Efficacy as an intrinsic property of the M2 muscarinic receptor in its tetrameric state

Biochemistry

Volumn 52, Issue 42, 2013, Pages 7405-7427

  Redka, Dar'Ya S ^a   Heerklotz, Heiko ^a   Wells, James W ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DISPERSIONS; LIGANDS; LIPOSOMES; MONOMERS; OLIGOMERS; PHOSPHOLIPIDS; PURIFICATION;

COOPERATIVE INTERACTIONS; EXPLICIT MODELING; G PROTEIN COUPLED RECEPTORS; INTRINSIC ACTIVITIES; INTRINSIC PROPERTY; MUSCARINIC RECEPTOR; NATURAL MEMBRANES; PHOSPHOLIPID VESICLES;

PROTEINS;

ARECOLINE; ATROPINE; BETHANECHOL; CARBACHOL; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; LIGAND; METHYLSCOPOLAMINE; MONOMER; MUSCARINIC M2 RECEPTOR; MUSCARINIC M2 RECEPTOR AGONIST; MUSCARINIC M2 RECEPTOR ANTAGONIST; N ETHYLMALEIMIDE; OXOTREMORINE M; PILOCARPINE; QUINUCLIDINYLBENZILATE; TETRAMER; UNCLASSIFIED DRUG;

ALLOSTERISM; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG BINDING SITE; DRUG RECEPTOR BINDING; MOLECULAR INTERACTION; NONHUMAN; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; SF9 CELL;

EID: 84886787864     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4003869     Document Type: Article

References (99)

