Detection of G protein-selective G protein-coupled receptor (GPCR) conformations in live cells

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17167-17178

  Malik, Rabia U ^a   Ritt, Michael ^a   DeVree, Brian T ^b   Neubig, Richard R ^b   Sunahara, Roger K ^b   Sivaramakrishnan, Sivaraj ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLYL CYCLASE; CONFORMATIONAL CHANGE; EFFECTIVE SUPPRESSION; G PROTEIN ACTIVATION; G-PROTEIN COUPLED RECEPTORS; IONIC INTERACTION; MULTIPLE CONFORMATIONS; STRUCTURAL MECHANISMS;

MUTAGENESIS; PROTEINS; SENSORS;

CONFORMATIONS;

ADENYLATE CYCLASE; ASPARTIC ACID; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; LYSINE; METOPROLOL; TRANSDUCIN;

ARTICLE; BIOSENSOR; CARBOXY TERMINAL SEQUENCE; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIVE CELL; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; VALIDATION PROCESS;

(E/D)RY MOTIF; 7-HELIX RECEPTOR; CELL SIGNALING; FRET; FUNCTIONAL SELECTIVITY; G PROTEIN-COUPLED RECEPTORS (GPCR); G PROTEINS;

ADRENERGIC BETA-2 RECEPTOR AGONISTS; ADRENERGIC BETA-ANTAGONISTS; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; CYCLIC AMP; FLUORESCENCE RESONANCE ENERGY TRANSFER; GTP-BINDING PROTEIN ALPHA SUBUNITS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HEK293 CELLS; HUMANS; METOPROLOL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OPSINS; PEPTIDE FRAGMENTS; PROPANOLAMINES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS;

EID: 84879054442     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.464065     Document Type: Article

References (44)

