Contributions of fluorescence techniques to understanding G protein-coupled receptor dimerisation

Biophysical Reviews

Volumn 4, Issue 4, 2012, Pages 291-298

  Goddard, Alan D ^a   Watts, Anthony ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Dimer; Fluorescence; FRET; G protein coupled receptor; Oligomerisation; Single molecule fluorescence

Indexed keywords

EUKARYOTA;

EID: 84873205676     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-012-0073-z     Document Type: Review

References (57)

1. Albizu L, Balestre MN, Breton C, Pin JP, Manning M, Mouillac B, Barberis C, 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.
2. Albizu L, Cottet M, Kralikova M, Stoev S, Seyer R, Brabet I, Roux T, Bazin H, Bourrier E, Lamarque L, Breton C, Rives ML, Newman A, Javitch J, Trinquet E, Manning M, Pin JP, Mouillac B, Durroux T (2010) Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat Chem Biol 6: 587-594.
3. Ambrosio M, Lohse MJ (2010) Microscopy: GPCR dimers moving closer. Nat Chem Biol 6: 570-571.
4. Angers S, Salahpour A, Joly E, Hilairet S, Chelsky D, Dennis M, Bouvier M (2000) Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc Natl Acad Sci USA 97: 3684-3689.
5. Birdsall NJ (2010) Class A GPCR heterodimers: evidence from binding studies. Trends Pharmacol Sci 31: 499-508.
6. Biteen J (2011) Moving toward the future of single-molecule-based super-resolution imaging. Biopolymers 95: 287-289.
7. Boyer SB, Slesinger PA (2010) Probing novel GPCR interactions using a combination of FRET and TIRF. Commun Integr Biol 3: 343-346.
8. Boyer SB, Clancy SM, Terunuma M, Revilla-Sanchez R, Thomas SM, Moss SJ, Slesinger PA (2009) Direct interaction of GABAB receptors with M2 muscarinic receptors enhances muscarinic signaling. J Neurosci 29: 15796-15809.
9. Ciruela F, Vallano A, Arnau JM, Sanchez S, Borroto-Escuela DO, Agnati LF, Fuxe K, Fernandez-Duenas V (2010a) G protein-coupled receptor oligomerization for what? J Recept Signal Transduct Res 30: 322-330.
10. Ciruela F, Vilardaga JP, Fernandez-Duenas V (2010b) Lighting up multiprotein complexes: lessons from GPCR oligomerization. Trends Biotechnol 28: 407-415.
11. Dinger MC, Bader JE, Kobor AD, Kretzschmar AK, Beck-Sickinger AG (2003) Homodimerization of neuropeptide y receptors investigated by fluorescence resonance energy transfer in living cells. J Biol Chem 278: 10562-10571.
12. Dorsch S, Klotz KN, Engelhardt S, Lohse MJ, Bunemann M (2009) Analysis of receptor oligomerization by FRAP microscopy. Nat Methods 6: 225-230.
13. Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K, Polyakova S, Belov VN, Hein B, von Middendorff C, Schonle A, Hell SW (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457: 1159-1162.
14. Franco R, Casado V, Cortes A, Ferrada C, Mallol J, Woods A, Lluis C, Canela EI, Ferre S (2007) Basic concepts in G-protein-coupled receptor homo- and heterodimerization. ScientificWorldJournal 7: 48-57.
15. Fung JJ, Deupi X, Pardo L, Yao XJ, Velez-Ruiz GA, Devree BT, Sunahara RK, Kobilka BK (2009) Ligand-regulated oligomerization of beta(2)-adrenoceptors in a model lipid bilayer. EMBO J 28: 3315-3328.
16. Fuxe K, Marcellino D, Borroto-Escuela DO, Frankowska M, Ferraro L, Guidolin D, Ciruela F, Agnati LF (2010) The changing world of G protein-coupled receptors: from monomers to dimers and receptor mosaics with allosteric receptor-receptor interactions. J Recept Signal Transduct Res 30: 272-283.
17. Golebiewska U, Johnston JM, Devi L, Filizola M, Scarlata S (2011) Differential response to morphine of the oligomeric state of mu-opioid in the presence of delta-opioid receptors. Biochemistry 50: 2829-2837.
