The heteromeric GABA-B receptor recognizes G-protein α subunit C-termini

Neuropharmacology

Volumn 38, Issue 11, 1999, Pages 1657-1666

  Franek, Miloslav ^a,b   Pagano, Adriana ^c,d   Kaupmann, Klemens ^c   Bettler, Bernhard ^c   Pin, Jean Philippe ^a   Blahos, Jaroslav ^a,b  

^a CNRS UPR9023   (France)

^b CHARLES UNIVERSITY   (Czech Republic)

^c NOVARTIS PHARMA AG   (Switzerland)

^d UNIVERSITY OF CATANIA   (Italy)

Author keywords

Dimerization; G protein coupled receptors; GABA B receptor; GTP binding protein

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR; PHOSPHOLIPASE C; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELLS, CULTURED; GABA AGONISTS; GAMMA-AMINOBUTYRIC ACID; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; INOSITOL PHOSPHATES; KIDNEY; RATS; RECEPTORS, GABA-B;

EID: 0032846317     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(99)00135-5     Document Type: Article

References (52)

1. Bae H., Anderson K., Flood L.A., Skiba N.P., Hamm H.E., Graber S.G. Molecular determinants of selectivity in 5-hydroxytryptamine (1B) receptor-G protein interactions. J. Biol. Chem. 272:1997;32071-32077.
2. Bahia D.S., Wise A., Fanelli F., Lee M., Rees S., Milligan G. Hydrophobicity of residue351 of the G protein Gil alpha determines the extent of activation by the alpha 2A-adrenoceptor. Biochemistry. 37:1998;11555-11562.
3. Bai M., Trivedi S., Brown E.M. Dimerization of the extracellular calcium-sensing receptor (CaR) on the cell surface of CaR-transfected HEK293 cells. J. Biol. Cell. 273:1998;23605-23610.
4. Berridge M., Dawson R., Downes C., Heslop J., Irvine R. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem. J. 212:1983;473-482.
5. Bettler B., Kaupmann K., Bowery N. GABA-B receptors: drugs meet clones. Curr. Opin. Neurobiol. 8:1998;345-350.
6. Blahos II, J., Mary, S., Perroy, J., de Colle, C., Brabet, I., Bockaert, J., Pin, J.-P., 1998. Extreme C-terminus of G-protein α-subunits contains a site that discriminates between Gi-coupled metabotropic glutamate receptors. J. Biol. Chem. 273, 25765-25769.
7. Blin N., Yun J., Wess J. Mapping of single amino acid residues required for selective activation of Gq/11 by m3 muscarinic acetylcholine receptor. J. Biol. Chem. 270:1995;17741-17748.
8. Bockaert J., Pin J.-P. Molecular tinkering of G-protein coupled receptors: an evolutionary success. EMBO J. 18:1999;1723-1729.
9. Bourne H.R. How receptors talk to trimeric G proteins. Curr. Opin. Cell Biol. 9:1997;134142.
10. 2+ currents in rat sensory neurones by G protein Go: antisense oligonucleotide studies. J. Physiol. (Lond.)470, 1-11.
11. Conklin B.R., Farfel Z., Lustig K.D., Julius D., Bourne H.R. Substitution of three amino acids switches receptor specificity of Gqα to that of Giα Nature. 363:1993;274-276.
12. Conklin B.R., Herzmark P., Ishida S., Voyno-Yasenetskaya T.A., Sun Y., Farfel Z., Bourne H. Carboxyl-terminal mutations of Gαa and Gαa that alter the fidelity of receptor activation. Mol. Pharmacol. 50:1996;885-890.
13. Dratz E.A., Furstenau J.E., Lambert C.G., Thireault D.L., Rarick H., Schepers T., Pakhlevaniants S., Hamm H.E. NMR structure of a receptor-bound G-protein peptide. Nature. 363:1993;276-281.
14. Galvez T., Parmentier M.-L., Joly C., Malitschek B., Kaupmann K., Kuhn R., Bittiger H., Froestl W., Bettler B., Pin J.-P. Mutagenesis and modeling of the GABA-B receptor binding site suggest a Venus Fly-trap mechanism for ligand binding. J. Biol. Chem. 274:1999;13362-13369.
15. Gilchrist A., Mazzoni M.R., Dineen B., Dice A., Linden J., Proctor W.R., Lupica C.R., Dunwiddie T.V., Hamm H.E. Antagonists of the receptor-G protein interface block Gi-coupled signal transduction. J. Biol. Chem. 273:1998;14912-14919.