1. Birdsall, N. J., Burgen, A. S., and Hulme, E. C. (1978) The binding of agonists to brain muscarinic receptors Mol. Pharmacol. 14, 723-736
2. Kent, R. S., De Lean, A., and Lefkowitz, R. J. (1980) A quantitative analysis of β-adrenergic receptor interactions: Resolution of high and low affinity states of the receptor by computer modeling of ligand binding data Mol. Pharmacol. 17, 14-23
3. Ehlert, F. J. (1985) The relationship between muscarinic receptor occupancy and adenylate cyclase inhibition in the rabbit myocardium Mol. Pharmacol. 28, 410-421
4. Berrie, C. P., Birdsall, N. J., Burgen, A. S., and Hulme, E. C. (1979) Guanine nucleotides modulate muscarinic receptor binding in the heart Biochem. Biophys. Res. Commun. 87, 1000-1005
5. Sibley, D. R. and Creese, I. (1983) Interactions of ergot alkaloids with anterior pituitary D-2 dopamine receptors Mol. Pharmacol. 23, 585-593
6. 2 serotonin receptors J. Neurochem. 43, 1213-1219
7. 2-adrenergic receptors in purified membranes from human platelets. Implications of receptor-inhibitory nucleotide-binding protein stoichiometry Mol. Pharmacol. 28, 475-486
8. Ross, E. M., Maguire, M. E., Sturgill, T. W., Biltonen, R. L., and Gilman, A. G. (1977) Relationship between the β-adrenergic receptor and adenylate cyclase J. Biol. Chem. 252, 5761-5775
9. 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
10. Bornancin, F., Pfister, C., and Chabre, M. (1989) The transitory complex between photoexcited rhodopsin and transducin. Reciprocal interaction between the retinal site in rhodopsin and the nucleotide site in transducin Eur. J. Biochem. 184, 687-698
11. Onaran, H. O., Costa, T., and Rodbard, D. (1993) βγ subunits of guanine nucleotide-binding proteins and regulation of spontaneous receptor activity: Thermodynamic model for the interaction between receptors and guanine nucleotide-binding protein subunits Mol. Pharmacol. 43, 245-256
12. Conklin, B. R. and Bourne, H. R. (1993) Structural elements of Gα subunits that interact with Gβγ, receptors, and effectors Cell 73, 631-641
13. Birnbaumer, L., Abramowitz, J., and Brown, A. M. (1990) Receptor-effector coupling by G proteins Biochim. Biophys. Acta 1031, 163-224
14. Hargrave, P. A., Hamm, H. E., and Hofmann, K. P. (1993) Interaction of rhodopsin with the G-protein, transducin BioEssays 15, 43-50
15. Limbird, L. E. and Lefkowitz, R. J. (1978) Agonist-induced increase in apparent β-adrenergic receptor size Proc. Natl. Acad. Sci. U.S.A. 75, 228-232
16. Matesic, D. F., Manning, D. R., and Luthin, G. R. (1991) Tissue-dependent association of muscarinic acetylcholine receptors with guanine nucleotide-binding regulatory proteins Mol. Pharmacol. 40, 347-353
17. Kuravi, S., Lan, T. H., Barik, A., and Lambert, N. A. (2010) Third-party bioluminescence resonance energy transfer indicates constitutive association of membrane proteins: Application to class a G-protein-coupled receptors and G-proteins Biophys. J. 98, 2391-2399
18. Yao, X. J., Velez, 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
19. 4 subtypes of muscarinic receptors in transfected CHO cells and of muscarinic receptors in the heart cells revealed by negative antagonists FEBS Lett. 377, 275-279
20. Seifert, R. and Wenzel-Seifert, K. (2002) Constitutive activity of G-protein-coupled receptors: Cause of disease and common property of wild-type receptors Naunyn-Schmiedeberg's Arch. Pharmacol. 366, 381-416
21. 2-adrenergic receptor J. Biol. Chem. 268, 16483-16487
22. Spalding, T. A., Burstein, E. S., Wells, J. W., and Brann, M. R. (1997) Constitutive activation of the m5 muscarinic receptor by a series of mutations at the extracellular end of transmembrane 6 Biochemistry 36, 10109-10116
23. 2 adrenergic receptor: Constitutive activation, structural instability, and conformational rearrangement of transmembrane segment 6 Mol. Pharmacol. 56, 175-184
24. Burstein, E. S., Spalding, T. A., and Brann, M. R. (1997) Pharmacology of muscarinic receptor subtypes constitutively activated by G proteins Mol. Pharmacol. 51, 312-319
25. i protein activation in intact cells involves subunit rearrangement rather than dissociation Proc. Natl. Acad. Sci. U.S.A. 100, 16077-16082
