Methods to monitor the quaternary structure of G protein-coupled receptors

FEBS Journal

Volumn 272, Issue 12, 2005, Pages 2914-2925

  Milligan, Graeme ^a,c   Bouvier, Michel ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Dimerization; Functional reconstitution; G protein coupled receptor; Immunoprecipitation; Resonance energy transfer

Indexed keywords

G PROTEIN COUPLED RECEPTOR;

BIOLUMINESCENCE; COIMMUNOPRECIPITATION; DIMERIZATION; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATION; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; SHORT SURVEY;

ANIMALS; BIOCHEMISTRY; DIMERIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; IMMUNOPRECIPITATION; LIGANDS; LUMINESCENT MEASUREMENTS; MOLECULAR BIOLOGY; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, G-PROTEIN-COUPLED;

EID: 21344433619     PISSN: 1742464X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04731.x     Document Type: Short Survey

References (67)

1. Salahpour A, Angers S & Bouvier M (2000) Functional significance of oligomerization of G-protein-coupled receptors. Trends Endocrinol Metab 11, 163-168.
2. Woolf PJ & Linderman JJ (2003) Self organization of membrane proteins via dimerization. Biophys Chem 104, 217-227.
3. Jones KA, Borowsky B, Tamm JA, Craig DA, Durkin MM, Dai M, Yao WJ, Johnson M, Gunwaldsen C, Huang LY, et al. (1998) GABA (B) receptors function as a heteromeric assembly of the subunits GABA (B) R1 and GABA (B) R2. Nature 396, 674-679.
4. White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, Barnes AA, Emson P, Foord SM & Marshall FH (1998) Heterodimerization is required for the formation of a functional GABA (B) receptor. Nature 396, 679-682.
5. Kaupmann K, Huggel K, Heid J, Flor PJ, Bischoff S, Mickel SJ, McMaster G, Angst C, Bittiger H, Froestl W & Bettler B (1997) Expression cloning of GABA (B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 386, 239-246.
6. Li X, Staszewski L, Xu H, Durick K, Zoller M & Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99, 4692-4696.
7. Pin J-P, Kniazeff J, Liu J, Binet V, Goudet C, Rondard P & Prézeau L (2005) Allosteric functioning of dimeric Class C G-protein coupled receptors. FEBS J 272, 2947-2955.
8. Hague C, Uberti MA, Chen Z, Hall RA & Minneman KP (2004a) Cell surface expression of alpha1D-adrenergic receptors is controlled by heterodimerization with alpha1B-adrenergic receptors. J Biol Chem 279, 15541-15549.
9. Hague C, Uberti MA, Chen Z, Bush CF, Jones SV, Ressler KJ, Hall RA & Minneman KP (2004b) Olfactory receptor surface expression is driven by association with the beta2-adrenergic receptor. Proc Natl Acad Sci USA 101, 13672-13676.
10. Bouvier M (2001) Oligomerization of G-protein-coupled transmitter receptors. Nat Rev Neurosci 2, 274-286.
11. George SR, O'Dowd BF & Lee SP (2002) G-protein-coupled receptor oligomerization and its potential for drug discovery. Nature Rev Drug Discovery 1, 808-820.
12. Milligan G (2004) G protein-coupled receptor dimerization: function and ligand pharmacology. Mol Pharmacol 66, 1-7.
13. Issafras H, Angers S, Bulenger S, Blanpain C, Parmentier M et al. (2002) Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J Biol Chem 277, 34666-34673.
14. Terrillon S, Durroux T, Mouillac B, Breit A, Ayoub MA, Taulan M, Jockers R, Barberis C & Bouvier M (2003) Oxytocin and vasopressin V1a and V2 receptors form constitutive homo- and heterodimers during biosynthesis. Mol Endocrinol 17, 677-691.
15. Salahpour A, Angers S, Mercier JF, Lagace M, Marullo S & Bouvier M (2004) Homodimerization of the beta 2-adrenergic receptor as a pre-requisite for cell surface targeting. J Biol Chem 279, 33390-33397.
16. Baneres JL & Parello J (2003) Structure-based analysis of GPCR function: evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G-protein. J Mol Biol 329, 815-829.
17. Angers S, Salahpour A & Bouvier M (2002) Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu Rev Pharmacol Toxicol 42, 409-435.
18. 2-adrenergic receptor transmembrane domain inhibits both receptor dimerization and activation. J Biol Chem 271, 16384-16392.
19. Nimchinsky EA, Hof PR, Janssen WG, Morrison JH & Schmauss C (1997) Expression of dopamine D3 receptor dimers and tetramers in brain and in transfected cells. J Biol Chem 212, 29229-29237.
