The functional size of GPCRs – Monomers, dimers or tetramers?

Subcellular Biochemistry

Volumn 63, Issue , 2012, Pages 67-81

  Pétrin, Darlaine ^a   Hébert, Terence E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Adrenergic receptors; GPCRs; Oligomerization; Signalling complexes

Indexed keywords

G PROTEIN COUPLED RECEPTOR;

ANIMAL; ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; ENDOPLASMIC RETICULUM; HUMANS; PROTEIN INTERACTION MAPS; PROTEIN MULTIMERIZATION; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84879079845     PISSN: 03060225     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4765-4_4     Document Type: Article

References (74)

1. Agnati LF, Guidolin D, Albertin G, Trivello E, Ciruela F, Genedani S, Tarakanov A, Fuxe K (2010) An integrated view on the role of receptor mosaics at perisynaptic level: focus on adenosine A(2A), dopamine D(2), cannabinoid CB(1), and metabotropic glutamate mGlu(5) receptors. J Recept Signal Transduct Res 30(5): 355-369. doi: 10. 3109/10799893. 2010. 487492.
2. 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 U S A 97(7): 3684-3689.
3. Baragli A, Grieco ML, Trieu P, Villeneuve LR, Hébert TE (2008) Heterodimers of adenylyl cyclases 2 and 5 show enhanced functional responses in the presence of Gα s. Cell Signal 20(3): 480-492. doi: 10. 1016/j. cellsig. 2007. 10. 033, pii: S0898-6568(07)00329-4.
4. Barki-Harrington L, Luttrell LM, Rockman HA (2003) Dual inhibition of beta-adrenergic and angiotensin II receptors by a single antagonist: a functional role for receptor-receptor interaction in vivo. Circulation 108(13): 1611-1618. doi: 10. 1161/01. CIR. 0000092166. 30360. 78, pii: 01. CIR. 0000092166. 30360. 78.
5. Berthouze M, Ayoub M, Russo O, Rivail L, Sicsic S, Fischmeister R, Berque-Bestel I, Jockers R, Lezoualc'h F (2005) Constitutive dimerization of human serotonin 5-HT4 receptors in living cells. FEBS Lett 579(14): 2973-2980. doi: 10. 1016/j. febslet. 2005. 04. 040, pii: S0014-5793(05)00515-6.
6. Breit A, Lagacé M, Bouvier M (2004) Hetero-oligomerization between beta2-and beta3-adrenergic receptors generates a beta-adrenergic signaling unit with distinct functional properties. J Biol Chem 279(27): 28756-28765.
7. Bulenger S, Marullo S, Bouvier M (2005) Emerging role of homo-and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol Sci 26(3): 131-137. doi: 10. 1016/j. tips. 2005. 01. 004, pii: S0165-6147(05)00020-9.
8. Carriba P, Navarro G, Ciruela F, Ferre S, Casado V, Agnati L, Cortes A, Mallol J, Fuxe K, Canela EI, Lluis C, Franco R (2008) Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat Methods 5(8): 727-733. doi: 10. 1038/nmeth. 1229, pii: nmeth. 1229.
9. Dai S, Hall DD, Hell JW (2009) Supramolecular assemblies and localized regulation of voltagegated ion channels. Physiol Rev 89(2): 411-452. doi: 10. 1152/physrev. 00029. 2007, pii: 89/2/411.
10. Daub H, Wallasch C, Lankenau A, Herrlich A, Ullrich A (1997) Signal characteristics of G proteintransactivated EGF receptor. EMBO J 16(23): 7032-7044. doi: 10. 1093/emboj/16. 23. 7032.
11. David M, Richer M, Mamarbachi AM, Villeneuve LR, Dupré DJ, Hébert TE (2006) Interactions between GABA-B(1) receptors and Kir 3 inwardly rectifying potassium channels. Cell Signal 18(12): 2172-2181.
12. Dong C, Filipeanu CM, Duvernay MT, Wu G (2007) Regulation of G protein-coupled receptor export trafficking. Biochim Biophys Acta 1768: 853-870.
13. Dupré DJ, Hébert TE (2006) Biosynthesis and trafficking of seven transmembrane receptor signalling complexes. Cell Signal 18(10): 1549-1559.
