235
Views
20
CrossRef citations to date
0
Altmetric
Research Articles

G protein-coupled receptor oligomerization for what?

, , , , , , & show all
Pages 322-330 | Received 06 Jul 2010, Accepted 10 Jul 2010, Published online: 18 Aug 2010

References

  • Agnati LF, Fuxe K, Zini I, Lenzi P, Hokfelt T. Aspects on receptor regulation and isoreceptor identification. Med Biol 1980, 58, 182–187.
  • Maggi A, U’Prichard DC, Enna SJ. beta-Adrenergic regulation of alpha 2-adrenergic receptors in the central nervous system. Science 1980, 207, 645–647.
  • Agnati LF, Ferré S, Lluis C, Franco R, Fuxe K. Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol Rev 2003, 55, 509–550.
  • Avissar S, Amitai G, Sokolovsky M. Oligomeric structure of muscarinic receptors is shown by photoaffinity labeling: subunit assembly may explain high- and low-affinity agonist states. Proc Natl Acad Sci USA 1983, 80, 156–159.
  • Fraser CM, Venter JC. The size of the mammalian lung beta 2-adrenergic receptor as determined by target size analysis and immunoaffinity chromatography. Biochem Biophys Res Commun 1982, 109, 21–29.
  • Peterson GL, Rosenbaum LC, Broderick DJ, Schimerlik MI. Physical properties of the purified cardiac muscarinic acetylcholine receptor. Biochemistry 1986, 25, 3189–3202.
  • Herberg JT, Codina J, Rich KA, Rojas FJ, Iyengar R. The hepatic glucagon receptor. Solubilization, characterization, and development of an affinity adsorption assay for the soluble receptor. J Biol Chem 1984, 259, 9285–9294.
  • Ng GY, George SR, Zastawny RL, Caron M, Bouvier M, Dennis M, O’Dowd BF. Human serotonin1B receptor expression in Sf9 cells: phosphorylation, palmitoylation, and adenylyl cyclase inhibition. Biochemistry 1993, 32, 11727–11733.
  • Ng GY, Mouillac B, George SR, Caron M, Dennis M, Bouvier M, O’Dowd BF. Desensitization, phosphorylation and palmitoylation of the human dopamine D1 receptor. Eur J Pharmacol 1994, 267, 7–19.
  • Ng GY, O’Dowd BF, Caron M, Dennis M, Brann MR, George SR. Phosphorylation and palmitoylation of the human D2L dopamine receptor in Sf9 cells. J Neurochem 1994, 63, 1589–1595.
  • Ng GY, O’Dowd BF, Lee SP, Chung HT, Brann MR, Seeman P, George SR. Dopamine D2 receptor dimers and receptor-blocking peptides. Biochem Biophys Res Commun 1996, 227, 200–204.
  • George SR, Lee SP, Varghese G, Zeman PR, Seeman P, Ng GY, O’Dowd BF. A transmembrane domain-derived peptide inhibits D1 dopamine receptor function without affecting receptor oligomerization. J Biol Chem 1998, 273, 30244–30248.
  • Zawarynski P, Tallerico T, Seeman P, Lee SP, O’Dowd BF, George SR. Dopamine D2 receptor dimers in human and rat brain. FEBS Lett 1998, 441, 383–386.
  • Ciruela F, Casadó V, Mallol J, Canela EI, Lluis C, Franco R. Immunological identification of A1 adenosine receptors in brain cortex. J Neurosci Res 1995, 42, 818–828.
  • Bouvier M. Oligomerization of G-protein-coupled transmitter receptors. Nat Rev Neurosci 2001, 2, 274–286.
  • Franco R, Canals M, Marcellino D, Ferré S, Agnati L, Mallol J, Casadó V, Ciruela F, Fuxe K, Lluis C, Canela EI. Regulation of heptaspanning-membrane-receptor function by dimerization and clustering. Trends Biochem Sci 2003, 28, 238–243.
  • Milligan G, Bouvier M. Methods to monitor the quaternary structure of G protein-coupled receptors. FEBS J 2005, 272, 2914–2925.
  • Pfleger KD, Eidne KA. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat Methods 2006, 3, 165–174.
  • Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O’Dowd BF, George SR. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci USA 2007, 104, 654–659.
  • Juhasz JR, Hasbi A, Rashid AJ, So CH, George SR, O’Dowd BF. Mu-opioid receptor heterooligomer formation with the dopamine D1 receptor as directly visualized in living cells. Eur J Pharmacol 2008, 581, 235–243.
