDES; PHENYLALANINE; PHEROMONES; RECEPTORS, MATING FACTOR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THERMODYNAMICS;

EID: 77953657578     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100280f     Document Type: Article

References (46)

1. Filmore, D. (2004) It's a GPCR World Mod. Drug Discovery 7, 24-28
2. Marshall, G. R. (2001) Peptide interactions with G-protein coupled receptors Biopolymers 60, 246-277
3. Kristiansen, K. (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function Pharmacol. Ther. 103, 21-80
4. Schyler, S. and Horuk, R. (2006) I want a new drug: G-protein-coupled receptors in drug development Drug Discovery Today 11, 481-493
5. Fredriksson, R. and Schioth, H. B. (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes Mol. Pharmacol. 67, 1414-1425
6. Crowe, M. L., Perry, B. N., and Connerton, I. F. (2000) Golf complements a GPA1 null mutation in Saccharomyces cerevisiae and functionally couples to the STE2 pheromone receptor J. Recept. Signal Transduction Res. 20, 61-73
7. King, K., Dohlman, H. G., Thorner, J., Caron, M. G., and Lefkowitz, R. J. (1990) Control of yeast mating signal transduction by a mammalian beta 2-adrenergic receptor and Gs alpha subunit Science (New York) 250, 121-123
8. Pausch, M. H. (1997) G-protein-coupled receptors in Saccharomyces cerevisiae: high-throughput screening assays for drug discovery Trends Biotechnol. 15, 487-494
9. Eilers, M., Hornak, V., Smith, S. O., and Konopka, J. B. (2005) Comparison of class A and D G protein-coupled receptors: common features in structure and activation Biochemistry 44, 8959-8975
10. Neumoin, A., Cohen, L. S., Arshava, B., Tantry, S., Becker, J. M., Zerbe, O., and Naider, F. (2009) Structure of a double transmembrane fragment of a G-protein-coupled receptor in micelles Biophys. J. 96, 3187-3196
11. Abel, M. G., Zhang, Y. L., Lu, H. F., Naider, F., and Becker, J. M. (1998) Structure-function analysis of the Saccharomyces cerevisiae tridecapeptide pheromone using alanine-scanned analogs J. Pept. Res. 52, 95-106 (Pubitemid 28374305)
12. Son, C. D., Sargsyan, H., Naider, F., and Becker, J. M. (2004) Identification of ligand binding regions of the Saccharomyces cerevisiae alpha-factor pheromone receptor by photoaffinity cross-linking Biochemistry 43, 13193-13203
13. Umanah, G. K., Son, C., Ding, F., Naider, F., and Becker, J. M. (2009) Cross-linking of a DOPA-containing peptide ligand into its G protein-coupled receptor Biochemistry 48, 2033-2044
14. Ma, J. C. and Dougherty, D. A. (1997) The cation-pi interaction Chem. Rev. 97, 1303-1324
15. Gallivan, J. P. and Dougherty, D. A. (1999) Cation-pi interactions in structural biology Proc. Natl. Acad. Sci. U.S.A. 96, 9459-9464
16. Crowley, P. B. and Golovin, A. (2005) Cation-pi interactions in protein-protein interfaces Proteins 59, 231-239
17. Zacharias, N. and Dougherty, D. A. (2002) Cation-pi interactions in ligand recognition and catalysis Trends Pharmacol. Sci. 23, 281-287
18. Zhong, W., Gallivan, J. P., Zhang, Y., Li, L., Lester, H. A., and Dougherty, D. A. (1998) From ab initio quantum mechanics to molecular neurobiology: a cation-pi binding site in the nicotinic receptor Proc. Natl. Acad. Sci. U.S.A. 95, 12088-12093
19. Beene, D. L., Brandt, G. S., Zhong, W., Zacharias, N. M., Lester, H. A., and Dougherty, D. A. (2002) Cation-pi interactions in ligand recognition by serotonergic (5-HT3A) and nicotinic acetylcholine receptors: the anomalous binding properties of nicotine Biochemistry 41, 10262-10269
20. Lummis, S. C., Beene, D. L., Harrison, N. J., Lester, H. A., and Dougherty, D. A. (2005) A cation-pi binding interaction with a tyrosine in the binding site of the GABAC receptor Chem. Biol. 12, 993-997
21. Ward, S. D., Curtis, C. A., and Hulme, E. C. (1999) Alanine-scanning mutagenesis of transmembrane domain 6 of the M(1) muscarinic acetylcholine receptor suggests that Tyr381 plays key roles in receptor function Mol. Pharmacol. 56, 1031-1041
22. Ding, F. X., Lee, B. K., Hauser, M., Davenport, L., Becker, J. M., and Naider, F. (2001) Probing the binding domain of the Saccharomyces cerevisiae alpha-mating factor receptor with rluorescent ligands Biochemistry 40, 1102-1108
23. Bajaj, A., Celic, A., Ding, F. X., Naider, F., Becker, J. M., and Dumont, M. E. (2004) A fluorescent alpha-factor analogue exhibits multiple steps on binding to its G protein coupled receptor in yeast Biochemistry 43, 13564-13578
24. Leavitt, L. M., Macaluso, C. R., Kim, K. S., Martin, N. P., and Dumont, M. E. (1999) Dominant negative mutations in the alpha-factor receptor, a G protein-coupled receptor encoded by the STE2 gene of the yeast Saccharomyces cerevisiae Mol. Gen. Genet. 261, 917-932