1. Bockenhauer, S., Fürstenberg, A., Yao, X. J., Kobilka, B. K., and Moerner, W. E. (2011) Conformational dynamics of single G protein-coupled receptors in solution. J. Phys. Chem. B 115, 13328-13338
2. Liu, J. J., Horst, R., Katritch, V., Stevens, R. C., and Wüthrich, K. (2012) Biased signaling pathways in β2-adrenergic receptor characterized by 19F-NMR. Science 335, 1106-1110
3. Kahsai, A. W., Xiao, K., Rajagopal, S., Ahn, S., Shukla, A. K., Sun, J., Oas, T. G., and Lefkowitz, R. J. (2011) Multiple ligand-specific conformations of the β2-adrenergic receptor. Nat. Chem. Biol. 7, 692-700
4. Vilardaga, J. P., Steinmeyer, R., Harms, G. S., and Lohse, M. J. (2005) Molecular basis of inverse agonism in a G protein-coupled receptor. Nat. Chem. Biol. 1, 25-28
5. Yao, X. J., Vélez Ruiz, G., Whorton, M. R., Rasmussen, S. G., DeVree, B. T., Deupi, X., Sunahara, R. K., and Kobilka, B. (2009) The effect of ligand efficacy on the formation and stability of a GPCR-G protein complex. Proc. Natl. Acad. Sci. U.S.A. 106, 9501-9506
6. Azzi, M., Charest, P. G., Angers, S., Rousseau, G., Kohout, T., Bouvier, M., and Piñeyro, G. (2003) β-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 100, 11406-11411 (Pubitemid 37205948)
7. Granier, S., and Kobilka, B. (2012) A new era of GPCR structural and chemical biology. Nat. Chem. Biol. 8, 670-673
8. Urban, J. D., Clarke, W. P., von Zastrow, M., Nichols, D. E., Kobilka, B., Weinstein, H., Javitch, J. A., Roth, B. L., Christopoulos, A., Sexton, P. M., Miller, K. J., Spedding, M., and Mailman, R. B. (2007) Functional selectivity and classical concepts of quantitative pharmacology. J. Pharmacol. Exp. Ther. 320, 1-13 (Pubitemid 46025713)
9. Onaran, H. O., and Costa, T. (2012) Where have all the active receptor states gone? Nat. Chem. Biol. 8, 674-677
10. Sivaramakrishnan, S., and Spudich, J. A. (2011) Systematic control of protein interaction using a modular ER/K α-helix linker. Proc. Natl. Acad. Sci. U.S.A. 108, 20467-20472
11. Hamm, H. E., Deretic, D., Arendt, A., Hargrave, P. A., Koenig, B., and Hofmann, K. P. (1988) Site of G protein binding to rhodopsin mapped with synthetic peptides from the α subunit. Science 241, 832-835
12. Oldham, W. M., and Hamm, H. E. (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9, 60-71
13. Rasenick, M. M., Watanabe, M., Lazarevic, M. B., Hatta, S., and Hamm, H. E. (1994) Synthetic peptides as probes forGprotein function. Carboxylterminal G α s peptides mimic Gs and evoke high affinity agonist binding to beta-adrenergic receptors. J. Biol. Chem. 269, 21519-21525
14. Choe, H. W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauss, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II. Nature 471, 651-655
15. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477, 549-555
16. Chung, K. Y., Rasmussen, S. G., Liu, T., Li, S., DeVree, B. T., Chae, P. S., Calinski, D., Kobilka, B. K., Woods, V. L., Jr., and Sunahara, R. K. (2011) Conformational changes in theGprotein Gs induced by the β2 adrenergic receptor. Nature 477, 611-615
17. Martin, E. L., Rens-Domiano, S., Schatz, P. J., and Hamm, H. E. (1996) Potent peptide analogues of a G protein receptor-binding region obtained with a combinatorial library. J. Biol. Chem. 271, 361-366 (Pubitemid 26026603)
18. Conklin, B. R., Farfel, Z., Lustig, K. D., Julius, D., and Bourne, H. R. (1993) Substitution of three amino acids switches receptor specificity of Gq α to that of Gi α. Nature 363, 274-276 (Pubitemid 23158533)
19. Conklin, B. R., Herzmark, P., Ishida, S., Voyno-Yasenetskaya, T. A., Sun, Y., Farfel, Z., and Bourne, H. R. (1996) Carboxyl-terminal mutations of Gq α and Gs α that alter the fidelity of receptor activation. Mol. Pharmacol. 50, 885-890 (Pubitemid 26347709)
20. Rovati, G. E., Capra, V., and Neubig, R. R. (2007) The highly conserved DRY motif of class A G protein-coupled receptors: beyond the ground state. Mol. Pharmacol. 71, 959-964 (Pubitemid 46456999)
21. Hofmann, K. P., Scheerer, P., Hildebrand, P. W., Choe, H. W., Park, J. H., Heck, M., and Ernst, O. P. (2009) A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem. Sci. 34, 540-552