  • Carriba P, Navarro G, Ciruela F, Ferré S, Casadó V, Agnati L, Cortés A, Mallol J, Fuxe K, Canela EI, Lluís C, Franco R. Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat Methods 2008, 5, 727–733.
  • Gandia J, Galino J, Amaral OB, Soriano A, Lluís C, Franco R, Ciruela F. Detection of higher-order G protein-coupled receptor oligomers by a combined BRET-BiFC technique. FEBS Lett 2008, 582, 2979–2984.
  • Dupré DJ, Robitaille M, Ethier N, Villeneuve LR, Mamarbachi AM, Hébert TE. Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking. J Biol Chem 2006, 281, 34561–34573.
  • Guo W, Urizar E, Kralikova M, Mobarec JC, Shi L, Filizola M, Javitch JA. Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J 2008, 27, 2293–2304.
  • Lopez-Gimenez JF, Canals M, Pediani JD, Milligan G. The alpha1b-adrenoceptor exists as a higher-order oligomer: effective oligomerization is required for receptor maturation, surface delivery, and function. Mol Pharmacol 2007, 71, 1015–1029.
  • Navarro G, Carriba P, Gandía J, Ciruela F, Casadó V, Cortés A, Mallol J, Canela EI, Lluis C, Franco R. Detection of heteromers formed by cannabinoid CB1, dopamine D2, and adenosine A2A G-protein-coupled receptors by combining bimolecular fluorescence complementation and bioluminescence energy transfer. ScientificWorldJournal 2008, 8, 1088–1097.
  • Vidi PA, Chen J, Irudayaraj JM, Watts VJ. Adenosine A(2A) receptors assemble into higher-order oligomers at the plasma membrane. FEBS Lett 2008, 582, 3985–3990.
  • Chabre M, Cone R, Saibil H. Biophysics: is rhodopsin dimeric in native retinal rods? Nature 2003, 426, 30–1; discussion 31.
  • Romano C, Yang WL, O’Malley KL. Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J Biol Chem 1996, 271, 28612–28616.
  • Robbins MJ, Ciruela F, Rhodes A, McIlhinney RA. Characterization of the dimerization of metabotropic glutamate receptors using an N-terminal truncation of mGluR1alpha. J Neurochem 1999, 72, 2539–2547.
  • Ray K, Hauschild BC, Steinbach PJ, Goldsmith PK, Hauache O, Spiegel AM. Identification of the cysteine residues in the amino-terminal extracellular domain of the human Ca(2+) receptor critical for dimerization. Implications for function of monomeric Ca(2+) receptor. J Biol Chem 1999, 274, 27642–27650.
  • White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, Barnes AA, Emson P, Foord SM, Marshall FH. Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 1998, 396, 679–682.
  • Fotiadis D, Jastrzebska B, Philippsen A, Müller DJ, Palczewski K, Engel A. Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 2006, 16, 252–259.
  • Jastrzebska B, Fotiadis D, Jang GF, Stenkamp RE, Engel A, Palczewski K. Functional and structural characterization of rhodopsin oligomers. J Biol Chem 2006, 281, 11917–11922.
  • Hebert TE, Moffett S, Morello JP, Loisel TP, Bichet DG, Barret C, Bouvier M. A peptide derived from a beta2-adrenergic receptor transmembrane domain inhibits both receptor dimerization and activation. J Biol Chem 1996, 271, 16384–16392.
  • Lee SP, O’Dowd BF, Rajaram RD, Nguyen T, George SR. D2 dopamine receptor homodimerization is mediated by multiple sites of interaction, including an intermolecular interaction involving transmembrane domain 4. Biochemistry 2003, 42, 11023–11031.
  • Guo W, Shi L, Javitch JA. The fourth transmembrane segment forms the interface of the dopamine D2 receptor homodimer. J Biol Chem 2003, 278, 4385–4388.
  • Guo W, Shi L, Filizola M, Weinstein H, Javitch JA. Crosstalk in G protein-coupled receptors: changes at the transmembrane homodimer interface determine activation. Proc Natl Acad Sci USA 2005, 102, 17495–17500.
  • Fonseca JM, Lambert NA. Instability of a class a G protein-coupled receptor oligomer interface. Mol Pharmacol 2009, 75, 1296–1299.
  • Mancia F, Assur Z, Herman AG, Siegel R, Hendrickson WA. Ligand sensitivity in dimeric associations of the serotonin 5HT2c receptor. EMBO Rep 2008, 9, 363–369.
