Selectivity and evolutionary divergence of metabotropic glutamate receptors for endogenous ligands and G proteins coupled to phospholipase C or TRP channels

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29961-29974

  Kang, Hye Jin ^a   Menlove, Kit ^a   Ma, Jianpeng ^a,b,c   Wilkins, Angela ^a   Lichtarge, Olivier ^a,b   Wensel, Theodore G ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Verna and Marrs McLean Department of Biochemistry and Molecular Biology   (United States)

^c Rice University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; EXPERIMENTS; PROTEINS;

ION CHANNEL; L-GLUTAMATE; METABOTROPIC GLUTAMATE RECEPTORS; MOLECULAR DOCKING; MUTAGENESIS EXPERIMENT; PERTUSSIS TOXIN; PHOSPHOLIPASE C; TRP CHANNELS;

AMINO ACIDS;

ARGININE; ASPARAGINE; BETA ALANINE; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; GLUTAMINE; LYSINE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 6; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8; METABOTROPIC RECEPTOR ANTAGONIST; PHOSPHOLIPASE C; PHOSPHOSERINE; SERINE; TAURINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4 BETA; UNCLASSIFIED DRUG; CALCIUM; GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; PROTEIN SUBUNIT;

AMINO ACID ANALYSIS; ARTICLE; BINDING AFFINITY; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS COUPLING REACTION; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; MUTAGENESIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; RESIDUE ANALYSIS; SIGNAL TRANSDUCTION; STEREOCHEMISTRY; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; DOMINANT GENE; DRUG EFFECTS; HEK293 CELL LINE; MEMBRANE POTENTIAL; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; RAT;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; EVOLUTION, MOLECULAR; GENES, DOMINANT; GLUTAMIC ACID; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; LIGANDS; MEMBRANE POTENTIALS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHOSERINE; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RATS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TYPE C PHOSPHOLIPASES;

EID: 84908191816     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.574483     Document Type: Article

References (48)