18. Gurevich VV, Gurevich EV (2008) How and why do GPCRs dimerize? Trends Pharmacol Sci 29: 234-240.
19. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP, Chien EY, Velasquez J, Kuhn P, Stevens RC (2008) A specific cholesterol binding site is established by the 2. 8 A structure of the human beta2-adrenergic receptor. Structure 16: 897-905.
20. Harding PJ, Attrill H, Boehringer J, Ross S, Wadhams GH, Smith E, Armitage JP, Watts A (2009) Constitutive dimerization of the G-protein coupled receptor, neurotensin receptor 1, reconstituted into phospholipid bilayers. Biophys J 96: 964-973.
21. Harikumar KG, Miller LJ (2008) Monitoring the state of cholecystokinin receptor oligomerization after ligand binding using decay of time-resolved fluorescence anisotropy. Ann N Y Acad Sci 1144: 21-27.
22. Hern JA, Baig AH, Mashanov GI, Birdsall B, Corrie JE, Lazareno S, Molloy JE, Birdsall NJ (2010) Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc Natl Acad Sci USA 107: 2693-2698.
23. Herrick-Davis K, Grinde E, Weaver BA (2007) Serotonin 5-HT(2C) receptor homodimerization is not regulated by agonist or inverse agonist treatment. Eur J Pharmacol 568: 45-53.
24. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY, Lane JR, Ijzerman AP, Stevens RC (2008) The 2. 6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322: 1211-1217.
25. Jacoby E, Bouhelal R, Gerspacher M, Seuwen K (2006) The 7 TM G-protein-coupled receptor target family. ChemMedChem 1: 761-782.
26. James JR, Oliveira MI, Carmo AM, Iaboni A, Davis SJ (2006) A rigorous experimental framework for detecting protein oligomerization using bioluminescence resonance energy transfer. Nat Methods 3: 1001-1006.
27. Kasai RS, Suzuki KG, Prossnitz ER, Koyama-Honda I, Nakada C, Fujiwara TK, Kusumi A (2011) Full characterization of GPCR monomer-dimer dynamic equilibrium by single molecule imaging. J Cell Biol 192: 463-480.
28. Kuder K, Kiec-Kononowicz K (2008) Fluorescent GPCR ligands as new tools in pharmacology. Curr Med Chem 15: 2132-2143.
29. Latif R, Graves P, Davies TF (2002) Ligand-dependent inhibition of oligomerization at the human thyrotropin receptor. J Biol Chem 277: 45059-45067.
30. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, Leslie AG, Tate CG (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474: 521-525.
31. Leitz AJ, Bayburt TH, Barnakov AN, Springer BA, Sligar SG (2006) Functional reconstitution of Beta2-adrenergic receptors utilizing self-assembling nanodisc technology. Biotechniques 40: 601-602, 604, 606, passim.
32. Lukasiewicz S, Blasiak E, Faron-Gorecka A, Polit A, Tworzydlo M, Gorecki A, Wasylewski Z, Dziedzicka-Wasylewska M (2007) Fluorescence studies of homooligomerization of adenosine A2A and serotonin 5-HT1A receptors reveal the specificity of receptor interactions in the plasma membrane. Pharmacol Rep 59: 379-392.
33. Luttrell LM (2008) Reviews in molecular biology and biotechnology: transmembrane signaling by G protein-coupled receptors. Mol Biotechnol 39: 239-264.
34. Mattheyses AL, Simon SM, Rappoport JZ (2010) Imaging with total internal reflection fluorescence microscopy for the cell biologist. J Cell Sci 123: 3621-3628.
35. Maurel D, Kniazeff J, Mathis G, Trinquet E, Pin JP, Ansanay H (2004) Cell surface detection of membrane protein interaction with homogeneous time-resolved fluorescence resonance energy transfer technology. Anal Biochem 329: 253-262.
36. Maurel D, Comps-Agrar L, Brock C, Rives ML, Bourrier E, Ayoub MA, Bazin H, Tinel N, Durroux T, Prezeau L, Trinquet E, Pin JP (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat Methods 5: 561-567.