26. Gales, C., Van Durm, J. J., Schaak, S., Pontier, S., Percherancier, Y., Audet, M., Paris, H., and Bouvier, M. (2006) Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes Nat. Struct. Mol. Biol. 13, 778-786
27. Wreggett, K. A. and Wells, J. W. (1995) Cooperativity manifest in the binding properties of purified cardiac muscarinic receptors J. Biol. Chem. 270, 22488-22499
28. Ma, A. W.-S., Pawagi, A. B., and Wells, J. W. (2008) Heterooligomers of the muscarinic receptor and G proteins purified from porcine atria Biochem. Biophys. Res. Commun. 374, 128-133
29. Dupre, D. J., Robitaille, M., Ethier, N., Villeneuve, L. R., Mamarbachi, A. M., and Hebert, T. E. (2006) Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking J. Biol. Chem. 281, 34561-34573
30. Lee, T. W., Sole, M. J., and Wells, J. W. (1986) Assessment of a ternary model for the binding of agonists to neurohumoral receptors Biochemistry 25, 7009-7020
31. Green, M. A., Chidiac, P., and Wells, J. W. (1997) Cardiac muscarinic receptors. Relationship between the G protein and multiple states of affinity Biochemistry 36, 7380-7394
32. Minton, A. P. and Sokolovsky, M. (1990) A model for the interaction of muscarinic receptors, agonists, and two distinct effector substances Biochemistry 29, 1586-1593
33. Sternweis, P. C. and Robishaw, J. D. (1984) Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain J. Biol. Chem. 259, 13806-13813
34. Peterson, G. L., Herron, G. S., Yamaki, M., Fullerton, D. S., and Schimerlik, M. I. (1984) Purification of the muscarinic acetylcholine receptor from porcine atria Proc. Natl. Acad. Sci. U.S.A. 81, 4993-4997
35. o) J. Biol. Chem. 261, 10133-10140
36. Peterson, G. L., Toumadje, A., Johnson, W. C., Jr., and Schimerlik, M. I. (1995) Purification of recombinant porcine m2 muscarinic acetylcholine receptor from Chinese hamster ovary cells. Circular dichroism spectra and ligand binding properties J. Biol. Chem. 270, 17808-17814
37. Gomes, I., Jordan, B. A., Gupta, A., Rios, C., Trapaidze, N., and Devi, L. A. (2001) G protein coupled receptor dimerization: Implications in modulating receptor function J. Mol. Med. 79, 226-242
38. Park, P. S., Filipek, S., Wells, J. W., and Palczewski, K. (2004) Oligomerization of G protein-coupled receptors: Past, present, and future Biochemistry 43, 15643-15656
39. Zeng, F. and Wess, J. (2000) Molecular aspects of muscarinic receptor dimerization Neuropsychopharmacology 23, S19-S31
40. Goin, J. C. and Nathanson, N. M. (2006) Quantitative analysis of muscarinic acetylcholine receptor homo- and heterodimerization in live cells: Regulation of receptor down-regulation by heterodimerization J. Biol. Chem. 281, 5416-5425
41. 2 muscarinic cholinergic receptor J. Neurochem. 90, 537-548
42. 2 muscarinic receptor in live cells as determined by quantitative fluorescence resonance energy transfer J. Biol. Chem. 285, 16723-16738
43. Nakamura, S. and Rodbell, M. (1991) Glucagon induces disaggregation of polymer-like structures of the α subunit of the stimulatory G protein in liver membranes Proc. Natl. Acad. Sci. U.S.A. 88, 7150-7154
44. oα induced by guanosine-5′-3-O-(thio) triphosphate activation Biochemistry (Moscow) 68, 121-128
45. Chidiac, P. and Wells, J. W. (1992) Effects of adenyl nucleotides and carbachol on cooperative interactions among G proteins Biochemistry 31, 10908-10921
46. Tota, M. R., Kahler, K. R., and Schimerlik, M. I. (1987) Reconstitution of the purified porcine atrial muscarinic acetylcholine receptor with purified porcine atrial inhibitory guanine nucleotide binding protein Biochemistry 26, 8175-8182
47. Ikegaya, T., Nishiyama, T., Haga, K., Haga, T., Ichiyama, A., Kobayashi, A., and Yamazaki, N. (1990) Interaction of atrial muscarinic receptors with three kinds of GTP-binding proteins J. Mol. Cell. Cardiol. 22, 343-351
48. Sum, C. S., Park, P. S., and Wells, J. W. (2002) Effects of N -ethylmaleimide on conformational equilibria in purified cardiac muscarinic receptors J. Biol. Chem. 277, 36188-36203
49. Chidiac, P., Green, M. A., Pawagi, A. B., and Wells, J. W. (1997) Cardiac muscarinic receptors. Cooperativity as the basis for multiple states of affinity Biochemistry 36, 7361-7379
50. 2 muscarinic cholinergic receptor are reconstituted into phospholipid vesicles Biochemistry 46, 7907-7927
