Glutamate acts as a partial inverse agonist to metabotropic glutamate receptor with a single amino acid mutation in the transmembrane domain

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 9593-9601

  Yanagawa, Masataka ^a   Yamashita, Takahiro ^a   Shichida, Yoshinori ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; FLUORESCENCE ENERGY TRANSFER; G-PROTEIN COUPLED RECEPTORS; HYDROGEN BONDING NETWORK; METABOTROPIC GLUTAMATE RECEPTORS; MUTATIONAL EXPERIMENTS; STRUCTURAL INFORMATION; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; AMINO ACIDS; ENERGY TRANSFER; HYDROGEN BONDS;

BIOLOGICAL MEMBRANES;

G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; METABOTROPIC RECEPTOR; RHODOPSIN;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HYDROGEN BOND; LIGAND BINDING; MUTATION; MUTATIONAL ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; CATTLE; DNA MUTATIONAL ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUTAMIC ACID; GLYCINE; HEK293 CELLS; HUMANS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENOTYPE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECEPTORS, METABOTROPIC GLUTAMATE; RHODOPSIN; SEQUENCE HOMOLOGY, AMINO ACID; TYROSINE;

EID: 84875972037     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.437780     Document Type: Article

References (35)

1. Vroling, B., Sanders, M., Baakman, C., Borrmann, A., Verhoeven, S., Klomp, J., Oliveira, L., de Vlieg, J., and Vriend, G. (2011) GPCRDB: information system for G protein-coupled receptors. Nucleic Acids Res. 39, D309-319
2. Choe, H. W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauss, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II. Nature 471, 651-655
3. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477, 549-555
4. Okada, T., Fujiyoshi, Y., Silow, M., Navarro, J., Landau, E. M., and Shichida, Y. (2002) Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 99, 5982-5987
5. Angel, T. E., Chance, M. R., and Palczewski, K. (2009) Conserved waters mediate structural and functional activation of family A (rhodopsin-like) Gprotein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 8555-8560
6. Smit, M. J., Vischer, H. F., Bakker, R. A., Jongejan, A., Timmerman, H., Pardo, L., and Leurs, R. (2007) Pharmacogenomic and structural analysis of constitutive g protein-coupled receptor activity. Annu. Rev. Pharmacol. Toxicol. 47, 53-87
7. Yanagawa, M., Yamashita, T., and Shichida, Y. (2009) Activation switch in the transmembrane domain of metabotropic glutamate receptor. Mol. Pharmacol. 76, 201-207
8. Ballesteros, J., and Weinstein, H. (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci. 25, 366-428
9. Kunishima, N., Shimada, Y., Tsuji, Y., Sato, T., Yamamoto, M., Kumasaka, T., Nakanishi, S., Jingami, H., and Morikawa, K. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977
10. Muto, T., Tsuchiya, D., Morikawa, K., and Jingami, H. (2007) Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 3759-3764
11. Huang, S., Cao, J., Jiang, M., Labesse, G., Liu, J., Pin, J. P., and Rondard, P. (2011) Interdomain movements in metabotropic glutamate receptor activation. Proc. Natl. Acad. Sci. U.S.A. 108, 15480-15485
12. Tateyama, M., Abe, H., Nakata, H., Saito, O., and Kubo, Y. (2004) Ligandinduced rearrangement of the dimeric metabotropic glutamate receptor 1α. Nat. Struct. Mol. Biol. 11, 637-642
13. Yanagawa, M., Yamashita, T., and Shichida, Y. (2011) Comparative fluorescence resonance energy transfer analysis of metabotropic glutamate receptors: implications about the dimeric arrangement and rearrangement upon ligand bindings. J. Biol. Chem. 286, 22971-22981
14. Hlavackova, V., Zabel, U., Frankova, D., Bátz, J., Hoffmann, C., Prezeau, L., Pin, J. P., Blahos, J., and Lohse, M. J. (2012) Sequential inter- and intrasubunit rearrangements during activation of dimeric metabotropic glutamate receptor 1. Sci. Signal. 5, ra59
15. Rizzo, M. A., Springer, G. H., Granada, B., and Piston, D. W. (2004) An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449
16. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90
17. Niwa, H., Yamamura, K., and Miyazaki, J. (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199
18. Yamashita, T., Terakita, A., Kai, T., and Shichida, Y. (2008) Conformational change of the transmembrane helices II and IV of metabotropic glutamate receptor involved in G protein activation. J. Neurochem. 106, 850-859
19. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5.6
20. Okada, T., Sugihara, M., Bondar, A. N., Elstner, M., Entel, P., and Buss, V. (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure. J. Mol. Biol. 342, 571-583
21. Malherbe, P., Kratochwil, N., Knoflach, F., Zenner, M. T., Kew, J. N., Kratzeisen, C., Maerki, H. P., Adam, G., and Mutel, V. (2003) Mutational analysis and molecular modeling of the allosteric binding site of a novel, selective, noncompetitive antagonist of the metabotropic glutamate 1 receptor. J. Biol. Chem. 278, 8340-8347
22. Malherbe, P., Kratochwil, N., Zenner, M. T., Piussi, J., Diener, C., Kratzeisen, C., Fischer, C., and Porter, R. H. (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
23. Petrel, C., Kessler, A., Maslah, F., Dauban, P., Dodd, R. H., Rognan, D., and Ruat, M. (2003) Modeling and mutagenesis of the binding site of Calhex 231, a novel negative allosteric modulator of the extracellular Ca2+-sensing receptor. J. Biol. Chem. 278, 49487-49494
24. Miedlich, S. U., Gama, L., Seuwen, K., Wolf, R. M., and Breitwieser, G. E. (2004) Homology modeling of the transmembrane domain of the human calcium sensing receptor and localization of an allosteric binding site. J. Biol. Chem. 279, 7254-7263
25. Bruno, A., Costantino, G., de Fabritiis, G., Pastor, M., and Selent, J. (2012) Membrane-sensitive conformational states of helix 8 in the metabotropic Glu2 receptor, a class C GPCR. PLoS One 7, e42023
26. Grell, L., Parkin, C., Slatest, L., and Craig, P. A. (2006) EZ-Viz, a tool for simplifying molecular viewing in PyMOL. Biochem. Mol. Biol. Educ. 34, 402-407
27. Pin, J. P., Galvez, T., and Prézeau, L. (2003) Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol. Ther. 98, 325-354
28. Binet, V., Duthey, B., Lecaillon, J., Vol, C., Quoyer, J., Labesse, G., Pin, J. P., and Prézeau, L. (2007) Common structural requirements for heptahelical domain function in class A and class C G protein-coupled receptors. J. Biol. Chem. 282, 12154-12163
29. Kobilka, B. K., and Deupi, X. (2007) Conformational complexity of G-protein- coupled receptors. Trends Pharmacol. Sci. 28, 397-406
30. Deupi, X., and Kobilka, B. K. (2010) Energy landscapes as a tool to integrate GPCR structure, dynamics, and function. Physiology 25, 293-303
31. Govaerts, C., Lefort, A., Costagliola, S., Wodak, S. J., Ballesteros, J. A., Van Sande, J., Pardo, L., and Vassart, G. (2001) A conserved Asn in transmembrane helix 7 is an on/off switch in the activation of the thyrotropin receptor. J. Biol. Chem. 276, 22991-22999
32. Urizar, E., Claeysen, S., Deupí, X., Govaerts, C., Costagliola, S., Vassart, G., and Pardo, L. (2005) An activation switch in the rhodopsin family of G protein-coupled receptors: the thyrotropin receptor. J. Biol. Chem. 280, 17135-17141
33. Deupi, X., Edwards, P., Singhal, A., Nickle, B., Oprian, D., Schertler, G., and Standfuss, J. (2012) StabilizedGprotein binding site in the structure of constitutively active metarhodopsin-II. Proc. Natl. Acad. Sci. U.S.A. 109, 119-124
34. Khelashvili, G., Dorff, K., Shan, J., Camacho-Artacho, M., Skrabanek, L., Vroling, B., Bouvier, M., Devi, L. A., George, S. R., Javitch, J. A., Lohse, M. J., Milligan, G., Neubig, R. R., Palczewski, K., Parmentier, M., Pin, J. P., Vriend, G., Campagne, F., and Filizola, M. (2010) GPCR-OKB: the G protein-coupled receptor oligomer knowledge base. Bioinformatics 26, 1804-1805
35. Urwyler, S. (2011) Allosteric modulation of family C G-protein-coupled receptors: from molecular insights to therapeutic perspectives. Pharmacol. Rev. 63, 59-126