A conformation-equilibrium model captures ligand-ligand interactions and ligand-biased signalling by G-protein coupled receptors

FEBS Journal

Volumn 281, Issue 20, 2014, Pages 4659-4671

  Roth, Susanne ^a   Bruggeman, Frank J ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Allostery; Cooperativity; G protein coupled receptors; Ligand biased signalling; MWC model

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LIGAND;

ALLOSTERISM; ARTICLE; CONCENTRATION RESPONSE; CONFORMATION EQUILIBRIUM MODEL; CONFORMATIONAL TRANSITION; DISSOCIATION CONSTANT; INTRACELLULAR SIGNALING; LIGAND BINDING; LIGAND LIGAND INTERACTION; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MOLECULAR INTERACTION; PARTITION COEFFICIENT; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROCESSING; RECEPTOR AFFINITY; RECEPTOR SENSITIVITY; SIGNAL TRANSDUCTION; CHEMISTRY; HUMAN; METABOLISM; THEORETICAL MODEL;

ALLOSTERIC REGULATION; HUMANS; LIGANDS; MODELS, THEORETICAL; PROTEIN CONFORMATION; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84915818939     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12970     Document Type: Article

References (42)

1. Lee JY & Lyman E (2012) Agonist dynamics and conformational selection during microsecond simulations of the a(2a) adenosine receptor. Biophys J 102: 2114-2120.
2. Nygaard R, Zou Y, Dror RO, Mildorf TJ, Arlow DH, Manglik A, Pan AC, Liu CW, Fung JJ, Bokoch MP et al. (2013) The dynamic process of (2)-adrenergic receptor activation. Cell 152, 532-542.
3. Preininger AM,Meiler J ,Hamm HE (2013),Conformational flexibility and structural dynamics in GPCR-mediated G protein activation: a perspective, J Mol Biol, 425, 2288-2298.
4. Marcaggi P, Mutoh H, Dimit rov D, Beato M & Kn opfel T (2009) Optical measurement of mglur1 conformational changes reveals fast activation, slow deactivation, and sensitization. Proc Natl Acad Sci USA 106, 11388-11393.
5. N ikolaev VO, Hoffmann C, B unemann M, Lohse MJ & Vilardaga JP (2006) Molecular basis of partial agonism at the neurotransmitter alpha2a-adrenergic receptor and gi-protein heterotrimer. J Biol Chem 281, 24506-245 11.
6. Swaminath G, Deupi X, Lee TW, Zhu W, Thian FS, Kobilka TS & Kobilka B (2005) Probing the beta2 adrenoceptor binding site with catechol reveals differences in binding and activation by agonis ts and partial agonists. J Biol Chem 280, 22165-22171.
7. Kobilka BK & Deupi X (2007) Conformational complexity of G-protein coupled receptors. Trends Pharmacol Sci 28, 397-406.
8. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, Choe HW, Hofmann KP & Ernst OP (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497- 502.
9. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D et al. (2011) Crystal structure of the b2 adrenergic receptor-Gs protein comp lex. Nature 477, 549-555.
10. Thomsen AR, Hvidtfeldt M & Brauner-Osborne H (2012) Biased agonism of the calcium-sensing receptor. Cell Calcium 51, 107-116.
11. Drake MT, Violin JD, Whalen EJ, Wisler JW, Shenoy SK & Lefkowitz RJ (2008) Beta-arrestin-biased agonism at the beta2-adrenergic receptor. J Biol Chem 283, 5669-5676.
12. Liu JJ, Ho rst R, Katritch V, Stevens RC & Wuthrich K (2012) Biased signaling pathways in b2-adrenergic receptor characterized by 19F-NMR. Science 335, 1106-1110.
13. Davey AE, Leach K, Valant C, Conigrave AD, Sexton PM & Christopoulos A (2012) Positive and negative allosteric modulators promote biased signaling at the calcium-sensing receptor. Endocrinology 153, 1232-1241.
14. Thomsen AR, Worm J, Jacobsen SE, Stahlhut M, Latta M & Br auner-Osborne H (2012) Strontium is a biased agonist of the calcium-sensing receptor in rat medullary thyroid carcinoma 6-23 cells. J Pharmacol Exp Ther 343, 638-649.
15. Katritch V, Cherezov V & Stevens RC (2013) Structure-function of the G protein-coupled receptor superfamily. Annu Rev Pharmacol Toxicol 53, 531-556.
16. Vauquelin G & Van Liefde I (2005) G protein-coupled receptors: a count of 1001 conformations. Fundam Clin Pharmacol 19, 45-56.
17. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF & Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194.
18. Gurevich VV & Gurevich EV (2008) How and why do GPCRs dimerize? Trends Pharmacol Sci 29, 234-240.
19. Pellissier LP, Barthet G, Gaven F, Cassier E, Trinquet E, Pin JP, Marin P, Dumuis A, Bockaert J, Ban-eres JL et al. (2011) G protein activation by serotonin type 4 receptor dimers: evidence that turning on two protomers is more efficient. J Biol Chem 286, 9985-9997.
20. Guo W, Urizar E, Kralikova M, Mobarec JC, Shi L, Filizola M & Jav itch JA (2008) Dopamine d2 receptors form higher order oligomers at physiological expression levels. EMBO J 27, 2293-2304.
21. Jastrzebska B, Orban T, Golczak M, Engel A & Palczewski K (2013) Asymmetry of the rhodopsin dimer in complex with transducin. FASEB J 27, 1572-1584.
22. Vilardaga JP, Nikolaev VO, Lorenz K, Ferrandon S, Zhuang Z & Lohse MJ (2008) Conformati onal cross-talk between alpha2a-adrenergic and mu-opioid receptors controls cell signaling. Nat Chem Biol 4, 126-131.
23. Monod J, Wyman J & Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12, 88-118.
24. Cui Q,Karplus M, 2008, Allostery and cooperativity revisited, Protein Sci, 17, 1295-1307.
25. Changeux JP Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428.
26. Koshland DE, N-emethy G & Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
27. Ehlert FJ (2005) Analysis of allosterism in functional assays. J Pharmacol Exp Ther 315, 740-754.
28. Kenakin T (2005) New concepts in drug discovery: collateral efficacy and permissive antagonism. Nat Rev Drug Discov 4, 919-927.
29. Hall DA (2000) Modeling the functional effects o f allosteric modulators at pharmacological receptors: an extension of the two-state model of receptor activation. Mol Pharmacol 58, 1412-1423.
30. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, Devree BT, Rosenbaum DM, Thian FS, Kobilka TS et al. (2011) Structure of a nanobodystabilized active state of the (2) adrenoceptor. Nature 469, 175-180.
31. Adair GS (1925) Th e hemoglobin system. vi. The oxygen dissociation curve of hemoglobin. J Biol Chem 63, 529-545.
32. Klotz IM & Hunston DL (1975) Protein interactions with small molecules. Relationships between stoichi ometric binding constants, site binding constants, and empirical binding parameters. J Biol Chem 250, 3001-3009.
33. Hilser VJ, Wrabl JO & Motlagh HN (2012) Structural and energetic basis of allostery. Annu Rev Biophys 41, 585-609.
34. Marzen S, Garcia HG & Phillips R (2013) Statistical mechanics of Monod-Wyman-Changeux (MWC) models. J Mol Biol 425, 1433-1460.
35. Leach K, Wen A, Davey AE, Sexton PM, Conigrave AD & Christopoulos A (2012) Identification of molecular phenotypes and biased signaling induced by naturally occurring mutations of the human calcium-sensing receptor. Endocrinology 153: 4304-4316.
36. Deupi X & Kobilka BK (2010) Energy landscapes as a tool to integrate GPCR structure, dynamics, and function. Physiology (Bethesda) 25, 293-303.
37. Nygaard R, Frimurer TM, Holst B, Rosenkilde MM & Schwartz TW (2009) Ligand binding and microswitches in 7tm receptor structures. Trends Pharmacol Sci 30, 249-259.
38. Vardy E & Roth BL (2013) Conformational ensembles in GPCR activation. Cell 152, 385-386.
39. Han G & Hampson DR (1999) Ligand binding to the amino-terminal domain of the mglur4 subtype of metabotropic glutamate receptor. J Biol Chem 274, 10008-10013.
40. Canals M, Lane JR, Wen A, Scammells PJ, Sexton PM & Christopoulos A (2012) A Monod-Wyman-Changeux mechanism can explain G protein-coupl ed receptor (GPCR) allosteric modulation. J Biol Chem 287, 650-659.
41. Ehlert FJ & Griffin MT (2008) Two-state models and the analysis of the allosteric effect of gallamine at the m2 muscarinic receptor. J Pharmacol Exp Ther 325, 1039-1060.
42. Leach K, Sexton PM & Christopoulos A (2007) Allosteric GPCR modulators: taking advantage of permissive receptor pharmacology. Trends Pharmacol Sci 28, 382-389.