20. Jordan BA & Devi LA (1999) G-protein-coupled receptor heterodimerization modulates receptor function. Nature 399, 697-700.
21. Salim K, Fenton T, Bacha J, Urien-Rodriguez H, Bonnert T, Skynner HA, Watts E, Kerby J, Heald A, Beer M, et al. (2002) Oligomerization of G-protein-coupled receptors shown by selective co-immunoprecipitation. J Biol Chem 277, 15482-15485.
22. Guo W, Shi L & Javitch JA (2003) The fourth transmembrane segment forms the interface of the dopamine d2 receptor homodimer. J Biol Chem 278, 4385-4388.
23. Klco JM, Lassere TB & Baranski TJ (2003) C5a receptor Oligomerization. I. Disulfide trapping reveals oligomers and potential contact surfaces in a G protein-coupled receptor. J Biol Chem 278, 35345-35353.
24. Park PS & Wells JW (2004) Oligomeric potential of the M2 muscarinic cholinergic receptor. J Neurochem 90, 537-548.
25. Rocheville M, Lange DC, Kumar U, Patel SC, Patel RC & Patel YC (2000) Receptors for dopamine and somatostatin: formation of hetero-oligomers with enhanced functional activity. Science 288, 154-157.
26. Rocheville M, Lange DC, Kumar U, Sasi R, Patel RC & Patel YC (2000) Subtypes of the somatostatin receptor assemble as functional homo- and heterodimers. J Biol Chem 275, 7862-7869.
27. Herrick-Davis K, Grinde E & Mazurkiewicz JE (2004) Biochemical and biophysical characterization of serotonin 5-HT (2C) receptor homodimers on the plasma membrane of living cells. Biochemistry 43, 13963-13971.
28. Milligan G (2004) Applications of bioluminescence- and fluorescence resonance energy transfer to drug discovery at G protein-coupled receptors. Eur J Pharm Sci 21, 397-405.
29. Kobilka BK & Gether U (2002) Use of fluorescence spectroscopy to study conformational changes in the beta 2-adrenoceptor. Methods Enzymol 343, 170-182.
30. Vilardaga JP, Bunemann M, Krasel C, Castro M & Lohse MJ (2003) Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat Biotechnol 21, 807-812.
31. Mesnier D & Baneres JL (2004) Cooperative conformational changes in a GPCR dimer, the leukotriene B4 receptor BLT1. J Biol Chem 279, 49664-49670.
32. Ayoub MA, Couturier C, Lucas-Meunier E, Angers S, Fossier P, Bouvier M & Jockers R (2002) Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J Biol Chem 277, 21522-21528.
33. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A & Palczewski K (2004) The G protein-coupled receptor rhodopsin in the native membrane. FEBS Lett 564, 281-288.
34. Liang Y, Fotiadis D, Maeda T, Maeda A, Modzelewska A, Filipek S, Saperstein DA, Engel A & Palczewski K (2004) Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J Biol Chem 279, 48189-48196.
35. 1b-adrenoceptor. Mol Pharmacol 66, 1123-1137.
36. He L, Grammer AC, Wu X & Lipsky PE (2004) TRAF3 forms heterotrimers with TRAF2 and modulates its ability to mediate NF-kB activation. J Biol Chem 279, 55855-55865.
37. 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.
38. Mercier JF, Salahpour A, Angers S, Breit A & Bouvier M (2002) Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J Biol Chem 277, 44925-44931.
39. Ramsay D & Milligan G (2005) Analysis of receptor-receptor interactions by using time-resolved fluorescence resonance energy transfer. In G Protein Coupled Receptor-Protein Interactions (George, SR & O'Dowd, BF, eds). pp. 37-52. John Wiley and Sons, Hoboken, N.J.
40. 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 δ opioid receptor displays constitutive oligomerization at the cell surface which is not regulated by receptor occupancy. J Biol Chem 276, 14092-14099.
41. Bakker RA, Dees G, Carrillo JJ, Booth RG, Lopez-Gimenez JF, Milligan G, Strange PG & Leurs R (2004) Domain swapping in the human histamine H 1 receptor. J Pharmacol Exp Ther 311, 131-138.
42. Canals M, Burgueno J, Marcellino D, Cabello N, Canela EI, Mallol J, Agnati L, Ferre S, Bouvier M, Fuxe K, et al. (2004) Homodimerization of adenosine A2A receptors: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J Neurochem 88, 726-734.
43. 1L-adrenoceptor. Mol Pharmacol 66, 228-239.
44. Morris DP, Price RR, Smith MP, Lei B & Schwinn DA (2004) Cellular trafficking of human alpha1a-adrenergic receptors is continuous and primarily agonist-independent. Mol Pharmacol 66, 843-854.
