Sequential inter- and intrasubunit rearrangements during activation of dimeric metabotropic glutamate receptor 1

Science Signaling

Volumn 5, Issue 237, 2012, Pages

  Hlavackova, Veronika ^a,b,c,d,e   Zabel, Ulrike ^a,b   Frankova, Daniela ^c   Bätz, Julia ^a   Hoffmann, Carsten ^a   Prezeau, Laurent ^d,e   Pin, Jean Philippe ^d,e   Blahos, Jaroslav ^c   Lohse, Martin J ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^d UNIV MONTPELLIER   (France)

^e INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; HOMODIMER; METABOTROPIC RECEPTOR 1; RECEPTOR SUBUNIT;

ARTICLE; CONFORMATIONAL TRANSITION; DIMERIZATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BACTERIAL PROTEINS; CALCIUM; CERCOPITHECUS AETHIOPS; COS CELLS; DIMERIZATION; DNA PRIMERS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; KINETICS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MUTATION, MISSENSE; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION;

EID: 84865180885     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002720     Document Type: Article

References (60)

1. L. Arcemisbéhère, T. Sen, L. Boudier, M. N. Balestre, G. Gaibelet, E. Detouillon, H. Orcel, C. Mendre, R. Rahmeh, S. Granier, C. Vivès, F. Fieschi, M. Damian, T. Durroux, J. L. Banères, B. Mouillac, Leukotriene BLT2 receptor monomers activate the Gi2 GTP-binding protein more efficiently than dimers. J. Biol. Chem. 285, 6337-6347 (2010).
2. O. P. Ernst, V. Gramse, M. Kolbe, K. P. Hofmann, M. Heck, Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit. Proc. Natl. Acad. Sci. U.S.A. 104, 10859-10864 (2007).
3. B. Jastrzebska, T. Maeda, L. Zhu, D. Fotiadis, S. Filipek, A. Engel, R. E. Stenkamp, K. Palczewski, Functional characterization of rhodopsin monomers and dimers in detergents. J. Biol. Chem. 279, 54663-54675 (2004).
4. A. J. Kuszak, S. Pitchiaya, J. P. Anand, H. I. Mosberg, N. G. Walter, R. K. Sunahara, Purification and functional reconstitution of monomeric μ-opioid receptors: Allosteric modulation of agonist binding by Gi2. J. Biol. Chem. 284, 26732-26741 (2009).
5. S. G. Rasmussen, B. T. DeVree, Y. Zou, A. C. Kruse, K. Y. Chung, T. S. Kobilka, F. S. Thian, P. S. Chae, E. Pardon, D. Calinski, J. M. Mathiesen, S. T. Shah, J. A. Lyons, M. Caffrey, S. H. Gellman, J. Steyaert, G. Skiniotis, W. I. Weis, R. K. Sunahara, B. K. Kobilka, Crystal structure of the β2 adrenergic receptor - Gs protein complex. Nature 477, 549-555 (2011).
6. M. R. Whorton, M. P. Bokoch, S. G. Rasmussen, B. Huang, R. N. Zare, B. Kobilka, R. K. Sunahara, 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, 7682-7687 (2007).
7. M. R. Whorton, B. Jastrzebska, P. S. Park, D. Fotiadis, A. Engel, K. Palczewski, R. K. Sunahara, Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J. Biol. Chem. 283, 4387-4394 (2008).
8. S. Ferré, A. S. Woods, G. Navarro, M. Aymerich, C. Lluis, R. Franco, Calcium-mediated modulation of the quaternary structure and function of adenosine A2A-dopamine D2 receptor heteromers. Curr. Opin. Pharmacol. 10, 67-72 (2010).
9. M. J. Lohse, Dimerization in GPCR mobility and signaling. Curr. Opin. Pharmacol. 10, 53-58 (2010).