14. Dupré DJ, Robitaille M, Ethier N, Villeneuve LR, Mamarbachi AM, Hébert TE (2006) Seven transmembrane receptor core signalling complexes are assembled prior to plasma membrane trafficking. J Biol Chem 281(45): 34561-34573.
15. Dupré DJ, Baragli A, Rebois RV, Ethier N, Hébert TE (2007) Signalling complexes associated with adenylyl cyclase II are assembled during their biosynthesis. Cell Signal 19: 481-489.
16. Fonseca JM, Lambert NA (2009) Instability of a class a G protein-coupled receptor oligomer interface. Mol Pharmacol 75(6): 1296-1299. doi: 10. 1124/mol. 108. 053876, pii: mol. 108. 053876.
17. 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(21): 3315-3328. doi: 10. 1038/emboj. 2009. 267, pii: emboj2009267.
18. Gandia J, Galino J, Amaral OB, Soriano A, Lluis C, Franco R, Ciruela F (2008) Detection of higherorder G protein-coupled receptor oligomers by a combined BRET-BiFC technique. FEBS Lett 582(20): 2979-2984. doi: 10. 1016/j. febslet. 2008. 07. 045, pii: S0014-5793(08)00646-7.
19. Guo W, Urizar E, Kralikova M, Mobarec JC, Shi L, Filizola M, Javitch JA (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J 27(17): 2293-2304. doi: 10. 1038/emboj. 2008. 153, pii: emboj2008153.
20. Haack KK, Tougas MR, Jones KT, El-Dahr SS, Radhakrishna H, McCarty NA (2010) A novel bioassay for detecting GPCR heterodimerization: transactivation of beta 2 adrenergic receptor by bradykinin receptor. J Biomol Screen 15(3): 251-260. doi: 10. 1177/1087057109360254, pii: 1087057109360254.
21. Hague C, Uberti MA, Chen Z, Bush CF, Jones SV, Ressler KJ, Hall RA, Minneman KP (2004) Olfactory receptor surface expression is driven by association with the beta2-adrenergic receptor. Proc Natl Acad Sci U S A 101(37): 13672-13676. doi: 10. 1073/pnas. 0403854101, pii: 0403854101.
22. Hamatake M, Aoki T, Futahashi Y, Urano E, Yamamoto N, Komano J (2009) Ligand-independent higher-order multimerization of CXCR4, a G-protein-coupled chemokine receptor involved in targeted metastasis. Cancer Sci 100(1): 95-102. doi: 10. 1111/j. 1349-7006. 2008. 00997. x, pii: CAS997.
23. Han Y, Moreira IS, Urizar E, Weinstein H, Javitch JA (2009) Allosteric communication between protomers of dopamine class a GPCR dimers modulates activation. Nat Chem Biol 5(9): 688-695. doi: 10. 1038/nchembio. 199, pii: nchembio. 199.
24. Hébert TE, Bouvier M (1998) Structural and functional aspects of G protein-coupled receptor oligomerization. Biochem Cell Biol 76(1): 1-11.
25. Hébert TE, Moffett S, Morello JP, Loisel TP, Bichet DG, Barret C, Bouvier M (1996) A peptide derived from a beta2-adrenergic receptor transmembrane domain inhibits both receptor dimerization and activation. J Biol Chem 271(27): 16384-16392.
26. 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 reflectionfluorescence imaging of single molecules. Proc Natl Acad Sci U S A 107(6): 2693-2698. doi: 10. 1073/pnas. 0907915107, pii: 0907915107.
27. Hudson BD, Hébert TE, Kelly ME (2010) Physical and functional interaction between CB1 cannabinoid receptors and beta2-adrenoceptors. Br J Pharmacol 160(3): 627-642. doi: 10. 1111/j. 1476-5381. 2010. 00681. x, pii: BPH681.
28. Joiner ML, Lise MF, Yuen EY, Kam AY, Zhang M, Hall DD, Malik ZA, Qian H, Chen Y, Ulrich JD, Burette AC, Weinberg RJ, Law PY, El-Husseini A, Yan Z, Hell JW (2010) Assembly of a beta2-adrenergic receptor-GluR1 signalling complex for localized cAMP signalling. EMBO J 29(2): 482-495. doi: 10. 1038/emboj. 2009. 344, pii: emboj2009344.