16. Gomeza J., Joly C., Kuhn R., Knopfel T., Bockaert J., Pin J.-P. The second intracellular loop of mGluR1 cooperates with the other intracellular domains to control coupling to G-protein. J. Biol. Chem. 271:1996a;2199-2205.
17. Gomeza J., Mary S., Brabet I., Parmentier M.-L., Restituito S., Bockaert J., Pin J.-P. Coupling of mGluR2 and mGluR4 to Gα15, Gα16 and chimeric Gαq/i proteins: characterization of new antagonists. Mol. Pharmacol. 50:1996;923-930.
18. Hamm H.E., Deretic D., Arendt A., Hargrave P.A., Koenig B., Hofmann K.P. Site of G protein binding to rhodopsin mapped with synthetic peptides from the α subunit. Science. 241:1988;832-835.
19. Hawrot E., Xiao Y., Shi Q.-I., Norman D., Kirkitadze M., Barlow P.N. Demonstration of a tandem pair of complement protein modules in GABAB receptorla. FEBS Lett. 432:1998;103-108.
20. Hebert T.E., Moffett S., Morello J.P., Loisel T.P., Bichet D.G., garret C., Bouvier M. A peptide derived from a beta2-adrenergic receptor transmembrane domain inhibits both receptor dimerization and activation. J. Biol. Chem. 271:1996;16384-16392.
21. Hinton D.R., Blanks J.C., Fong H.K.W., Casey P.J., Hildebrandt E., Simons M.I. Novel localization of a G protein, Gz-α, in neurons of brain and retina. J. Neuroscience. 10:1990;2763-2770.
22. Jeong S.-W., Ikeda S.R. G protein α subunit Gαz couples neurotransmitter receptors to ion channels in sympathetic neurons. Neuron. 21:1998;1201-1212.
23. Jones K.A., Borowsky B., Tamm J.A., Craig D.A., Durkin M.M., Dai M., Yao W.-J., Johnson M., Gunwaldsen C., Huang L.-Y., Tang C., Shen Q., Salon J.A., Morse K., Laz T., Smith K.E., Nagarathnam D., Noble S.A., Branchek T.A., Gerald C. GABA B receptors function as a heteromeric assembly of the subunits GABA B R1 and GABA B R2. Nature. 396:1998;674-679.
24. Kaupmann K., Huggel K., Heid J., Flor P.J., Bischoff S., Mickel S.J., McMaster G., Angst C., Bittiger H., Froestl W., Bettler B. Expression cloning of GABA-B receptors uncovers similarity to metabotropic glutamate receptors. Nature. 386:1997;239-246.
25. Kaupmann K., Malitschek B., Schuler V., Heid J., Froestl W., Beck P., Mosbacher J., Bishoff S., Kulik A., Shigemoto R., Karschin A., Bettler B. GABA-B receptor subtypes assemble into functional heteromeric complexes. Nature. 396:1998;683-687.
26. 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. 95:1998;14991-14996.
27. Kerr D.I., Ong J. GABA-B receptors. Pharmacol. Ther. 67:1995;187-246.
28. Kostenis E., Conklin B.R., Wess J. Molecular basis of receptor/G protein coupling selectivity studied by coexpression of wild type and mutant m2 muscarinic receptors with mutant G alpha(q) subunits. Biochemistry. 36:1997;1487-1495.
29. Kostenis E., Gomeza J., Lerche C., Wess J. Genetic analysis of receptor-G alpha(q) coupling selectivity. J. Biol. Chem. 272:1997;23675-23681.
30. Kuner R., Kohr G., Grunewald S., Eisenhardt G., Bach A., Kornau H.C. Role of heteromer formation in GABAB receptor function. Science. 283:1999;74-77.
31. Lichtarge O., Bourne H.R., Cohen F.E. Evolutionarily conserved G(alpha beta gamma) binding surfaces support a model of the G protein-receptor complex. Proc. Natl. Acad. Sci. USA. 93:1996;7507-7511.
32. Liu J., Conklin B.R., Thin N., Yun J., Wess J. Identification of a receptor G-protein contact site critical for signaling specificity and G-protein activation. Proc. Natl. Acad. Sci. USA. 92:1995;11642-11646.
33. Maggio R., Vogel Z., Wess J. Coexpression studies with mutant muscarinic/adrenergic receptors provide evidence for intermolecular 'cross-talk' between G-protein-linked receptors. Proc. Natl. Acad. Sci. USA. 90:1993;3103-3107.
