Ligand-Induced Coupling between Oligomers of the M2 Receptor and the Gi1 Protein in Live Cells

Biophysical Journal

Volumn 115, Issue 5, 2018, Pages 881-895

  Li, Yuchong ^a   Shivnaraine, Rabindra V ^a   Huang, Fei ^a   Wells, James W ^a   Gradinaru, Claudiu C ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; MUSCARINIC M2 RECEPTOR;

ANIMAL; CELL SURVIVAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; CHO CELLS; CRICETULUS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; LIGANDS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR, MUSCARINIC M2; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 85051646805     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2018.08.001     Document Type: Article

References (82)

1. Wacker, D., Stevens, R.C., Roth, B.L., How ligands illuminate GPCR molecular pharmacology. Cell 170 (2017), 414–427.
2. Rosenbaum, D.M., Rasmussen, S.G., Kobilka, B.K., The structure and function of G-protein-coupled receptors. Nature 459 (2009), 356–363.
3. Manglik, A., Kruse, A.C., Structural basis for G protein-coupled receptor activation. Biochemistry 56 (2017), 5628–5634.
4. Whorton, M.R., Bokoch, M.P., et al., Sunahara, R.K., A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. USA 104 (2007), 7682–7687.
5. Kuszak, A.J., Pitchiaya, S., et al., Sunahara, R.K., Purification and functional reconstitution of monomeric mu-opioid receptors: allosteric modulation of agonist binding by Gi2. J. Biol. Chem 284 (2009), 26732–26741.
6. De Lean, A., Stadel, J.M., Lefkowitz, R.J., A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled beta-adrenergic receptor. J. Biol. Chem 255 (1980), 7108–7117.
7. Marsango, S., Ward, R.J., et al., Milligan, G., Muscarinic receptor oligomerization. Neuropharmacology 136 (2018), 401–410.
8. Ferré S., Casadó V., et al., Guitart, X., G protein-coupled receptor oligomerization revisited: functional and pharmacological perspectives. Pharmacol. Rev 66 (2014), 413–434.
9. Redka, D.S., Heerklotz, H., Wells, J.W., Efficacy as an intrinsic property of the M(2) muscarinic receptor in its tetrameric state. Biochemistry 52 (2013), 7405–7427.
10. Redka, D.S., Morizumi, T., et al., Wells, J.W., Coupling of g proteins to reconstituted monomers and tetramers of the M2 muscarinic receptor. J. Biol. Chem 289 (2014), 24347–24365.
11. Shivnaraine, R.V., Fernandes, D.D., et al., Gradinaru, C.C., Single-molecule analysis of the supramolecular organization of the M2 muscarinic receptor and the Gαi1 protein. J. Am. Chem. Soc 138 (2016), 11583–11598.
12. Calebiro, D., Rieken, F., et al., Lohse, M.J., Single-molecule analysis of fluorescently labeled G-protein-coupled receptors reveals complexes with distinct dynamics and organization. Proc. Natl. Acad. Sci. USA 110 (2013), 743–748.
13. Palczewski, K., Oligomeric forms of G protein-coupled receptors (GPCRs). Trends Biochem. Sci 35 (2010), 595–600.
14. Tabor, A., Weisenburger, S., et al., Gmeiner, P., Visualization and ligand-induced modulation of dopamine receptor dimerization at the single molecule level. Sci. Rep, 6, 2016, 33233.
15. Jonas, K.C., Fanelli, F., et al., Hanyaloglu, A.C., Single molecule analysis of functionally asymmetric G protein-coupled receptor (GPCR) oligomers reveals diverse spatial and structural assemblies. J. Biol. Chem 290 (2015), 3875–3892.
16. Yang, H., Qu, L., et al., Huang, Y., Palmitoylation participates in G protein coupled signal transduction by affecting its oligomerization. Mol. Membr. Biol 25 (2008), 58–71.
17. Hein, P., Frank, M., et al., Bünemann, M., Dynamics of receptor/G protein coupling in living cells. EMBO J 24 (2005), 4106–4114.
18. Lober, R.M., Pereira, M.A., Lambert, N.A., Rapid activation of inwardly rectifying potassium channels by immobile G-protein-coupled receptors. J. Neurosci 26 (2006), 12602–12608.