51. 2 muscarinic cholinergic receptor purified from Sf 9 cells Biochemistry 42, 12960-12971
52. Rasband, W. S. (1997-2012) ImageJ, National Institutes of Health, Bethesda, MD.
53. Wells, J. W. (1992) in Receptor-Ligand Interactions. A Practical Approach (Hulme, E. C., Ed.) pp 289-395, Oxford University Press, Oxford, England.
54. 2 muscarinic cholinergic receptor Mol. Pharmacol. 74, 834-843
55. Aronstam, R. S., Hoss, W., and Abood, L. G. (1977) Conversion between configurational states of the muscarinic receptor in rat brain Eur. J. Pharmacol. 46, 279-282
56. Ehlert, F. J., Roeske, W. R., and Yamamura, H. I. (1980) Regulation of muscarinic receptor binding by guanine nucleotides and N -ethylmaleimide J. Supramol. Struct. 14, 149-162
57. Sum, C. S., Pyo, N., and Wells, J. W. (2001) Apparent capacity of cardiac muscarinic receptors for different radiolabeled antagonists Biochem. Pharmacol. 62, 829-851
58. 3H]histamine in guinea pig cerebral cortex. II. Mechanistic basis for multiple states of affinity Mol. Pharmacol. 43, 583-594
59. Park, P. S., Sum, C. S., Pawagi, A. B., and Wells, J. W. (2002) Cooperativity and oligomeric status of cardiac muscarinic cholinergic receptors Biochemistry 41, 5588-5604
60. 2 muscarinic receptors in Sf 9 cells: Characterisation and reconstitution with G-proteins J. Recept. Signal Transduction Res. 15, 55-70
61. Knight, P. J. and Grigliatti, T. A. (2004) Diversity of G proteins in Lepidopteran cell lines: Partial sequences of six G protein α subunits Arch. Insect Biochem. Physiol. 57, 142-150
62. 2 muscarinic receptor activation of different G protein subtypes Neurochem. Int. 44, 119-124
63. i1 fusion protein J. Biochem. 135, 589-596
64. sα fusion protein Eur. J. Biochem. 255, 369-382
65. Ehlert, F. J. and Rathbun, B. E. (1990) Signaling through the muscarinic receptor-adenylate cyclase system of the heart is buffered against GTP over a range of concentrations Mol. Pharmacol. 38, 148-158
66. Hulme, E. C., Berrie, C. P., Birdsall, N. J., and Burgen, A. S. (1981) Two populations of binding sites for muscarinic antagonists in the rat heart Eur. J. Pharmacol. 73, 137-142
67. Vanderheyden, P., Andre, C., de Backer, J. P., and Vauquelin, G. (1984) Agonist mediated conformational changes of solubilized calf forebrain muscarinic acetylcholine receptors Biochem. Pharmacol. 33, 2981-2987
68. Bayburt, T. H., Vishnivetskiy, S. A., McLean, M. A., Morizumi, T., Huang, C. C., Tesmer, J. J., Ernst, O. P., Sligar, S. G., and Gurevich, V. V. (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding J. Biol. Chem. 286, 1420-1428
69. 2 muscarinic acetylcholine receptor bound to an antagonist Nature 482, 547-551
70. Vogel, W. K., Sheehan, D. M., and Schimerlik, M. I. (1997) Site-directed mutagenesis on the m2 muscarinic acetylcholine receptor: The significance of Tyr403 in the binding of agonists and functional coupling Mol. Pharmacol. 52, 1087-1094
71. 2 muscarinic acetylcholine receptors that contribute to ligand-selective signaling bias J. Biol. Chem. 285, 7459-7474
72. Valant, C., Gregory, K. J., Hall, N. E., Scammells, P. J., Lew, M. J., Sexton, P. M., and Christopoulos, A. (2008) A novel mechanism of G protein-coupled receptor functional selectivity. Muscarinic partial agonist McN-A-343 as a bitopic orthosteric/allosteric ligand J. Biol. Chem. 283, 29312-29321
73. 2 muscarinic receptor Biochemistry 51, 4518-4540
74. Bock, A., Merten, N., Schrage, R., Dallanoce, C., Batz, J., Klockner, J., Schmitz, J., Matera, C., Simon, K., Kebig, A., Peters, L., Muller, A., Schrobang-Ley, J., Trankle, C., Hoffmann, C., De Amici, M., Holzgrabe, U., Kostenis, E., and Mohr, K. (2012) The allosteric vestibule of a seven transmembrane helical receptor controls G-protein coupling Nat. Commun. 3, 1044
75. 2 dopamine receptor Mol. Pharmacol. 69, 226-235
76. Casado, V., Ferrada, C., Bonaventura, J., Gracia, E., Mallol, J., Canela, E. I., Lluis, C., Cortes, A., and Franco, R. (2009) Useful pharmacological parameters for G-protein-coupled receptor homodimers obtained from competition experiments. Agonist-antagonist binding modulation Biochem. Pharmacol. 78, 1456-1463