29. Jordan BA, Trapaidze N, Gomes I, Nivarthi R, Devi LA (2001) Oligomerization of opioid receptors with beta 2-adrenergic receptors: a role in trafficking and mitogen-activated protein kinase activation. Proc Natl Acad Sci U S A 98(1): 343-348.
30. 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(3): 463-480. doi: 10. 1083/jcb. 201009128, pii: jcb. 201009128.
31. Katritch V, Cherezov V, Stevens RC (2012) Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol Sci 33(1): 17-27. doi: 10. 1016/j. tips. 2011. 09. 003, pii: S0165-6147(11)00172-6.
32. Kern A, Albarran-Zeckler R, Walsh HE, Smith RG (2012) Apo-ghrelin receptor forms heteromers with DRD2 in hypothalamic neurons and is essential for anorexigenic effects of DRD2 agonism. Neuron 73(2): 317-332. doi: 10. 1016/j. neuron. 2011. 10. 038, pii: S0896-6273(11)01087-7.
33. Kuravi S, Lan TH, Barik A, Lambert NA (2010) Third-party bioluminescence resonance energy transfer indicates constitutive association of membrane proteins: application to class a g-proteincoupled receptors and g-proteins. Biophys J 98(10): 2391-2399. doi: 10. 1016/j. bpj. 2010. 02. 004, pii: S0006-3495(10)00232-8.
34. Lan TH, Kuravi S, Lambert NA (2011) Internalization dissociates beta2-adrenergic receptors. PLoS One 6(2): e17361. doi: 10. 1371/journal. pone. 0017361.
35. Larocca TJ, Schwarzkopf M, Altman P, Zhang S, Gupta A, Gomes I, Alvin Z, Champion HC, Haddad G, Hajjar RJ, Devi LA, Schecter AD, Tarzami ST (2010) beta2-Adrenergic receptor signaling in the cardiac myocyte is modulated by interactions with CXCR4. J Cardiovasc Pharmacol 56(5): 548-559. doi: 10. 1097/FJC. 0b013e3181f713fe.
36. Lavine N, Ethier N, Oak JN, Pei L, Liu F, Trieu P, Rebois RV, Bouvier M, Hébert TE, Van Tol HH (2002) G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J Biol Chem 277(48): 46010-46019.
37. Lavoie C, Hébert TE (2003) Pharmacological characterization of putative beta1-beta2-adrenergic receptor heterodimers. Can J Physiol Pharmacol 81(2): 186-195.
38. Lavoie C, Mercier JF, Salahpour A, Umapathy D, Breit A, Villeneuve LR, Zhu WZ, Xiao RP, Lakatta EG, Bouvier M, Hébert TE (2002) Beta 1/beta 2-adrenergic receptor heterodimerization regulates beta 2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem 277(38): 35402-35410.
39. Lopez-Gimenez JF, Canals M, Pediani JD, Milligan G (2007) The alpha1b-adrenoceptor exists as a higher-order oligomer: effective oligomerization is required for receptor maturation, surface delivery, and function. Mol Pharmacol 71(4): 1015-1029. doi: 10. 1124/mol. 106. 033035, pii: mol. 106. 033035.
40. Luttrell DK, Luttrell LM (2003) Signaling in time and space: G protein-coupled receptors and mitogen-activated protein kinases. Assay Drug Dev Technol 1(2): 327-338. doi: 10. 1089/15406580360545143.
41. Luttrell LM, van Biesen T, Hawes BE, Koch WJ, Krueger KM, Touhara K, Lefkowitz RJ (1997) G-protein-coupled receptors and their regulation: activation of the MAP kinase signaling pathway by G-protein-coupled receptors. Adv Second Messenger Phosphoprotein Res 31: 263-277.
42. Ma AW, Redka DS, Pisterzi LF, Angers S, Wells JW (2007) Recovery of oligomers and cooperativity when monomers of the M2 muscarinic cholinergic receptor are reconstituted into phospholipid vesicles. Biochemistry 46(26): 7907-7927. doi: 10. 1021/bi6026105.
43. Ma AW, Pawagi AB, Wells JW (2008) Heterooligomers of the muscarinic receptor and G proteins purified from porcine atria. Biochem Biophys Res Commun 374(1): 128-133. doi: 10. 1016/j. bbrc. 2008. 06. 105, pii: S0006-291X(08)01287-4.
44. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, Sunahara RK, Pardo L, Weis WI, Kobilka BK, Granier S (2012) Crystal structure of the micro-opioid receptor bound to a morphinan antagonist. Nature 485: 321-326. doi: 10. 1038/nature10954, pii: nature10954.
45. Maudsley S, Pierce KL, Zamah AM, Miller WE, Ahn S, Daaka Y, Lefkowitz RJ, Luttrell LM (2000) The beta(2)-adrenergic receptor mediates extracellular signal-regulated kinase activation via assembly of a multi-receptor complex with the epidermal growth factor receptor. J Biol Chem 275(13): 9572-9580.
46. McGraw DW, Mihlbachler KA, Schwarb MR, Rahman FF, Small KM, Almoosa KF, Liggett SB (2006) Airway smooth muscle prostaglandin-EP1 receptors directly modulate beta2-adrenergic receptors within a unique heterodimeric complex. J Clin Invest 116(5): 1400-1409. doi: 10. 1172/JCI25840.
47. McVey M, Ramsay D, Kellett E, Rees S, Wilson S, Pope AJ, Milligan G (2001) Monitoring receptor oligomerization using time-resolvedfluorescence 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(17): 14092-14099.
48. Mercier J-F, 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(47): 44925-44931.
49. Milligan G (2007) G protein-coupled receptor dimerisation: molecular basis and relevance to function. Biochim Biophys Acta 1768(4): 825-835. doi: 10. 1016/j. bbamem. 2006. 09. 021, pii: S0005-2736(06)00380-4.
50. Milligan G (2009) G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br J Pharmacol 158(1): 5-14. doi: 10. 1111/j. 1476-5381. 2009. 00169. x, pii: BPH169.
51. Milligan G (2010) The role of dimerisation in the cellular trafficking of G-protein-coupled receptors. Curr Opin Pharmacol 10(1): 23-29. doi: 10. 1016/j. coph. 2009. 09. 010, pii: S1471-4892(09)00158-1.
52. Pétrin D, Hébert TE (2011) Imaging-based approaches to understanding G protein-coupled receptor signalling complexes. Methods Mol Biol 756: 37-60.
53. Pisterzi LF, Jansma DB, Georgiou J, Woodside MJ, Chou JT, Angers S, Raicu V, Wells JW (2010) Oligomeric size of the m2 muscarinic receptor in live cells as determined by quantitativefluorescence resonance energy transfer. J Biol Chem 285(22): 16723-16738. doi: 10. 1074/jbc. M109. 069443, pii: M109. 069443.
54. Prinster SC, Hague C, Hall RA (2005) Heterodimerization of g protein-coupled receptors: specificity and functional significance. Pharmacol Rev 57(3): 289-298. doi: 10. 1124/pr. 57. 3. 1, pii: 57/3/289.
55. Qin K, Dong C, Wu G, Lambert NA (2011) Inactive-state preassembly of G(q)-coupled receptors and G(q) heterotrimers. Nat Chem Biol 7(10): 740-747. doi: 10. 1038/nchembio. 642, pii: nchembio. 642.
56. Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O'Dowd BF, George SR (2007) D1-D2 Dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 104(2): 654-659. doi: 10. 1073/pnas. 0604049104, pii: 0604049104.
57. Rebois RV, Hébert TE (2003) Protein complexes involved in heptahelical receptor-mediated signal transduction. Receptors Channels 9(3): 169-194.
58. Rebois RV, Robitaille M, Gales C, Dupré DJ, Baragli A, Trieu P, Ethier N, Bouvier M, Hébert TE (2006) Heterotrimeric G proteins form stable complexes with adenylyl cyclase and Kir3. 1 Channels in living cells. J Cell Sci 119(Pt 13): 2807-2818.
59. Rebois RV, Robitaille M, Pétrin D, Zylbergold P, Trieu P, Hébert TE (2008) Combining protein complementation assays with resonance energy transfer to detect multipartner protein complexes in living cells. Methods 45(3): 214-218. doi: 10. 1016/j. ymeth. 2008. 06. 006, pii: S1046-2023(08)00103-5.