10. J. P. Pin, R. Neubig, M. Bouvier, L. Devi, M. Filizola, J. A. Javitch, M. J. Lohse, G. Milligan, K. Palczewski, M. Parmentier, M. Spedding, International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol. Rev. 59, 5-13 (2007).
11. S. R. George, T. Fan, Z. Xie, R. Tse, V. Tam, G. Varghese, B. F. O'Dowd, Oligomerization of μ- and δ-opioid receptors. Generation of novel functional properties. J. Biol. Chem. 275, 26128-26135 (2000).
12. I. Gomes, B. A. Jordan, A. Gupta, N. Trapaidze, V. Nagy, L. A. Devi, Heterodimerization of μ and δ opioid receptors: A role in opiate synergy. J. Neurosci. 20, RC110 (2000).
13. R. C. Patel, U. Kumar, D. C. Lamb, J. S. Eid, M. Rocheville, M. Grant, A. Rani, T. Hazlett, S. C. Patel, E. Gratton, Y. C. Patel, Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells. Proc. Natl. Acad. Sci. U.S.A. 99, 3294-3299 (2002).
14. J. M. Rodríguez-Frade, A. J. Vila-Coro, A. M. de Ana, J. P. Albar, A. C. Martínez, M. Mellado, The chemokine monocyte chemoattractant protein-1 induces functional responses through dimerization of its receptor CCR2. Proc. Natl. Acad. Sci. U.S.A. 96, 3628-3633 (1999).
15. S. Angers, A. Salahpour, M. Bouvier, Dimerization: An emerging concept for G protein-coupled receptor ontogeny and function. Annu. Rev. Pharmacol. Toxicol. 42, 409-435 (2002).
16. S. Dorsch, K. N. Klotz, S. Engelhardt, M. J. Lohse, M. Bünemann, Analysis of receptor oligomerization by FRAP microscopy. Nat. Methods 6, 225-230 (2009).
17. D. Maurel, L. Comps-Agrar, C. Brock, M. L. Rives, E. Bourrier, M. A. Ayoub, H. Bazin, N. Tinel, T. Durroux, L. Prézeau, E. Trinquet, J. P. Pin, Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: Application to GPCR oligomerization. Nat. Methods 5, 561-567 (2008).
18. A. Salahpour, S. Angers, M. Bouvier, Functional significance of oligomerization of G-protein-coupled receptors. Trends Endocrinol. Metab. 11, 163-168 (2000).
19. M. J. Robbins, F. Ciruela, A. Rhodes, R. A. McIlhinney, Characterization of the dimerization of metabotropic glutamate receptors using an N-terminal truncation of mGluR1α. J. Neurochem. 72, 2539-2547 (1999).
20. C. Romano, W. L. Yang, K. L. O'Malley, Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271, 28612-28616 (1996).
21. J. H. White, A. Wise, M. J. Main, A. Green, N. J. Fraser, G. H. Disney, A. A. Barnes, P. Emson, S. M. Foord, F. H. Marshall, Heterodimerization is required for the formation of a functional GABAB receptor. Nature 396, 679-682 (1998).
22. A. S. Bessis, P. Rondard, F. Gaven, I. Brabet, N. Triballeau, L. Prézeau, F. Acher, J. P. Pin, Closure of the Venus flytrap module of mGlu8 receptor and the activation process: Insights from mutations converting antagonists into agonists. Proc. Natl. Acad. Sci. U.S.A. 99, 11097-11102 (2002).
23. K. Kaupmann, B. Malitschek, V. Schuler, J. Heid, W. Froestl, P. Beck, J. Mosbacher, S. Bischoff, A. Kulik, R. Shigemoto, A. Karschin, B. Bettler, GABAB-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687 (1998).
24. C. Parnot, B. Kobilka, Toward understanding GPCR dimers. Nat. Struct. Mol. Biol. 11, 691-692 (2004).
25. M. Tateyama, H. Abe, H. Nakata, O. Saito, Y. Kubo, Ligand-induced rearrangement of the dimeric metabotropic glutamate receptor 1α. Nat. Struct. Mol. Biol. 11, 637-642 (2004).