34. Malitschek, B., Schweizer, C., Keir, M. Heid, J., Froestl, W., Mosbacher, J., Kuhn, R., Henley, J., Joly, C., Pin, J.-P., Kaupmann, K., Bettler, B., 1999. The N-terminal domain of GABA-B receptors is aufficient to specify agonist and antagonist binding. Mol. Pharmacol. 56, 448-454.
35. Milligan G., Marshall F., Rees S. G16 as a universal G protein adapter: implications for agonist screening strategies. Trends Pharmacol. Sci. 17:1996;235-237.
36. Milligan G., Rees S. Chimaeric G α proteins: their potential use in drug discovery. Trends Pharmacol. Sci. 20:1999;118-124.
37. O'Hara P.J., Sheppard P.O., Thogersen H., Venezia D., Haldeman B.A., McGrane V., Houamed K.M., Thomsen C., Gilbert T.L., Mulvihill E.R. The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron. 11:1993;41-52.
38. Offermanns S., Simon M.I. Gα15 and Gα16 couple a wide variety of receptors to phospholipase C. J. Biol. Chem. 270:1995;15175-15180.
39. Olpe H.R., Karlsson G., Pozza M.F., Brugger F., Steinmann M., Van Riezen H., Fagg G., Hall R.G., Froestl W., Bittiger H. CGP 35348: a centrally active blocker of GABAB receptors. Eur. J. Pharmacol. 187:1990;27-38.
40. Onrust R., Herzmark P., Chi P., Garcia P.D., Lichtarge O., Kingsley C., Bourne H. Receptor and βγ binding sites in the α subunit of the retinal G protein transducin. Science. 275:1997;381-384.
41. Palm D., Munch G., Malek D., Dees C., Hekman M. Identification of a Gs-protein coupling domain to the beta-adrenoceptor using site-specific synthetic peptides. Carboxyl terminus of Gs alpha is involved in coupling to beta-adrenoceptors. FEBS Lett. 261:1990;294-298.
42. Parmentier M.L., Joly C., Restituito S., Bockaert J., Grau Y., Pin J.-P. The G-protein coupling profile of metabotropic glutamate receptors, as determined with exogenous G-proteins, is independent of their ligand recognition domain. Mol. Pharmacol. 53:1998;778-786.
43. Pin J.-P., Joly C., Heinemann S.F., Bockaert J. Domains involved in the specificity of G protein activation in phospholipase C coupled metabotropic glutamate receptor. EMBO J. 13:1994;342-348.
44. Romano C., Yang W.-L., O'Malley K.L. Metabotropic glutamate receptor 5 is a distilfide-linked dimer. J. Biol. Chem. 271:1996;28612-28616.
45. Simon M.I., Strathmann M.P., Gautam N. Diversity of G proteins in signal transduction. Science. 252:1991;802-808.
46. Sodickson D.L., Bean B.P. GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J. Neurosci. 16:1996;6374-6385.
47. Takahashi K., Tsuchida K., Tanabe Y., Masu M., Nakanishi S. Role of the large extracellular domain of metabotropic glutamate receptors in agonist selectivity determination. J. Biol. Chem. 268:1993;19341-19345.
48. Takahashi T., Kajikawa Y., Tsujimoto T. G-protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J. Neurosci. 18:1998;3138-3146.
49. Umemori H., Inoue T., Kume S., Sekiyama N., Nagao M., Itoh H., Nakanishi S., Mikoshiba K., Yamamoto T. Activation of the G protein Gq/11 through tyrosine phosphorylation of the alpha subunit. Science. 276:1997;1878-1881.
50. Wess J. G-protein-coupled receptors: molecular mechanisms involved in receptor activation and selectivity of G-protein recognition. FASEB J. 11:1997;346-354.
51. White J.H., Wise A., Main M.J., Green A., Fraser N.J., Disney G.H., Barnes A.A., Emson P., Foord S.M., Marshall F.H. Heterodimerisation is required for the formation of a functional GABA B receptor. Nature. 396:1998;679-682.
52. Wong Y.H., Conklin B.R., Bourne H.R. Gz-mediated hormonal inhibition of cyclic AMP accumulation. Science. 255:1992;339-342.