19. Korenbrot, J.I., Speed, sensitivity, and stability of the light response in rod and cone photoreceptors: facts and models. Prog. Retin. Eye Res 31 (2012), 442–466.
20. Falkenburger, B.H., Jensen, J.B., Hille, B., Kinetics of M1 muscarinic receptor and G protein signaling to phospholipase C in living cells. J. Gen. Physiol 135 (2010), 81–97.
21. Sykes, D.A., Dowling, M.R., et al., Charlton, S.J., The Influence of receptor kinetics on the onset and duration of action and the therapeutic index of NVA237 and tiotropium. J. Pharmacol. Exp. Ther 343 (2012), 520–528.
22. Stein, R.S., Ehlert, F.J., A kinetic model of GPCRs: analysis of G protein activity, occupancy, coupling and receptor-state affinity constants. J. Recept. Signal Transduct. Res 35 (2015), 269–283.
23. Oldham, W.M., Hamm, H.E., Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol 9 (2008), 60–71.
24. Qin, K., Dong, C., et al., Lambert, N.A., Inactive-state preassembly of G(q)-coupled receptors and G(q) heterotrimers. Nat. Chem. Biol 7 (2011), 740–747.
25. Kusumi, A., Suzuki, K.G., et al., Fujiwara, T.K., Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci 36 (2011), 604–615.
26. 2 muscarinic acetylcholine receptors in live cardiac muscle. J. Mol. Cell. Cardiol 57 (2013), 129–136.
27. Sungkaworn, T., Jobin, M.L., et al., Calebiro, D., Single-molecule imaging reveals receptor-G protein interactions at cell surface hot spots. Nature 550 (2017), 543–547.
28. Bacia, K., Kim, S.A., Schwille, P., Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 3 (2006), 83–89.
29. Comar, W.D., Schubert, S.M., et al., Smith, A.W., Time-resolved fluorescence spectroscopy measures clustering and mobility of a G protein-coupled receptor opsin in live cell membranes. J. Am. Chem. Soc 136 (2014), 8342–8349.
30. Lohse, M.J., Hoffmann, C., et al., Bünemann, M., Kinetic analysis of G protein-coupled receptor signaling using fluorescence resonance energy transfer in living cells. Adv. Protein Chem 74 (2007), 167–188.
31. Pisterzi, L.F., Jansma, D.B., et al., Wells, J.W., Oligomeric size of the m2 muscarinic receptor in live cells as determined by quantitative fluorescence resonance energy transfer. J. Biol. Chem 285 (2010), 16723–16738.
32. Lommerse, P.H., Snaar-Jagalska, B.E., et al., Schmidt, T., Single-molecule diffusion measurements of H-Ras at the plasma membrane of live cells reveal microdomain localization upon activation. J. Cell Sci 118 (2005), 1799–1809.
33. Wiseman, P.W., Image correlation spectroscopy: mapping correlations in space, time, and reciprocal space. Methods Enzymol 518 (2013), 245–267.
34. Godin, A.G., Costantino, S., et al., Wiseman, P.W., Revealing protein oligomerization and densities in situ using spatial intensity distribution analysis. Proc. Natl. Acad. Sci. USA 108 (2011), 7010–7015.
35. Pediani, J.D., Ward, R.J., et al., Milligan, G., Dynamic regulation of quaternary organization of the M1 muscarinic receptor by subtype-selective antagonist drugs. J. Biol. Chem 291 (2016), 13132–13146.
36. Shivnaraine, R.V., Kelly, B., et al., Wells, J.W., Allosteric modulation in monomers and oligomers of a G protein-coupled receptor. eLife, 5, 2016, e11685.
37. Park, P., Sum, C.S., et al., Wells, J.W., Nature of the oligomers formed by muscarinic m2 acetylcholine receptors in Sf9 cells. Eur. J. Pharmacol 421 (2001), 11–22.
38. Park, P.S., Wells, J.W., Monomers and oligomers of the M2 muscarinic cholinergic receptor purified from Sf9 cells. Biochemistry 42 (2003), 12960–12971.
39. Shivnaraine, R.V., Huang, X.P., et al., Wells, J.W., Heterotropic cooperativity within and between protomers of an oligomeric M(2) muscarinic receptor. Biochemistry 51 (2012), 4518–4540.