45. 1a-adrenoceptor endocytosis causes intracellular transportation of -blockers via recycling compartments. Mol Pharmacol 67, 992-1004.
46. Ramsay D, Kellett E, McVey M, Rees S & Milligan G (2002) Homo -and hetero-oligomeric interactions between G protein-coupled receptors in living cells monitored by two variants of bioluminesence resonance energy transfer. Hetero-oligomers between receptor subtypes form more efficiency than between less closely related sequences. Biochem J 365, 429-440.
47. Perroy J, Pontier S, Charest PG, Aubry M & Bouvier M (2004) Real-time monitoring of ubiquitination in living cells by BRET. Nature Meth 1, 203-208.
48. 2-adrenergic receptor dimerization in living cells using bioluminescene resonance energy transfer (BRET). Proc Natl Acad Sci USA 97, 3684-3689.
49. Ayoub MA, Levoye A, Delagrange P & Jockers R (2004) Preferential formation of MT1/MT2 melatonin receptor heterodimers with distinct ligand interaction properties compared with MT2 homodimers. Mol Pharmacol 66, 312-321.
50. Armstrong D & Strange PG (2001) Dopamine D2 receptor dimer formation: evidence from ligand binding. J Biol Chem 276, 22621-22629.
51. Monnot C, Bihoreau C, Conchon S, Curnow KM, Corvol P & Clauser E (1996) Polar residues in the transmembrane domains of the type 1 angiotensin II receptor are required for binding and coupling. Reconstitution of the binding site by co-expression of two deficient mutants. J Biol Chem 271, 1507-1513.
52. Dean MK, Higgs C, Smith RE, Bywater RP, Snell CR, Scott PD, Upton GJ, Howe TJ & Reynolds CA (2001) Dimerization of G-protein-coupled receptors. J Med Chem 44, 4595-4614.
53. Maggio R, Novi F & Scarselli M (2005) The impact of GPCR heterodimerization on function and pharmacology. FEBS J 272, 2939-2946.
54. Maggio R, Vogel Z & Wess J (1993) Coexpression studies with mutant muscarinic/adrenergic receptors provide evidence for intermolecular 'cross-talk' between G-protein-linked receptors. Proc Natl Acad Sci USA 90, 3103-3107.
55. Yang S, Cho SS, Levy Y, Cheung MS, Levine H, Wolynes PG & Onuchic JN (2004) Domain swapping is a consequence of minimal frustration. Proc Natl Acad Sci USA 101, 13786-13791.
56. George SR, Fan T, Xie Z, Tse R, Tam V, Varghese G & O'Dowd BF (2000) Oligomerization of μ- and δ-opioid receptors. J Biol Chem 275, 26128-26135.
57. Devi LA (2001) Heterodimerization of G-protein-coupled receptors: pharmacology, signaling and trafficking. Trends Pharmacol Sci 22, 532-537.
58. 3-adrenergic receptors generates a β-Adrenergic signaling unit with distinct functional properties. J Biol Chem 279, 28756-28765.
59. Lee C, Ji I, Ryu K, Song Y, Conn PM & Ji TH (2002) Two defective heterozygous luteinizing hormone receptors can rescue hormone action. J Biol Chem 277, 15795-15800.
60. Ji I, Lee C, Song Y, Conn PM & Ji TH (2002) Cis- and trans-activation of hormone receptors: the LH receptor. Mol Endocrinol 16, 1299-1308.
61. Carrillo JJ, Pediani J & Milligan G (2003) Dimers of class A G protein-coupled receptors function via agonist-mediated trans-activation of associated G proteins. J Biol Chem 278, 42578-42587.
62. Milligan G (2002) The use of receptor-G protein fusion proteins for the study of ligand activity. Receptors Channels 8, 309-317.
63. Molinari P, Ambrosio C, Riitano D, Sbraccia M, Gro MC & Costa T (2003) Promiscuous coupling at receptor-Galpha fusion proteins. The receptor of one covalent complex interacts with the alpha-subunit of another. J Biol Chem 278, 15778-15788.
64. Park PS, Sum CS, Pawagi AB & Wells JW (2002) Cooperativity and oligomeric status of cardiac muscarinic cholinergic receptors. Biochemistry 41, 5588-5604.
65. Costa T & Herz A (1989) Antagonists with negative intrinsic activity at δ opiod receptors coupled to GTP-binding proteins. Proc Natl Acad Sci USA 86, 7321-7325.
66. Azzi M, Pineyro G, Pontier S, Parent S, Ansanay H & Bouvier M (2001) Allosteric effects of G protein overexpression on the binding of {beta}-adrenergic ligands with distinct inverse efficacies. Mol Pharmacol 60, 999-1007.
67. Law PY, Erickson-Herbrandson LJ, Zha QQ, Solberg J, Chu J, Sarre A & Loh HH (2005) Heterodimerization of μ and δ-opioid receptors occurs at the cell surface only and requires receptor-G protein interactions. J Biol Chem 280, 11152-11164.