37. May LT, Bridge LJ, Stoddart LA, Briddon SJ, Hill SJ (2011) Allosteric interactions across native adenosine-A3 receptor homodimers: quantification using single-cell ligand-binding kinetics. FASEB J 25: 3465-3476.
38. McVey M, Ramsay D, Kellett E, Rees S, Wilson S, Pope AJ, Milligan G (2001) Monitoring receptor oligomerization using time-resolved fluorescence resonance energy transfer and bioluminescence resonance energy transfer. The human delta-opioid receptor displays constitutive oligomerization at the cell surface, which is not regulated by receptor occupancy. J Biol Chem 276: 14092-14099.
39. Milligan G, Ramsay D, Pascal G, Carrillo JJ (2003) GPCR dimerisation. Life Sci 74: 181-188.
40. Oldham WM, Hamm HE (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol 9: 60-71.
41. Overton MC, Blumer KJ (2000) G-protein-coupled receptors function as oligomers in vivo. Curr Biol 10: 341-344.
42. Paila YD, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2011) Oligomerization of the serotonin(1A) receptor in live cells: a time-resolved fluorescence anisotropy approach. J Phys Chem B 115: 11439-11447.
43. Palczewski K (2010) Oligomeric forms of G protein-coupled receptors (GPCRs). Trends Biochem Sci 35: 595-600.
44. Piehler J (2011) GPCRs: caught in a spectroscopic trap. Nat Chem Biol 7: 578-579.
45. Pioszak AA, Harikumar KG, Parker NR, Miller LJ, Xu HE (2010) Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation. J Biol Chem 285: 12435-12444.
46. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VR, Sanishvili R, Fischetti RF, Schertler GF, Weis WI, Kobilka BK (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450: 383-387.
47. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, Devree BT, Rosenbaum DM, Thian FS, Kobilka TS, Schnapp A, Konetzki I, Sunahara RK, Gellman SH, Pautsch A, Steyaert J, Weis WI, Kobilka BK (2011a) Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 469: 175-180.
48. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011b) Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477: 549-555.
49. Rosenbaum DM, Zhang C, Lyons JA, Holl R, Aragao D, Arlow DH, Rasmussen SG, Choi HJ, Devree BT, Sunahara RK, Chae PS, Gellman SH, Dror RO, Shaw DE, Weis WI, Caffrey M, Gmeiner P, Kobilka BK (2011) Structure and function of an irreversible agonist-beta(2) adrenoceptor complex. Nature 469: 236-240.
50. Stryer L (1978) Fluorescence energy transfer as a spectroscopic ruler. Annu Rev Biochem 47: 819-846.
51. Stryer L, Haugland RP (1967) Energy transfer: a spectroscopic ruler. Proc Natl Acad Sci USA 58: 719-726.
52. Urizar E, Yano H, Kolster R, Gales C, Lambert N, Javitch JA (2011) CODA-RET reveals functional selectivity as a result of GPCR heteromerization. Nat Chem Biol 7: 624-630.
53. Warne T, Moukhametzianov R, Baker JG, Nehme R, Edwards PC, Leslie AG, Schertler GF, Tate CG (2011) The structural basis for agonist and partial agonist action on a beta(1)-adrenergic receptor. Nature 469: 241-244.
54. Whorton MR, Bokoch MP, Rasmussen SG, Huang B, Zare RN, Kobilka B, Sunahara RK (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc Natl Acad Sci USA 104: 7682-7687.
55. Wurch T, Matsumoto A, Pauwels PJ (2001) Agonist-independent and -dependent oligomerization of dopamine D(2) receptors by fusion to fluorescent proteins. FEBS Lett 507: 109-113.
56. Xu F, Wu H, Katritch V, Han GW, Jacobson KA, Gao ZG, Cherezov V, Stevens RC (2011) Structure of an agonist-bound human A2A adenosine receptor. Science 332: 322-327.
57. Yanagawa M, Yamashita T, Shichida Y (2011) Comparative fluorescence resonance energy transfer analysis of metabotropic glutamate receptors: implications about the dimeric arrangement and rearrangement upon ligand bindings. J Biol Chem 286: 22971-22981.