25. Gehret, A. U., Bajaj, A., Naider, F., and Dumont, M. E. (2006) Oligomerization of the yeast alpha-factor receptor: implications for dominant negative effects of mutant receptors J. Biol. Chem. 281, 20698-20714
26. Rose, M., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Mecozzi, S., West, A. P., Jr., and Dougherty, D. A. (1996) Cation-pi interactions in aromatics of biological and medicinal interest: electrostatic potential surfaces as a useful qualitative guide Proc. Natl. Acad. Sci. U.S.A. 93, 10566-10571
28. Raines, D. E., Gioia, F., Claycomb, R. J., and Stevens, R. J. (2004) The N-methyl- d -aspartate receptor inhibitory potencies of aromatic inhaled drugs of abuse: evidence for modulation by cation-pi interactions J. Pharmacol. Exp. Ther. 311, 14-21
29. Liu, S., Henry, L. K., Lee, B. K., Wang, S. H., Arshava, B., Becker, J. M., and Naider, F. (2000) Position 13 analogs of the tridecapeptide mating pheromone from Saccharomyces cerevisiae: design of an iodinatable ligand for receptor binding J. Pept. Res. 56, 24-34
30. Shenbagamurthi, P., Baffi, R., Khan, S. A., Lipke, P., Pousman, C., Becker, J. M., and Naider, F. (1983) Structure-activity relationships in the dodecapeptide alpha factor of Saccharomyces cerevisiae Biochemistry 22, 1298-1304
31. Raths, S. K., Naider, F., and Becker, J. M. (1988) Peptide analogues compete with the binding of alpha-factor to its receptor in Saccharomyces cerevisiae J. Biol. Chem. 263, 17333-17341
32. Naider, F., Yaron, A., Ewenson, A., Tallon, M., Xue, C. B., Srinivasan, J. V., Eriotou-Bargiota, E., and Becker, J. M. (1990) Synthetic probes for the alpha-factor receptor Biopolymers 29, 237-245
33. Naider, F. and Becker, J. M. (2004) The alpha-factor mating pheromone of Saccharomyces cerevisiae: a model for studying the interaction of peptide hormones and G protein-coupled receptors Peptides 25, 1441-1463
34. Eriotou-Bargiota, E., Xue, C. B., Naider, F., and Becker, J. M. (1992) Antagonistic and synergistic peptide analogues of the tridecapeptide mating pheromone of Saccharomyces cerevisiae Biochemistry 31, 551-557
35. Martin, N. P., Celic, A., and Dumont, M. E. (2002) Mutagenic mapping of helical structures in the transmembrane segments of the yeast alpha-factor receptor J. Mol. Biol. 317, 765-788
36. Lee, B. K., Lee, Y. H., Hauser, M., Son, C. D., Khare, S., Naider, F., and Becker, J. M. (2002) Tyr266 in the sixth transmembrane domain of the yeast alpha-factor receptor plays key roles in receptor activation and ligand specificity Biochemistry 41, 13681-13689
37. Hauser, M., Kauffman, S., Lee, B. K., Naider, F., and Becker, J. M. (2007) The first extracellular loop of the Saccharomyces cerevisiae G protein-coupled receptor Ste2p undergoes a conformational change upon ligand binding J. Biol. Chem. 282, 10387-10397
38. Parrish, W., Eilers, M., Ying, W., and Konopka, J. B. (2002) The cytoplasmic end of transmembrane domain 3 regulates the activity of the Saccharomyces cerevisiae G-protein-coupled alpha-factor receptor Genetics 160, 429-443
39. Nygaard, R., Frimurer, T. M., Holst, B., Rosenkilde, M. M., and Schwartz, T. W. (2009) Ligand binding and micro-switches in 7TM receptor structures Trends Pharmacol. Sci. 30, 249-259
40. Lawson, Z. and Wheatley, M. (2004) The third extracellular loop of G-protein-coupled receptors: more than just a linker between two important transmembrane helices Biochem. Soc. Trans. 32, 1048-1050
41. Shi, L. and Javitch, J. A. (2004) The second extracellular loop of the dopamine D2 receptor lines the binding-site crevice Proc. Natl. Acad. Sci. U.S.A. 101, 440-445
42. Klco, J. M., Wiegand, C. B., Narzinski, K., and Baranski, T. J. (2005) Essential role for the second extracellular loop in C5a receptor activation Nat. Struct. Mol. Biol. 12, 320-326
43. Klco, J. M., Nikiforovich, G. V., and Baranski, T. J. (2006) Genetic analysis of the first and third extracellular loops of the C5a receptor reveals an essential WXFG motif in the first loop J. Biol. Chem. 281, 12010-12019
44. Ahuja, S., Hornak, V., Yan, E. C., Syrett, N., Goncalves, J. A., Hirshfeld, A., Ziliox, M., Sakmar, T. P., Sheves, M., Reeves, P. J., Smith, S. O., and Eilers, M. (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation Nat. Struct. Mol. Biol. 16, 168-175
45. Bokoch, M. P., Zou, Y., Rasmussen, S. G., Liu, C. W., Nygaard, R., Rosenbaum, D. M., Fung, J. J., Choi, H. J., Thian, F. S., Kobilka, T. S., Puglisi, J. D., Weis, W. I., Pardo, L., Prosser, R. S., Mueller, L., and Kobilka, B. K. (2010) Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor Nature 463, 108-112
46. Akal-Strader, A., Khare, S., Xu, D., Naider, F., and Becker, J. M. (2002) Residues in the first extracellular loop of a G protein-coupled receptor play a role in signal transduction J. Biol. Chem. 277, 30581-30590