  • Berthouze M, Rivail L, Lucas A, Ayoub MA, Russo O, Sicsic S, Fischmeister R, Berque-Bestel I, Jockers R, Lezoualc’h F. Two transmembrane Cys residues are involved in 5-HT4 receptor dimerization. Biochem Biophys Res Commun 2007, 356, 642–647.
  • Hernanz-Falcón P, Rodríguez-Frade JM, Serrano A, Juan D, del Sol A, Soriano SF, Roncal F, Gómez L, Valencia A, Martínez-A C, Mellado M. Identification of amino acid residues crucial for chemokine receptor dimerization. Nat Immunol 2004, 5, 216–223.
  • Wang HX, Konopka JB. Identification of amino acids at two dimer interface regions of the alpha-factor receptor (Ste2). Biochemistry 2009, 48, 7132–7139.
  • Mikhailova MV, Blansett J, Jacobi S, Mayeux PR, Cornett LE. Transmembrane domain IV of the Gallus gallus VT2 vasotocin receptor is essential for forming a heterodimer with the corticotrophin releasing hormone receptor. J Biomed Opt 2008, 13, 031208.
  • González-Maeso J, Ang RL, Yuen T, Chan P, Weisstaub NV, López-Giménez JF, Zhou M, Okawa Y, Callado LF, Milligan G, Gingrich JA, Filizola M, Meana JJ, Sealfon SC. Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature 2008, 452, 93–97.
  • Carrillo JJ, López-Giménez JF, Milligan G. Multiple interactions between transmembrane helices generate the oligomeric alpha1b-adrenoceptor. Mol Pharmacol 2004, 66, 1123–1137.
  • Overton MC, Blumer KJ. The extracellular N-terminal domain and transmembrane domains 1 and 2 mediate oligomerization of a yeast G protein-coupled receptor. J Biol Chem 2002, 277, 41463–41472.
  • Filizola M. Increasingly accurate dynamic molecular models of G-protein coupled receptor oligomers: Panacea or Pandora’s box for novel drug discovery? Life Sci 2010, 86, 590–597.
  • Agnati LF, Guidolin D, Leo G, Carone C, Genedani S, Fuxe K. Receptor-receptor interactions: A novel concept in brain integration. Prog Neurobiol 2010, 90, 157–175.
  • Ciruela F, Burgueño J, Casadó V, Canals M, Marcellino D, Goldberg SR, Bader M, Fuxe K, Agnati LF, Lluis C, Franco R, Ferré S, Woods AS. Combining mass spectrometry and pull-down techniques for the study of receptor heteromerization. Direct epitope-epitope electrostatic interactions between adenosine A2A and dopamine D2 receptors. Anal Chem 2004, 76, 5354–5363.
  • Borroto-Escuela DO, Marcellino D, Narvaez M, Flajolet M, Heintz N, Agnati L, Ciruela F, Fuxe K. A serine point mutation in the adenosine A2AR C-terminal tail reduces receptor heteromerization and allosteric modulation of the dopamine D2R. Biochem Biophys Res Commun 2010, 394, 222–227.
  • Borroto-Escuela DO, García-Negredo G, Garriga P, Fuxe K, Ciruela F. The M(5) muscarinic acetylcholine receptor third intracellular loop regulates receptor function and oligomerization. Biochim Biophys Acta 2010, 1803, 813–825.
  • Zhang W, Yamada M, Gomeza J, Basile AS, Wess J. Multiple muscarinic acetylcholine receptor subtypes modulate striatal dopamine release, as studied with M1-M5 muscarinic receptor knock-out mice. J Neurosci 2002, 22, 6347–6352.
  • Aihara T, Nakamura Y, Taketo MM, Matsui M, Okabe S. Cholinergically stimulated gastric acid secretion is mediated by M(3) and M(5) but not M(1) muscarinic acetylcholine receptors in mice. Am J Physiol Gastrointest Liver Physiol 2005, 288, G1199–G1207.
  • Kawashima K, Fujii T. The lymphocytic cholinergic system and its contribution to the regulation of immune activity. Life Sci 2003, 74, 675–696.
  • Petaja-Repo UE, Hogue M, Laperriere A, Walker P, Bouvier M. Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human delta opioid receptor. J Biol Chem 2000, 275, 13727–13736.
  • Petaja-Repo UE, Hogue M, Laperriere A, Bhalla S, Walker P, Bouvier M. Newly synthesized human delta opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J Biol Chem 2001, 276, 4416–4423.