77. Urizar, E., Montanelli, L., Loy, T., Bonomi, M., Swillens, S., Gales, C., Bouvier, M., Smits, G., Vassart, G., and Costagliola, S. (2005) Glycoprotein hormone receptors: Link between receptor homodimerization and negative cooperativity EMBO J. 24, 1954-1964
78. Albizu, L., Balestre, M. N., Breton, C., Pin, J. P., Manning, M., Mouillac, B., Barberis, C., and Durroux, T. (2006) Probing the existence of G protein-coupled receptor dimers by positive and negative ligand-dependent cooperative binding Mol. Pharmacol. 70, 1783-1791
79. 2 dopamine receptor: Evidence from agonist dissociation kinetics J. Neurochem. 112, 1442-1453
80. Albizu, L., Cottet, M., Kralikova, M., Stoev, S., Seyer, R., Brabet, I., Roux, T., Bazin, H., Bourrier, E., Lamarque, L., Breton, C., Rives, M. L., Newman, A., Javitch, J., Trinquet, E., Manning, M., Pin, J. P., Mouillac, B., and Durroux, T. (2010) Time-resolved FRET between GPCR ligands reveals oligomers in native tissues Nat. Chem. Biol. 6, 587-594
81. Neri, M., Vanni, S., Tavernelli, I., and Rothlisberger, U. (2010) Role of aggregation in rhodopsin signal transduction Biochemistry 49, 4827-4832
82. Pin, J. P., Kniazeff, J., Liu, J., Binet, V., Goudet, C., Rondard, P., and Prezeau, L. (2005) Allosteric functioning of dimeric class C G-protein-coupled receptors FEBS J. 272, 2947-2955
83. Han, Y., Moreira, I. S., Urizar, E., Weinstein, H., and Javitch, J. A. (2009) Allosteric communication between protomers of dopamine class A GPCR dimers modulates activation Nat. Chem. Biol. 5, 688-695
84. 4 receptor BLT1 and the G-protein J. Mol. Biol. 329, 815-829
85. Filipek, S., Krzysko, K. A., Fotiadis, D., Liang, Y., Saperstein, D. A., Engel, A., and Palczewski, K. (2004) A concept for G protein activation by G protein-coupled receptor dimers: The transducin/rhodopsin interface Photochem. Photobiol. Sci. 3, 628-638
86. 2A receptors assemble into higher-order oligomers at the plasma membrane FEBS Lett. 582, 3985-3990
87. Carriba, P., Navarro, G., Ciruela, F., Ferre, S., Casado, V., Agnati, L., Cortes, A., Mallol, J., Fuxe, K., Canela, E. I., Lluis, C., and Franco, R. (2008) Detection of heteromerization of more than two proteins by sequential BRET-FRET Nat. Methods 5, 727-733
88. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M., and Javitch, J. A. (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels EMBO J. 27, 2293-2304
89. 1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules Proc. Natl. Acad. Sci. U.S.A. 107, 2693-2698
90. Calebiro, D., Rieken, F., Wagner, J., Sungkaworn, T., Zabel, U., Borzi, A., Cocucci, E., Zurn, A., and Lohse, M. J. (2013) Single-molecule analysis of fluorescently labeled G-protein-coupled receptors reveals complexes with distinct dynamics and organization Proc. Natl. Acad. Sci. U.S.A. 110, 743-748
91. Golebiewska, U., Johnston, J. M., Devi, L., Filizola, M., and Scarlata, S. (2011) Differential response to morphine of the oligomeric state of μ-opioid in the presence of δ-opioid receptors Biochemistry 50, 2829
92. 2C) receptor revealed by fluorescence correlation spectroscopy with photon counting histogram analysis: Evidence for homodimers without monomers or tetramers J. Biol. Chem. 287, 23604-23614
93. Ianoul, A., Grant, D. D., Rouleau, Y., Bani-Yaghoub, M., Johnston, L. J., and Pezacki, J. P. (2005) Imaging nanometer domains of β-adrenergic receptor complexes on the surface of cardiac myocytes Nat. Chem. Biol. 1, 196-202
94. Milligan, G. (2010) The role of dimerisation in the cellular trafficking of G-protein-coupled receptors Curr. Opin. Pharmacol. 10, 23-29
95. Milligan, G. (2009) G protein-coupled receptor hetero-dimerization: Contribution to pharmacology and function Br. J. Pharmacol. 158, 5-14
96. Bayburt, T. H., Leitz, A. J., Xie, G., Oprian, D. D., and Sligar, S. G. (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins J. Biol. Chem. 282, 14875-14881
97. Ernst, O. P., Gramse, V., Kolbe, M., Hofmann, K. P., and Heck, M. (2007) Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit Proc. Natl. Acad. Sci. U.S.A. 104, 10859-10864
98. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein Proc. Natl. Acad. Sci. U.S.A. 104, 7682-7687
99. Wong, H. M., Sole, M. J., and Wells, J. W. (1986) Assessment of mechanistic proposals for the binding of agonists to cardiac muscarinic receptors Biochemistry 25, 6995-7008