22. Wacker, D., Fenalti, G., Brown, M. A., Katritch, V., Abagyan, R., Cherezov, V., and Stevens, R. C. (2010) Conserved binding mode of human β2 adrenergic receptor inverse agonists and antagonist revealed by X-ray crystallography. J. Am. Chem. Soc. 132, 11443-11445
23. Ballesteros, J. A. (2001) Activation of the β2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J. Biol. Chem. 276, 29171-29177
24. Rao, V. R., and Oprian, D. D. (1996) Activating mutations of rhodopsin and other G protein-coupled receptors. Annu. Rev. Biophys. Biomol. Struct. 25, 287-314 (Pubitemid 26197501)
25. Wald, G. (1968) The molecular basis of visual excitation. Nature 219, 800-807
26. Galandrin, S., and Bouvier, M. (2006) Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol. Pharmacol. 70, 1575-1584
27. Locht, C., Coutte, L., and Mielcarek, N. (2011) The ins and outs of pertussis toxin. FEBS J. 278, 4668-4682
28. Clark, M. J., Neubig, R. R., and Traynor, J. R. (2004) Endogenous regulator of G protein signaling proteins suppress Gαo-dependent, mu-opioid agonist-mediated adenylyl cyclase supersensitization. J. Pharmacol. Exp. Ther. 310, 215-222 (Pubitemid 38812714)
29. Fung, J. J., Deupi, X., Pardo, L., Yao, X. J., Velez-Ruiz, G. A., Devree, B. T., Sunahara, R. K., and Kobilka, B. K. (2009) Ligand-regulated oligomerization of β(2)-adrenoceptors in a model lipid bilayer. EMBO J. 28, 3315-3328
30. 35S]GTPγS binding assay: approaches and applications in pharmacology. Life Sci. 74, 489-508
31. Chidiac, P., Hebert, T. E., Valiquette, M., Dennis, M., and Bouvier, M. (1994) Inverse agonist activity of β-adrenergic antagonists. Mol. Pharmacol. 45, 490-499 (Pubitemid 24094939)
32. Samama, P., Cotecchia, S., Costa, T., and Lefkowitz, R. J. (1993) A mutation-induced activated state of the β2-adrenergic receptor. Extending the ternary complex model. J. Biol. Chem. 268, 4625-4636 (Pubitemid 23081571)
33. Kjelsberg, M. A., Cotecchia, S., Ostrowski, J., Caron, M. G., and Lefkowitz, R. J. (1992) Constitutive activation of the α1B-adrenergic receptor by all amino acid substitutions at a single site. Evidence for a region which constrains receptor activation. J. Biol. Chem. 267, 1430-1433
34. De Lean, A., Stadel, J. M., and Lefkowitz, R. J. (1980) A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled β-adrenergic receptor. J. Biol. Chem. 255, 7108-7117 (Pubitemid 11232874)
35. Li, J., Edwards, P. C., Burghammer, M., Villa, C., and Schertler, G. F. (2004) Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343, 1409-1438 (Pubitemid 39387834)
36. Rudling, J. E., Richardson, J., and Evans, P. D. (2000) A comparison of agonist-specific coupling of cloned human α(2)-adrenoceptor subtypes. Br. J. Pharmacol. 131, 933-941
37. Daaka, Y., Luttrell, L. M., and Lefkowitz, R. J. (1997) Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390, 88-91 (Pubitemid 27494762)
38. Xiao, R. P. (2001) β-adrenergic signaling in the heart: dual coupling of the β2-adrenergic receptor to G(s) and G(i) proteins. Sci. STKE 2001, re15
39. Okada, T., Sugihara, M., Bondar, A. N., Elstner, M., Entel, P., and Buss, V. (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J. Mol. Biol. 342, 571-583 (Pubitemid 39149759)
40. Chuang, J. Z., Vega, C., Jun, W., and Sung, C. H. (2004) Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-arrestin complexes. J. Clin. Invest. 114, 131-140 (Pubitemid 39071652)
41. Musarella, M. A., and MacDonald, I. M. (2011) Current concepts in the treatment of retinitis pigmentosa. J. Ophthalmol. 2011, 1-8
42. Daiger, S. P., Bowne, S. J., and Sullivan, L. S. (2007) Perspective on genes and mutations causing retinitis pigmentosa. Arch. Ophthalmol. 125, 151-158
43. Lem, J., and Fain, G. L. (2004) Constitutive opsin signaling: night blindness or retinal degeneration? Trends Mol. Med. 10, 150-157 (Pubitemid 38410972)
44. Kim, J. M., Altenbach, C., Kono, M., Oprian, D. D., Hubbell, W. L., and Khorana, H. G. (2004) Structural origins of constitutive activation in rhodopsin: Role of the K296/E113 salt bridge. Proc. Natl. Acad. Sci. U.S.A. 101, 12508-12513 (Pubitemid 39122054)