  • Reddy PS, Corley RB. Assembly, sorting, and exit of oligomeric proteins from the endoplasmic reticulum. Bioessays 1998, 20, 546–554.
  • Jones KA, Borowsky B, Tamm JA, Craig DA, Durkin MM, Dai M, Yao WJ, Johnson M, Gunwaldsen C, Huang LY, Tang C, Shen Q, Salon JA, Morse K, Laz T, Smith KE, Nagarathnam D, Noble SA, Branchek TA, Gerald C. GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 1998, 396, 674–679.
  • Kaupmann K, Schuler V, Mosbacher J, Bischoff S, Bittiger H, Heid J, Froestl W, Leonhard S, Pfaff T, Karschin A, Bettler B. Human gamma-aminobutyric acid type B receptors are differentially expressed and regulate inwardly rectifying K+ channels. Proc Natl Acad Sci USA 1998, 95, 14991–14996.
  • Kuner R, Köhr G, Grünewald S, Eisenhardt G, Bach A, Kornau HC. Role of heteromer formation in GABAB receptor function. Science 1999, 283, 74–77.
  • Kaupmann K, Huggel K, Heid J, Flor PJ, Bischoff S, Mickel SJ, McMaster G, Angst C, Bittiger H, Froestl W, Bettler B. Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 1997, 386, 239–246.
  • Bowery NG, Brown DA. The cloning of GABA(B) receptors. Nature 1997, 386, 223–224.
  • Isomoto S, Kaibara M, Sakurai-Yamashita Y, Nagayama Y, Uezono Y, Yano K, Taniyama K. Cloning and tissue distribution of novel splice variants of the rat GABAB receptor. Biochem Biophys Res Commun 1998, 253, 10–15.
  • Pfaff T, Malitschek B, Kaupmann K, Prézeau L, Pin JP, Bettler B, Karschin A. Alternative splicing generates a novel isoform of the rat metabotropic GABA(B)R1 receptor. Eur J Neurosci 1999, 11, 2874–2882.
  • Filippov AK, Couve A, Pangalos MN, Walsh FS, Brown DA, Moss SJ. Heteromeric assembly of GABA(B)R1 and GABA(B)R2 receptor subunits inhibits Ca(2+) current in sympathetic neurons. J Neurosci 2000, 20, 2867–2874.
  • Schwarz DA, Barry G, Eliasof SD, Petroski RE, Conlon PJ, Maki RA. Characterization of gamma-aminobutyric acid receptor GABAB(1e), a GABAB(1) splice variant encoding a truncated receptor. J Biol Chem 2000, 275, 32174–32181.
  • Briddon SJ, Gandía J, Amaral OB, Ferré S, Lluís C, Franco R, Hill SJ, Ciruela F. Plasma membrane diffusion of G protein-coupled receptor oligomers. Biochim Biophys Acta 2008, 1783, 2262–2268.
  • Sengupta P, Balaji J, Maiti S. Measuring diffusion in cell membranes by fluorescence correlation spectroscopy. Methods 2002, 27, 374–387.
  • Briddon SJ, Hill SJ. Pharmacology under the microscope: the use of fluorescence correlation spectroscopy to determine the properties of ligand-receptor complexes. Trends Pharmacol Sci 2007, 28, 637–645.
  • Licht SS, Sonnleitner A, Weiss S, Schultz PG. A rugged energy landscape mechanism for trapping of transmembrane receptors during endocytosis. Biochemistry 2003, 42, 2916–2925.
  • Philip F, Sengupta P, Scarlata S. Signaling through a G Protein-coupled receptor and its corresponding G protein follows a stoichiometrically limited model. J Biol Chem 2007, 282, 19203–19216.
  • Briddon SJ, Middleton RJ, Cordeaux Y, Flavin FM, Weinstein JA, George MW, Kellam B, Hill SJ. Quantitative analysis of the formation and diffusion of A1-adenosine receptor-antagonist complexes in single living cells. Proc Natl Acad Sci USA 2004, 101, 4673–4678.
  • Waldhoer M, Fong J, Jones RM, Lunzer MM, Sharma SK, Kostenis E, Portoghese PS, Whistler JL. A heterodimer-selective agonist shows in vivo relevance of G protein-coupled receptor dimers. Proc Natl Acad Sci USA 2005, 102, 9050–9055.
  • Chabre M, Deterre P, Antonny B. The apparent cooperativity of some GPCRs does not necessarily imply dimerization. Trends Pharmacol Sci 2009, 30, 182–187.