1. Conn, P. J., and Pin, J. P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237
2. O'Hara, P. J., Sheppard, P. O., Thøgersen, H., Venezia, D., Haldeman, B. A., McGrane, V., Houamed, K. M., Thomsen, C., Gilbert, T. L., and Mulvihill, E. R. (1993) The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11, 41-52
3. Zhang, Z., Qiu, W., Quinn, S. J., Conigrave, A. D., Brown, E. M., and Bai, M. (2002) Three Adjacent Serines in the Extracellular Domains of the CaR Are Required for L-Amino Acid-mediated Potentiation of Receptor Function. J. Biol. Chem. 277, 33727-33735
4. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J., and Zuker, C. S. (2001) Mammalian sweet taste receptors. Cell 106, 381-390
5. Wilkins, A. D., Venner, E., Marciano, D. C., Erdin, S., Atri, B., Lua, R. C., and Lichtarge, O. (2013) Accounting for epistatic interactions improves the functional analysis of protein structures. Bioinformatics 29, 2714-2721
6. Patneau, D. K., and Mayer, M. L. (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J. Neurosci. 10, 2385-2399
7. Johnson, J. W., and Ascher, P. (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531
8. Conigrave, A. D., Quinn, S. J., and Brown, E. M. (2000) L-amino acid sensing by the extracellular Ca2+-sensing receptor. Proc. Natl. Acad. Sci. U.S.A. 97, 4814-4819
9. Frauli, M., Neuville, P., Vol, C., Pin, J.-P., and Prézeau, L. (2006) Among the twenty classical l-amino acids, only glutamate directly activates metabotropic glutamate receptors. Neuropharmacology 50, 245-253
10. Antflick, J. E., Vetiska, S., Baizer, J. S., Yao, Y., Baker, G. B., and Hampson, D. R. (2009) L-Serine-O-phosphate in the central nervous system. Brain Res. 1300, 1-13
11. Gilliam, J. C., and Wensel, T. G. (2011) TRP channel gene expression in the mouse retina. Vision Res. 51, 2440-2452
12. Davis, I. W., and Baker, D. (2009) RosettaLigand docking with full ligand and receptor flexibility. J. Mol. Biol. 385, 381-392
13. Meiler, J., and Baker, D. (2006) ROSETTALIGAND: Protein-small molecule docking with full side-chain flexibility. Proteins: Structure, Function, and Bioinformatics 65, 538-548
14. Hawkins, P. C. D., Skillman, A. G., Warren, G. L., Ellingson, B. A., and Stahl, M. T. (2010) Conformer Generation with OMEGA: Algorithm and Validation Using High Quality Structures from the Protein Databank and Cambridge Structural Database. J. Chem. Inf. Model. 50, 572-584
15. Mihalek, I., Res, I., and Lichtarge, O. (2004) A family of evolution-entropy hybrid methods for ranking protein residues by importance. J. Mol. Biol. 336, 1265-1282
16. Pei, J., Kim, B. H., and Grishin, N. V. (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 36, 2295-2300
17. Rauw, G. A., Grant, S. L., Labrie, V., Roder, J. C., Antflick, J. E., Hampson, D. R., and Baker, G. B. (2010) Determination of L-serine-O-phosphate in rat and mouse brain tissue using high-performance liquid chromatography and fluorimetric detection. Anal. Biochem. 405, 260-262
18. 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
19. Offermanns, S., and Simon, M. I. (1995) Gα15 and Gα16 couple a wide variety of receptors to phospholipase C. J. Biol. Chem. 270, 15175-15180
20. q/i proteins: characterization of new antagonists. Mol. Pharmacol. 50, 923-930
21. Conklin, B. R., Farfel, Z., Lustig, K. D., Julius, D., and Bourne, H. R. (1993) Substitution of three amino acids switches receptor specificity of Gqα to that of Giα. Nature 363, 274-276
22. Conklin, B. R., Herzmark, P., Ishida, S., Voyno-Yasenetskaya, T. A., Sun, Y., Farfel, Z., and Bourne, H. R. (1996) Carboxyl-terminal mutations of Gq α and Gs α that alter the fidelity of receptor activation. Mol. Pharmacol. 50, 885-890
23. Rodriguez, G. J., Yao, R., Lichtarge, O., and Wensel, T. G. (2010) Evolution-guided discovery and recoding of allosteric pathway specificity determinants in psychoactive bioamine receptors. Proc. Natl. Acad. Sci. U.S.A. 107, 7787-7792
24. Miller, M., Shi, J., Zhu, Y., Kustov, M., Tian, J. B., Stevens, A., Wu, M., Xu, J., Long, S., Yang, P., Zholos, A. V., Salovich, J. M., Weaver, C. D., Hopkins, C. R., Lindsley, C. W., McManus, O., Li, M., and Zhu, M. X. (2011) Identification of ML204, a novel potent antagonist that selectively modulates native TRPC4/C5 ion channels. J. Biol. Chem. 286, 33436-33446
25. Miller, M., Wu, M., Xu, J., Weaver, D., Li, M., and Zhu, M. X. (2011) in TRP Channels (Zhu M. X., ed) pp. 1-20, CRC Press, Inc
26. Trabanco, A. A., Duvey, G., Cid, J. M., Macdonald, G. J., Cluzeau, P., Nhem, V., Furnari, R., Behaj, N., Poulain, G., Finn, T., Lavreysen, H., Poli, S., Raux, A., Thollon, Y., Poirier, N., D'Addona, D., Andrés, J. I., Lutjens, R., Le Poul, E., Imogai, H., and Rocher, J. P. (2011) New positive allosteric modulators of the metabotropic glutamate receptor 2 (mGluR2): identification and synthesis of N-propyl-8-chloro-6-substituted isoquinolones. Bioorg. Med. Chem. Lett. 21, 971-976