40. Liu, B., Chia, D., et al., Gradinaru, C.C., The effect of intrachain electrostatic repulsion on conformational disorder and dynamics of the Sic1 protein. J. Phys. Chem. B 118 (2014), 4088–4097.
41. Zhang, Z., Yomo, D., Gradinaru, C., Choosing the right fluorophore for single-molecule fluorescence studies in a lipid environment. Biochim. Biophys. Acta 1859 (2017), 1242–1253.
42. Haustein, E., Schwille, P., Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct 36 (2007), 151–169.
43. Gendron, P.O., Avaltroni, F., Wilkinson, K.J., Diffusion coefficients of several rhodamine derivatives as determined by pulsed field gradient-nuclear magnetic resonance and fluorescence correlation spectroscopy. J. Fluoresc 18 (2008), 1093–1101.
44. Vámosi, G., Mücke, N., et al., Tóth, K., EGFP oligomers as natural fluorescence and hydrodynamic standards. Sci. Rep, 6, 2016, 33022.
45. Mazouchi, A., Liu, B., et al., Gradinaru, C.C., On the performance of bioanalytical fluorescence correlation spectroscopy measurements in a multiparameter photon-counting microscope. Anal. Chim. Acta 688 (2011), 61–69.
46. Foo, Y.H., Naredi-Rainer, N., et al., Wohland, T., Factors affecting the quantification of biomolecular interactions by fluorescence cross-correlation spectroscopy. Biophys. J 102 (2012), 1174–1183.
47. Bacia, K., Petrášek, Z., Schwille, P., Correcting for spectral cross-talk in dual-color fluorescence cross-correlation spectroscopy. ChemPhysChem 13 (2012), 1221–1231.
48. Chen, P.C., Hub, J.S., Structural properties of protein-detergent complexes from SAXS and MD simulations. J. Phys. Chem. Lett 6 (2015), 5116–5121.
49. Grisshammer, R., Purification of recombinant G-protein-coupled receptors. Methods Enzymol 463 (2009), 631–645.
50. Ma, A.W., Pawagi, A.B., Wells, J.W., Heterooligomers of the muscarinic receptor and G proteins purified from porcine atria. Biochem. Biophys. Res. Commun 374 (2008), 128–133.
51. Nakamura, S., Rodbell, M., Glucagon induces disaggregation of polymer-like structures of the alpha subunit of the stimulatory G protein in liver membranes. Proc. Natl. Acad. Sci. USA 88 (1991), 7150–7154.
52. Jahangeer, S., Rodbell, M., The disaggregation theory of signal transduction revisited: further evidence that G proteins are multimeric and disaggregate to monomers when activated. Proc. Natl. Acad. Sci. USA 90 (1993), 8782–8786.
53. Elmore, S., Apoptosis: a review of programmed cell death. Toxicol. Pathol 35 (2007), 495–516.
54. Weiss, M., Hashimoto, H., Nilsson, T., Anomalous protein diffusion in living cells as seen by fluorescence correlation spectroscopy. Biophys. J 84 (2003), 4043–4052.
55. Wachsmuth, M., Waldeck, W., Langowski, J., Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J. Mol. Biol 298 (2000), 677–689.
56. Tuteja, N., Signaling through G protein coupled receptors. Plant Signal. Behav 4 (2009), 942–947.
57. Herrick-Davis, K., Grinde, E., et al., Mazurkiewicz, J.E., Fluorescence correlation spectroscopy analysis of serotonin, adrenergic, muscarinic, and dopamine receptor dimerization: the oligomer number puzzle. Mol. Pharmacol 84 (2013), 630–642.
58. Lachance, M., Ethier, N., et al., Hébert, T.E., Stable association of G proteins with beta 2AR is independent of the state of receptor activation. Cell. Signal 11 (1999), 523–533.
59. Nobles, M., Benians, A., Tinker, A., Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc. Natl. Acad. Sci. USA 102 (2005), 18706–18711.
60. Zacharias, N., Dougherty, D.A., Cation-π interactions in ligand recognition and catalysis. Trends Pharmacol. Sci 23 (2002), 281–287.
61. Haga, K., Kruse, A.C., et al., Kobayashi, T., Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482 (2012), 547–551.
