Distinct roles of metabotropic glutamate receptor dimerization in agonist activation and G-protein coupling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages 16342-16347

  El Moustaine, Driss ^a,b   Granier, Sébastien ^a,b   Doumazane, Etienne ^a,b   Scholler, Pauline ^a,b   Rahmeh, Rita ^a,b   Bron, Patrick ^b   Mouillac, Bernard ^a,b   Banères, Jean Louis ^c   Rondard, Philippe ^a,b   Pin, Jean Philippe ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

Oligomerization; SNAP tag; Time resolved FRET

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR;

ARTICLE; DIMERIZATION; PRIORITY JOURNAL; PROTEIN STRUCTURE;

DIMERIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUTAMIC ACID; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; INOSITOL PHOSPHATES; MICROSCOPY, ELECTRON, TRANSMISSION; NANOSTRUCTURES; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84867045173     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205838109     Document Type: Article

References (54)

1. Nicoletti F, et al. (2011) Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 60:1017-1041.
2. Niswender CM, Conn PJ (2010) Metabotropic glutamate receptors: Physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50:295-322.
3. Swanson CJ, et al. (2005) Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat Rev Drug Discov 4:131-144. (Pubitemid 40277494)
4. Bräuner-Osborne H, Wellendorph P, Jensen AA (2007) Structure, pharmacology and therapeutic prospects of family C G-protein coupled receptors. Curr Drug Targets 8: 169-184. (Pubitemid 46049458)
5. Romano C, Yang WL, O'Malley KL (1996) Metabotropic glutamate receptor 5 is a di-sulfide- linked dimer. J Biol Chem 271:28612-28616. (Pubitemid 26374686)
6. Doumazane E, et al. (2011) A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J 25:66-77.
7. Kniazeff J, Prézeau L, Rondard P, Pin J-P, Goudet C (2011) Dimers and beyond: The functional puzzles of class C GPCRs. Pharmacol Ther 130:9-25.
8. Rondard P, Goudet C, Kniazeff J, Pin J-P, Prézeau L (2011) The complexity of their activation mechanism opens new possibilities for the modulation of mGlu and GABAB class C G protein-coupled receptors. Neuropharmacology 60:82-92.
9. Kunishima N, et al. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407:971-977.
10. Urwyler S (2011) Allosteric modulation of family C G-protein-coupled receptors: From molecular insights to therapeutic perspectives. Pharmacol Rev 63:59-126.
11. Bessis A-S, et al. (2002) Closure of the Venus flytrap module of mGlu8 receptor and the activation process: Insights from mutations converting antagonists into agonists. Proc Natl Acad Sci USA 99:11097-11102. (Pubitemid 34920885)
12. Kniazeff J, et al. (2004) Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat Struct Mol Biol 11:706-713. (Pubitemid 39014495)
13. Kniazeff J, et al. (2004) Locking the dimeric GABA(B) G-protein-coupled receptor in its active state. J Neurosci 24:370-377. (Pubitemid 38112368)
14. Muto T, Tsuchiya D, Morikawa K, Jingami H (2007) Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc Natl Acad Sci USA 104:3759-3764. (Pubitemid 47189144)
15. Tsuchiya D, Kunishima N, Kamiya N, Jingami H, Morikawa K (2002) Structural views of the ligand-binding cores of a metabotropic glutamate receptor complexed with an antagonist and both glutamate and Gd3+. Proc Natl Acad Sci USA 99:2660-2665. (Pubitemid 34240517)
16. Binet V, et al. (2007) Common structural requirements for heptahelical domain function in class A and class C G protein-coupled receptors. J Biol Chem 282: 12154-12163. (Pubitemid 47103115)
17. Goudet C, et al. (2005) Asymmetric functioning of dimeric metabotropic glutamate receptors disclosed by positive allosteric modulators. J Biol Chem 280:24380-24385. (Pubitemid 40934521)
18. Hlavackova V, et al. (2005) Evidence for a single heptahelical domain being turned on upon activation of a dimeric GPCR. EMBO J 24:499-509. (Pubitemid 40343252)
19. Hlavackova V, et al. (2012) Sequential inter- and intra-subunit rearrangements during asymmetric activation of dimeric metabotropic glutamate receptor 1. Sci Signal, 10.1126/scisignal.2002720.
20. Rondard P, et al. (2008) Functioning of the dimeric GABA(B) receptor extracellular domain revealed by glycan wedge scanning. EMBO J 27:1321-1332. (Pubitemid 351655177)
21. Marcaggi P, Mutoh H, Dimitrov D, Beato M, Knöpfel T (2009) Optical measurement of mGluR1 conformational changes reveals fast activation, slow deactivation, and sensitization. Proc Natl Acad Sci USA 106:11388-11393.
22. TateyamaM, Abe H, Nakata H, Saito O, Kubo Y (2004) Ligand-induced rearrangement of the dimeric metabotropic glutamate receptor 1alpha. Nat Struct Mol Biol 11: 637-642. (Pubitemid 38823530)
23. Goudet C, et al. (2004) Heptahelical domain of metabotropic glutamate receptor 5 behaves like rhodopsin-like receptors. Proc Natl Acad Sci USA 101:378-383.