27. Jin, X., Semenova, S., Yang, L., Ardecky, R., Sheffler, D. J., Dahl, R., Conn, P. J., Cosford, N. D., and Markou, A. (2010) The mGluR2 positive allosteric modulator BINA decreases cocaine self-administration and cue-induced cocaine-seeking and counteracts cocaine-induced enhancement of brain reward function in rats. Neuropsychopharmacology 35, 2021-2036
28. Schoepp, D. D., Jane, D. E., and Monn, J. A. (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476
29. Okamoto, N., Hori, S., Akazawa, C., Hayashi, Y., Shigemoto, R., Mizuno, N., and Nakanishi, S. (1994) Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J. Biol. Chem. 269, 1231-1236
30. Saugstad, J. A., Kinzie, J. M., Mulvihill, E. R., Segerson, T. P., and Westbrook, G. L. (1994) Cloning and expression of a new member of the L-2-amino-4-phosphonobutyric acid-sensitive class of metabotropic glutamate receptors. Mol. Pharmacol. 45, 367-372
31. Flor, P. J., Van Der Putten, H., Rüegg, D., Lukic, S., Leonhardt, T., Bence, M., Sansig, G., Knöpfel, T., and Kuhn, R. (1997) A novel splice variant of a metabotropic glutamate receptor, human mGluR7b. Neuropharmacology 36, 153-159
32. Masu, M., Tanabe, Y., Tsuchida, K., Shigemoto, R., and Nakanishi, S. (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349, 760-765
33. Aramori, I., and Nakanishi, S. (1992) Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8, 757-765
34. Schaefer, M., Plant, T. D., Obukhov, A. G., Hofmann, T., Gudermann, T., and Schultz, G. (2000) Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275, 17517-17526
35. Jeon, J. P., Roh, S. E., Wie, J., Kim, J., Kim, H., Lee, K. P., Yang, D., Jeon, J. H., Cho, N. H., Kim, I. G., Kang, D. E., Kim, H. J., and So, I. (2013) Activation of TRPC4beta by Galphai subunit increases Ca2+ selectivity and controls neurite morphogenesis in cultured hippocampal neuron. Cell Calcium 54, 307-319
36. Jeon, J. P., Hong, C., Park, E. J., Jeon, J. H., Cho, N. H., Kim, I. G., Choe, H., Muallem, S., Kim, H. J., and So, I. (2012) Selective Gαi subunits as novel direct activators of transient receptor potential canonical (TRPC)4 and TRPC5 channels. J. Biol. Chem. 287, 17029-17039
37. Nicoletti, F., Wroblewski, J. T., Iadarola, M. J., and Costa, E. (1986) Serine-O-phosphate, an endogenous metabolite, inhibits the stimulation of inositol phospholipid hydrolysis elicited by ibotenic acid in rat hippocampal slices. Neuropharmacology 25, 335-338
38. Foster, A. C., Fagg, G. E., Harris, E. W., and Cotman, C. W. (1982) Regulation of glutamate receptors: possible role of phosphatidylserine. Brain Res. 242, 374-377
39. Klunk, W. E., McClure, R. J., and Pettegrew, J. W. (1991) Possible roles of L-phosphoserine in the pathogenesis of Alzheimer's disease. Mol. Chem. Neuropathol. 15, 51-73
40. Kataoka, H., Sakiyama, N., and Makita, M. (1991) Distribution and contents of free O-phosphoamino acids in animal tissues. J. Biochem. 109, 577-580
41. Rosemond, E., Wang, M., Yao, Y., Storjohann, L., Stormann, T., Johnson, E. C., and Hampson, D. R. (2004) Molecular basis for the differential agonist affinities of group III metabotropic glutamate receptors. Mol. Pharmacol. 66, 834-842
42. Hermit, M. B., Greenwood, J. R., and Bräuner-Osborne, H. (2004) Mutation-induced quisqualic acid and ibotenic acid affinity at the metabotropic glutamate receptor subtype 4: ligand selectivity results from a synergy of several amino acid residues. J. Biol. Chem. 279, 34811-34817
43. Wu, H., Wang, C., Gregory, K. J., Han, G. W., Cho, H. P., Xia, Y., Niswender, C. M., Katritch, V., Meiler, J., Cherezov, V., Conn, P. J., and Stevens, R. C. (2014) Structure of a class C GPCR metabotropic glutamate receptor 1 bound to an allosteric modulator. Science 344, 58-64
44. Gomeza, J., Joly, C., Kuhn, R., Knöpfel, T., Bockaert, J., and Pin, J. P. (1996) The second intracellular loop of metabotropic glutamate receptor 1 cooperates with the other intracellular domains to control coupling to G-proteins. J. Biol. Chem. 271, 2199-2205
45. Sawaki, K., Hiramatsu, Y., Baum, B. J., and Ambudkar, I. S. (1993) Involvement of G alpha q/11 in m3-muscarinic receptor stimulation of phosphatidylinositol 4,5 bisphosphate-specific phospholipase C in rat parotid gland membranes. Arch. Biochem. Biophys. 305, 546-550
46. Offermanns, S., Wieland, T., Homann, D., Sandmann, J., Bombien, E., Spicher, K., Schultz, G., and Jakobs, K. H. (1994) Transfected muscarinic acetylcholine receptors selectively couple to Gi-type G proteins and Gq/11. Mol. Pharmacol. 45, 890-898
47. Riccio, A., Li, Y., Tsvetkov, E., Gapon, S., Yao, G. L., Smith, K. S., Engin, E., Rudolph, U., Bolshakov, V. Y., and Clapham, D. E. (2014) Decreased Anxiety-Like Behavior and Gαq/11-Dependent Responses in the Amygdala of Mice Lacking TRPC4 Channels. J. Neurosci. 34, 3653-3667
48. Francesconi, A., and Duvoisin, R. M. (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