26. M. J. Lohse, P. Hein, C. Hoffmann, V. O. Nikolaev, J. P. Vilardaga, M. Bünemann, Kinetics of G-protein-coupled receptor signals in intact cells. Br. J. Pharmacol. 153 (Suppl. 1), S125-S132 (2008).
27. C. Goudet, J. Kniazeff, V. Hlavackova, F. Malhaire, D. Maurel, F. Acher, J. Blahos, L. Prézeau, J. P. Pin, Asymmetric functioning of dimeric metabotropic glutamate receptors disclosed by positive allosteric modulators. J. Biol. Chem. 280, 24380-24385 (2005).
28. V. Hlavackova, C. Goudet, J. Kniazeff, A. Zikova, D. Maurel, C. Vol, J. Trojanova, L. Prézeau, J. P. Pin, J. Blahos, Evidence for a single heptahelical domain being turned on upon activation of a dimeric GPCR. EMBO J. 24, 499-509 (2005).
29. F. K. Chan, R. M. Siegel, D. Zacharias, R. Swofford, K. L. Holmes, R. Y. Tsien, M. J. Lenardo, Fluorescence resonance energy transfer analysis of cell surface receptor interactions and signaling using spectral variants of the green fluorescent protein. Cytometry 44, 361-368 (2001).
30. C. Hoffmann, G. Gaietta, M. Bünemann, S. R. Adams, S. Oberdorff-Maass, B. Behr, J. P. Vilardaga, R. Y. Tsien, M. H. Ellisman, M. J. Lohse, A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat. Methods 2, 171-176 (2005).
31. J. B. Jensen, J. S. Lyssand, C. Hague, B. Hille, Fluorescence changes reveal kinetic steps of muscarinic receptor-mediated modulation of phosphoinositides and Kv7.2/7.3 K+ channels. J. Gen. Physiol. 133, 347-359 (2009).
32. M. Maier-Peuschel, N. Frölich, C. Dees, L. G. Hommers, C. Hoffmann, V. O. Nikolaev, M. J. Lohse, A fluorescence resonance energy transfer-based M2 muscarinic receptor sensor reveals rapid kinetics of allosteric modulation. J. Biol. Chem. 285, 8793-8800 (2010).
33. S. Reiner, M. Ambrosio, C. Hoffmann, M. J. Lohse, Differential signaling of the endogenous agonists at the β2-adrenergic receptor. J. Biol. Chem. 285, 36188-36198 (2010).
34. F. Rochais, J. P. Vilardaga, V. O. Nikolaev, M. Bünemann, M. J. Lohse, S. Engelhardt, Real-time optical recording of β1-adrenergic receptor activation reveals supersensitivity of the Arg389 variant to carvedilol. J. Clin. Invest. 117, 229-235 (2007).
35. J. P. Vilardaga, M. Bünemann, C. Krasel, M. Castro, M. J. Lohse, Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat. Biotechnol. 21, 807-812 (2003).
36. N. Ziegler, J. Bätz, U. Zabel, M. J. Lohse, C. Hoffmann, FRET-based sensors for the human M1-, M3-, and M5-acetylcholine receptors. Bioorg. Med. Chem. 19, 1048-1054 (2011).
37. M. Bünemann, M. Frank, M. J. Lohse, Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. U.S.A. 100, 16077-16082 (2003).
38. P. Hein, M. Frank, C. Hoffmann, M. J. Lohse, M. Bünemann, Dynamics of receptor/G protein coupling in living cells. EMBO J. 24, 4106-4114 (2005).
39. P. Hein, F. Rochais, C. Hoffmann, S. Dorsch, V. O. Nikolaev, S. Engelhardt, C. H. Berlot, M. J. Lohse, M. Bünemann, Gs activation is time-limiting in initiating receptor-mediated signaling. J. Biol. Chem. 281, 33345-33351 (2006).
40. M. J. Lohse, V. O. Nikolaev, P. Hein, C. Hoffmann, J. P. Vilardaga, M. Bünemann, Optical techniques to analyze real-time activation and signaling of G-protein-coupled receptors. Trends Pharmacol. Sci. 29, 159-165 (2008).