60. Robitaille M, Ramakrishnan N, Baragli A, Hébert TE (2009) Intracellular trafficking and assembly of specific Kir3 channel/G protein complexes. Cell Signal 21(4): 488-501. doi: 10. 1016/j. cellsig. 2008. 11. 011, pii: S0898-6568(08)00342-2.
61. Salahpour A, Angers S, Mercier JF, Lagace M, Marullo S, Bouvier M (2004) Homodimerization of the beta2-adrenergic receptor as a prerequisite for cell surface targeting. J Biol Chem 279(32): 33390-33397.
62. Terrillon S, Bouvier M (2004) Roles of G-protein-coupled receptor dimerization. EMBO Rep 5(1): 30-34.
63. Uberti MA, Hague C, Oller H, Minneman KP, Hall RA (2005) Heterodimerization with beta2-adrenergic receptors promotes surface expression and functional activity of alpha1D-adrenergic receptors. J Pharmacol Exp Ther 313(1): 16-23. doi: 10. 1124/jpet. 104. 079541, pii: jpet. 104. 079541.
64. Vidi PA, Chemel BR, Hu CD, Watts VJ (2008a) Ligand-dependent oligomerization of dopamine D(2) and adenosine a(2A) receptors in living neuronal cells. Mol Pharmacol 74(3): 544-551. doi: 10. 1124/mol. 108. 047472, pii: mol. 108. 047472.
65. Vidi PA, Chen J, Irudayaraj JM, Watts VJ (2008b) Adenosine a(2A) receptors assemble into higherorder oligomers at the plasma membrane. FEBS Lett 582(29): 3985-3990. doi: 10. 1016/j. febslet. 2008. 09. 062, pii: S0014-5793(08)00897-1.
66. 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 U S A 104(18): 7682-7687. doi: 10. 1073/pnas. 0611448104, pii: 0611448104.
67. Whorton MR, Jastrzebska B, Park PS, Fotiadis D, Engel A, Palczewski K, Sunahara RK (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283(7): 4387-4394. doi: 10. 1074/jbc. M703346200, pii: M703346200.
68. Wrzal PK, Devost D, Pétrin D, Goupil E, Iorio-Morin C, Laporte SA, Zingg HH, Hébert TE (2012a) Allosteric interactions between the oxytocin receptor and the beta2-adrenergic receptor in the modulation of ERK1/2 activation are mediated by heterodimerization. Cell Signal 24(1): 342-350. doi: 10. 1016/j. cellsig. 2011. 09. 020, pii: S0898-6568(11)00301-9.
69. Wrzal PK, Goupil E, Laporte SA, Hébert TE, Zingg HH (2012b) Functional interactions between the oxytocin receptor and the beta2-adrenergic receptor: implications for ERK1/2 activation in human myometrial cells. Cell Signal 24(1): 333-341. doi: 10. 1016/j. cellsig. 2011. 09. 019, pii: S0898-6568(11)00300-7.
70. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V, Abagyan R, Brooun A, Wells P, Bi FC, Hamel DJ, Kuhn P, Handel TM, Cherezov V, Stevens RC (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330: 1066-1071. doi: 10. 1126/science. 1194396, pii: science. 1194396.
71. Wu H, Wacker D, Mileni M, Katritch V, Han GW, Vardy E, Liu W, Thompson AA, Huang XP, Carroll FI, Mascarella SW, Westkaemper RB, Mosier PD, Roth BL, Cherezov V, Stevens RC (2012) Structure of the human kappa-opioid receptor in complex with JDTic. Nature 485: 327-332. doi: 10. 1038/nature10939, pii: nature10939.
72. Xu J, He J, Castleberry AM, Balasubramanian S, Lau AG, Hall RA (2003) Heterodimerization of alpha 2A-and beta 1-adrenergic receptors. J Biol Chem 278(12): 10770-10777. doi: 10. 1074/jbc. M207968200, pii: M207968200.
73. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2(2): 107-117.
74. Zhu WZ, Chakir K, Zhang S, Yang D, Lavoie C, Bouvier M, Hébert TE, Lakatta EG, Cheng H, Xiao RP (2005) Heterodimerization of beta1-and beta2-adrenergic receptor subtypes optimizes beta-adrenergic modulation of cardiac contractility. Circ Res 97(3): 244-251. doi: 10. 1161/01. RES. 0000176764. 38934. 86, pii: 01. RES. 0000176764. 38934. 86.