24. Maurel D, et al. (2008) Cell-surface protein-protein interaction analysis with timeresolved FRET and snap-tag technologies: Application to GPCR oligomerization. Nat Methods 5:561-567. (Pubitemid 351761765)
25. Johnson MP, et al. (2003) Discovery of allosteric potentiators for the metabotropic glutamate 2 receptor: Synthesis and subtype selectivity of N-(4-(2-methoxyphenoxy) phenyl)-N-(2,2,2- trifluoroethylsulfonyl)pyrid-3- ylmethylamine. J Med Chem 46: 3189-3192. (Pubitemid 36842403)
26. Bayburt TH, Leitz AJ, Xie G, Oprian DD, Sligar SG (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J Biol Chem 282: 14875-14881. (Pubitemid 47093370)
27. Whorton MR, et al. (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. (Pubitemid 47185966)
28. Whorton MR, et al. (2008) Ef ficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283:4387-4394.
29. Rondard P, et al. (2006) Coupling of agonist binding to effector domain activation in metabotropic glutamate-like receptors. J Biol Chem 281:24653-24661. (Pubitemid 44274238)
30. Kobilka BK (1995) Amino and carboxyl terminal modifications to facilitate the production and purification of a G protein-coupled receptor. Anal Biochem 231:269-271.
31. Granier S, et al. (2007) Structure and conformational changes in the C-terminal domain of the beta2-adrenoceptor: insights from fluorescence resonance energy transfer studies. J Biol Chem 282:13895-13905. (Pubitemid 47100565)
32. Malherbe P, et al. (2003) Mutational analysis and molecular modeling of the binding pocket of the metabotropic glutamate 5 receptor negative modulator 2-methyl-6-(phenylethynyl)-pyridine. Mol Pharmacol 64:823-832. (Pubitemid 37153050)
33. Denisov IG, Grinkova YV, Lazarides AA, Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J Am Chem Soc 126:3477-3487. (Pubitemid 38366738)
34. Hemstapat K, et al. (2007) A novel family of potent negative allosteric modulators of group II metabotropic glutamate receptors. J Pharmacol Exp Ther 322:254-264. (Pubitemid 46956377)
35. Oldham WM, Van Eps N, Preininger AM, Hubbell WL, Hamm HE (2006) Mechanism of the receptor-catalyzed activation of heterotrimeric G proteins. Nat Struct Mol Biol 13: 772-777. (Pubitemid 44338770)
36. Oldham WM, Van Eps N, Preininger AM, Hubbell WL, Hamm HE (2007) Mapping allosteric connections from the receptor to the nucleotide-binding pocket of heterotrimeric G proteins. Proc Natl Acad Sci USA 104:7927-7932. (Pubitemid 47185853)
37. Francesconi A, Duvoisin RM (1998) Role of the second and third intracellular loops of metabotropic glutamate receptors in mediating dual signal transduction activation. J Biol Chem 273:5615-5624. (Pubitemid 28124031)
38. Johnson BG, et al. (1999) [3H]-LY341495 as a novel antagonist radioligand for group II metabotropic glutamate (mGlu) receptors: Characterization of binding to membranes of mGlu receptor subtype expressing cells. Neuropharmacology 38:1519-1529. (Pubitemid 29457734)
39. Galvez T, et al. (2001) Allosteric interactions between GB1 and GB2 subunits are required for optimal GABA(B) receptor function. EMBO J 20:2152-2159. (Pubitemid 32410585)
40. Xu H, et al. (2004) Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci USA 101:14258-14263. (Pubitemid 39305062)
41. Albizu L, et al. (2010) Time-resolved FRET between ligands bound on asymmetric G protein-coupled receptor reveals oligomers in native tissues. Nat Chem Biol 6: 587-594.
42. Damian M, Martin A, Mesnier D, Pin JP, Banères JL (2006) Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J 25:5693-5702. (Pubitemid 44967753)
43. 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 5:688-695.
44. Monnier C, et al. (2011) Trans-activation between 7TM domains: implication in heterodimeric GABAB receptor activation. EMBO J 30:32-42.
45. Duthey B, et al. (2002) A single subunit (GB2) is required for G-protein activation by the heterodimeric GABA(B) receptor. J Biol Chem 277:3236-3241. (Pubitemid 34953187)
46. Huang S, et al. (2011) Interdomain movements in metabotropic glutamate receptor activation. Proc Natl Acad Sci USA 108:15480-15485.
47. Lefkowitz RJ, Shenoy SK (2005) Transduction of receptor signals by beta-arrestins. Science 308:512-517.
48. Bockaert J, Perroy J, Bécamel C, Marin P, Fagni L (2010) GPCR interacting proteins (GIPs) in the nervous system: Roles in physiology and pathologies. Annu Rev Pharmacol Toxicol 50:89-109.
49. 1 receptor/RGS20/G(i) protein complex reveal asymmetry of receptor dimers for RGS and G(i) coupling. EMBO J 29:3646-3659.
50. Bouvier M (2001) Oligomerization of G-protein-coupled transmitter receptors. Nat Rev Neurosci 2:274-286.
51. Lohse MJ (2010) Dimerization in GPCR mobility and signaling. Curr Opin Pharmacol 10:53-58.
52. Granier S, Kim S, Fung JJ, Bokoch MP, Parnot C (2009) FRET-based measurement of GPCR conformational changes. Methods Mol Biol 552:253-268.
53. Bayburt TH, Grinkova YV, Sligar SG (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett 2:853-856. (Pubitemid 135706448)
54. Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nat Protoc 1:418-428.