  • Jordan BA, Devi LA. G-protein-coupled receptor heterodimerization modulates receptor function. Nature 1999, 399, 697–700.
  • Berque-Bestel I, Lezoualc’h F, Jockers R. Bivalent ligands as specific pharmacological tools for G protein-coupled receptor dimers. Curr Drug Discov Technol 2008, 5, 312–318.
  • Daniels DJ, Lenard NR, Etienne CL, Law PY, Roerig SC, Portoghese PS. Opioid-induced tolerance and dependence in mice is modulated by the distance between pharmacophores in a bivalent ligand series. Proc Natl Acad Sci USA 2005, 102, 19208–19213.
  • Xie Z, Bhushan RG, Daniels DJ, Portoghese PS. Interaction of bivalent ligand KDN21 with heterodimeric delta-kappa opioid receptors in human embryonic kidney 293 cells. Mol Pharmacol 2005, 68, 1079–1086.
  • Daniels DJ, Kulkarni A, Xie Z, Bhushan RG, Portoghese PS. A bivalent ligand (KDAN-18) containing delta-antagonist and kappa-agonist pharmacophores bridges delta2 and kappa1 opioid receptor phenotypes. J Med Chem 2005, 48, 1713–1716.
  • Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001, 46, 3–26.
  • Israilova M, Tanaka T, Suzuki F, Morishima S, Muramatsu I. Pharmacological characterization and cross talk of alpha1a- and alpha1b-adrenoceptors coexpressed in human embryonic kidney 293 cells. J Pharmacol Exp Ther 2004, 309, 259–266.
  • Hornigold DC, Mistry R, Raymond PD, Blank JL, Challiss RA. Evidence for cross-talk between M2 and M3 muscarinic acetylcholine receptors in the regulation of second messenger and extracellular signal-regulated kinase signalling pathways in Chinese hamster ovary cells. Br J Pharmacol 2003, 138, 1340–1350.
  • Hanke S, Nürnberg B, Groll DH, Liebmann C. Cross talk between beta-adrenergic and bradykinin B(2) receptors results in cooperative regulation of cyclic AMP accumulation and mitogen-activated protein kinase activity. Mol Cell Biol 2001, 21, 8452–8460.
  • Charles AC, Mostovskaya N, Asas K, Evans CJ, Dankovich ML, Hales TG. Coexpression of delta-opioid receptors with micro receptors in GH3 cells changes the functional response to micro agonists from inhibitory to excitatory. Mol Pharmacol 2003, 63, 89–95.
  • Jordan BA, Gomes I, Rios C, Filipovska J, Devi LA. Functional interactions between mu opioid and alpha 2A-adrenergic receptors. Mol Pharmacol 2003, 64, 1317–1324.
  • Vilardaga JP, Nikolaev VO, Lorenz K, Ferrandon S, Zhuang Z, Lohse MJ. Conformational cross-talk between alpha2A-adrenergic and mu-opioid receptors controls cell signaling. Nat Chem Biol 2008, 4, 126–131.
  • Mellado M, Rodríguez-Frade JM, Vila-Coro AJ, Fernández S, Martín de Ana A, Jones DR, Torán JL, Martínez-A C. Chemokine receptor homo- or heterodimerization activates distinct signaling pathways. EMBO J 2001, 20, 2497–2507.
  • Fuxe K, Marcellino D, Guidolin D, Woods AS, Agnati LF. Heterodimers and receptor mosaics of different types of G-protein-coupled receptors. Physiology (Bethesda) 2008, 23, 322–332.
  • Fan T, Varghese G, Nguyen T, Tse R, O’Dowd BF, George SR. A role for the distal carboxyl tails in generating the novel pharmacology and G protein activation profile of mu and delta opioid receptor hetero-oligomers. J Biol Chem 2005, 280, 38478–38488.
  • Breitwieser GE. G protein-coupled receptor oligomerization: implications for G protein activation and cell signaling. Circ Res 2004, 94, 17–27.
  • Small KM, Schwarb MR, Glinka C, Theiss CT, Brown KM, Seman CA, Liggett SB. Alpha2A- and alpha2C-adrenergic receptors form homo- and heterodimers: the heterodimeric state impairs agonist-promoted GRK phosphorylation and beta-arrestin recruitment. Biochemistry 2006, 45, 4760–4767.
  • Rozenfeld R, Devi LA. Receptor heterodimerization leads to a switch in signaling: beta-arrestin2-mediated ERK activation by mu-delta opioid receptor heterodimers. FASEB J 2007, 21, 2455–2465.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.