62. Kruse, A.C., Ring, A.M., et al., Kobilka, B.K., Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 504 (2013), 101–106.
63. Wall, M.A., Coleman, D.E., et al., Sprang, S.R., The structure of the G protein heterotrimer Gi α 1 β 1 γ 2. Cell 83 (1995), 1047–1058.
64. Bacia, K., Schwille, P., Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nat. Protoc 2 (2007), 2842–2856.
65. Adams, P.R., Acetylcholine receptor kinetics. J. Membr. Biol 58 (1981), 161–174.
66. Kyrozis, A., Albuquerque, C., et al., MacDermott, A.B., Ca(2+)-dependent inactivation of NMDA receptors: fast kinetics and high Ca2+ sensitivity in rat dorsal horn neurons. J. Physiol 495 (1996), 449–463.
67. Ackers, G.K., Doyle, M.L., et al., Daugherty, M.A., Molecular code for cooperativity in hemoglobin. Science 255 (1992), 54–63.
68. Riggs, A.F., Self-association, cooperativity and supercooperativity of oxygen binding by hemoglobins. J. Exp. Biol 201 (1998), 1073–1084.
69. Kniazeff, J., Prézeau, L., et al., Goudet, C., Dimers and beyond: The functional puzzles of class C GPCRs. Pharmacol. Ther 130 (2011), 9–25.
70. Zhang, X.C., Liu, J., Jiang, D., Why is dimerization essential for class-C GPCR function? New insights from mGluR1 crystal structure analysis. Protein Cell 5 (2014), 492–495.
71. Petersen, J., Wright, S.C., et al., Schulte, G., Agonist-induced dimer dissociation as a macromolecular step in G protein-coupled receptor signaling. Nat. Commun., 8, 2017, 226.
72. Chidiac, P., Wells, J.W., Effects of adenyl nucleotides and carbachol on cooperative interactions among G proteins. Biochemistry 31 (1992), 10908–10921.
73. Chidiac, P., Green, M.A., et al., Wells, J.W., Cardiac muscarinic receptors. Cooperativity as the basis for multiple states of affinity. Biochemistry 36 (1997), 7361–7379.
74. Ma, A.W., Redka, D.S., et al., Wells, J.W., Recovery of oligomers and cooperativity when monomers of the M2 muscarinic cholinergic receptor are reconstituted into phospholipid vesicles. Biochemistry 46 (2007), 7907–7927.
75. Ashkenazi, A., Winslow, J.W., et al., Ramachandran, J., An M2 muscarinic receptor subtype coupled to both adenylyl cyclase and phosphoinositide turnover. Science 238 (1987), 672–676.
76. Parker, E.M., Kameyama, K., et al., Ross, E.M., Reconstitutively active G protein-coupled receptors purified from baculovirus-infected insect cells. J. Biol. Chem. 266 (1991), 519–527.
77. Shivnaraine, R.V., Fernandes, D.D., et al., Gradinaru, C.C., Single-molecule analysis of the supramolecular organization of the M2 muscarinic receptor and the Gαi1 protein. Journal of the American Chemical Society 138 (2016), 11583–11598.
78. Meyer, A., Dierks, K., et al., Betzel, C., Systematic analysis of protein–detergent complexes applying dynamic light scattering to optimize solutions for crystallization trials. Acta. Crystallogr. F Struct. Biol. Commun 71 (2015), 75–81.
79. Kruse, A.C., Hu, J., et al., Kobilka, B., Structure and dynamics of the M(3) muscarinic acetylcholine receptor. Nature 482 (2012), 552–556.
80. Mazouchi, A., Liu, B., Bahram, A., Gradinaru, C.C., On the performance of bioanalytical fluorescence correlation spectroscopy measurements in a multiparameter photon-counting microscope. Anal. Chim. Acta 688 (2011), 61–69.
81. Bacia, K., Petrášek, Z., Schwille, P., Correcting for Spectral Cross-Talk in Dual-Color Fluorescence Cross-Correlation Spectroscopy. Chemphyschem 13 (2012), 1221–1231.
82. Wohland, T., Rigler, R., Vogel, H., The standard deviation in fluorescence correlation spectroscopy. Biophys. J. 80 (2001), 2987–2999.