41. V. O. Nikolaev, M. Bünemann, L. Hein, A. Hannawacker, M. J. Lohse, Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37215-37218 (2004).
42. P. Marcaggi, H. Mutoh, D. Dimitrov, M. Beato, T. Knöpfel, Optical measurement of mGluR1 conformational changes reveals fast activation, slow deactivation, and sensitization. Proc. Natl. Acad. Sci. U.S.A. 106, 11388-11393 (2009).
43. J. Kniazeff, A. S. Bessis, D. Maurel, H. Ansanay, L. Prézeau, J. P. Pin, Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat. Struct. Mol. Biol. 11, 706-713 (2004).
44. C. Joly, J. Gomeza, I. Brabet, K. Curry, J. Bockaert, J. P. Pin, Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: Comparison with mGluR1. J. Neurosci. 15, 3970-3981 (1995).
45. 3H]quisqualate binding to recombinant rat metabotropic glutamate 1a and 5a receptors and to rat and human brain sections. J. Neurochem. 75, 2590-2601 (2000).
46. N. Kunishima, Y. Shimada, Y. Tsuji, T. Sato, M. Yamamoto, T. Kumasaka, S. Nakanishi, H. Jingami, K. Morikawa, Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977 (2000).
47. T. Muto, D. Tsuchiya, K. Morikawa, H. Jingami, Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 3759-3764 (2007).
48. J. P. Pin, J. Kniazeff, C. Goudet, A. S. Bessis, J. Liu, T. Galvez, F. Acher, P. Rondard, L. Prézeau, The activation mechanism of class-C G-protein coupled receptors. Biol. Cell 96, 335-342 (2004).
49. 2A-adrenergic receptor and Gi-protein heterotrimer. J. Biol. Chem. 281, 24506-24511 (2006).
50. I. Brabet, S. Mary, J. Bockaert, J. P. Pin, Phenylglycine derivatives discriminate between mGluR1- and mGluR5-mediated responses. Neuropharmacology 34, 895-903 (1995).
51. P. Rondard, J. Liu, S. Huang, F. Malhaire, C. Vol, A. Pinault, G. Labesse, J. P. Pin, Coupling of agonist binding to effector domain activation in metabotropic glutamatelike receptors. J. Biol. Chem. 281, 24653-24661 (2006).
52. C. Brock, N. Oueslati, S. Soler, L. Boudier, P. Rondard, J. P. Pin, Activation of a dimeric metabotropic glutamate receptor by intersubunit rearrangement. J. Biol. Chem. 282, 33000-33008 (2007).
53. 2 adrenergic receptor. J. Biol. Chem. 276, 24433-24436 (2001).
54. 2Y receptors with b-arrestin-1 and -2. J. Biol. Chem. 283, 30933-30941 (2008).
55. B. K. Kobilka, Structural insights into adrenergic receptor function and pharmacology. Trends Pharmacol. Sci. 32, 213-218 (2011).
56. 2-adrenoceptor. Nat. Chem. Biol. 2, 417-422 (2006).
57. 2A-adrenergic receptor activation reveals distinct agonist-specific conformational changes. Mol. Pharmacol. 75, 534-541 (2009).
58. M. Damian, A. Martin, D. Mesnier, J. P. Pin, J. L. Banères, Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J. 25, 5693-5702 (2006).
59. J. P. Vilardaga, V. O. Nikolaev, K. Lorenz, S. Ferrandon, Z. Zhuang, M. J. Lohse, Conformational cross-talk between a2A-adrenergic and μ-opioid receptors controls cell signaling. Nat. Chem. Biol. 4, 126-131 (2008).
60. I. Brabet, M. L. Parmentier, C. De Colle, J. Bockaert, F. Acher, J. P. Pin, Comparative effect of L-CCG-I, DCG-IV and γ-carboxy-L-glutamate on all cloned metabotropic glutamate receptor subtypes. Neuropharmacology 37, 1043-1051 (1998).