Identification of three residues essential for 5-hydroxytryptamine 2A-metabotropic glutamate 2 (5-HT2A·mGlu2) receptor heteromerization and its psychoactive behavioral function

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44301-44319

  Moreno, José L ^a   Muguruza, Carolina ^b   Umali, Adrienne ^a   Mortillo, Steven ^a   Holloway, Terrell ^a   Pilar Cuéllar, Fuencisla ^a   Mocci, Giuseppe ^a   Seto, Jeremy ^a   Callado, Luis F ^b   Neve, Rachael L ^e   Milligan, Graeme ^d   Sealfon, Stuart C ^a   López Giménez, Juan F ^c,d   Meana, J Javier ^b   Benson, Deanna L ^a   González Maeso, Javier ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c UNIVERSITY OF CANTABRIA   (Spain)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; BINDING ENERGY; LIGANDS; MAMMALS;

FRONTAL CORTEX; G-PROTEIN COUPLED RECEPTORS; HETEROMERIC COMPLEXES; LIGAND BINDING; RECEPTOR COMPLEX; STRUCTURAL ARRANGEMENT; STRUCTURAL EVIDENCE; TRANS-MEMBRANE DOMAINS;

CELL SIGNALING;

ALANINE; METABOTROPIC RECEPTOR 2; SEROTONIN 2A RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA SEQUENCE; FRONTAL CORTEX; HUMAN; HUMAN CELL; HUMAN TISSUE; LIGAND BINDING; MALE; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; SCHIZOPHRENIA; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

MUS; RODENTIA;

EID: 84871760600     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.413161     Document Type: Article

References (63)

1. Pierce, K. L., Premont, R. T., and Lefkowitz, R. J. (2002) Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650
2. Perez, D. M. (2003) The evolutionarily triumphant G-protein-coupled receptor. Mol. Pharmacol. 63, 1202-1205
3. Rosenbaum, D. M., Rasmussen, S. G., and Kobilka, B. K. (2009) The structure and function of G-protein-coupled receptors. Nature 459, 356-363
4. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) 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
5. Whorton, M. R., Jastrzebska, B., Park, P. S., Fotiadis, D., Engel, A., Palczewski, K., and Sunahara, R. K. (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J. Biol. Chem. 283, 4387-4394
6. Lopez-Gimenez, J. F., Canals, M., Pediani, J. D., and Milligan, G. (2007) The α1b-adrenoceptor exists as a higher order oligomer. Effective oligomerization is required for receptor maturation, surface delivery, and function. Mol. Pharmacol. 71, 1015-1029
7. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M., and Javitch, J. A. (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J. 27, 2293-2304
8. 2-adrenoceptors in a model lipid bilayer. EMBO J. 28, 3315-3328
9. Hern, J. A., Baig, A. H., Mashanov, G. I., Birdsall, B., Corrie, J. E., Lazareno, S., Molloy, J. E., and Birdsall, N. J. (2010) Formation and dissociation ofM1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc. Natl. Acad. Sci. U.S.A. 107, 2693-2698
10. Milligan, G. (2009) G protein-coupled receptor hetero-dimerization. Contribution to pharmacology and function. Br. J. Pharmacol. 158, 5-14
11. Prezeau, L., Rives, M. L., Comps-Agrar, L., Maurel, D., Kniazeff, J., and Pin, J. P. (2010) Functional cross-talk between GPCRs: with or without oligomerization. Curr. Opin. Pharmacol. 10, 6-13
12. Carriba, P., Navarro, G., Ciruela, F., Ferré, S., Casadó, V., Agnati, L., Cortés, A., Mallol, J., Fuxe, K., Canela, E. I., Lluís, C., and Franco, R. (2008) Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat. Methods 5, 727-733
13. González-Maeso, J., Ang, R. L., Yuen, T., Chan, P., Weisstaub, N. V., López-Giménez, J. F., Zhou, M., Okawa, Y., Callado, L. F., Milligan, G., Gingrich, J. A., Filizola, M., Meana, J. J., and Sealfon, S. C. (2008) Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature 452, 93-97
14. Vilardaga, J. P., Nikolaev, V. O., Lorenz, K., Ferrandon, S., Zhuang, Z., and Lohse, M. J. (2008) Conformational cross-talk between α2A-adrenergic and μ-opioid receptors controls cell signaling. Nat. Chem. Biol. 4, 126-131
15. Urizar, E., Yano, H., Kolster, R., Galés, C., Lambert, N., and Javitch, J. A. (2011) CODA-RET reveals functional selectivity as a result of GPCR heteromerization. Nat. Chem. Biol. 7, 624-630
16. Fribourg, M., Moreno, J. L., Holloway, T., Provasi, D., Baki, L., Mahajan, R., Park, G., Adney, S. K., Hatcher, C., Eltit, J. M., Ruta, J. D., Albizu, L., Li, Z., Umali, A., Shim, J., Fabiato, A., MacKerell, A. D., Jr., Brezina, V., Sealfon, S. C., Filizola, M., González-Maeso, J., and Logothetis, D. E. (2011) Decoding the signaling of a GPCR heteromeric complex reveals a unifying mechanism of action of antipsychotic drugs. Cell 147, 1011-1023
17. Tsuji, Y., Shimada, Y., Takeshita, T., Kajimura, N., Nomura, S., Sekiyama, N., Otomo, J., Usukura, J., Nakanishi, S., and Jingami, H. (2000) Cryptic dimer interface and domain organization of the extracellular region of metabotropic glutamate receptor subtype 1. J. Biol. Chem. 275, 28144-28151
18. B receptor heterodimerization. Neuron 27, 97-106
19. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K., and Engel, A. (2003) Organization of theGprotein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278, 21655-21662
20. González-Maeso, J., and Sealfon, S. C. (2009) Psychedelics and schizophrenia. Trends Neurosci. 32, 225-232
21. Aghajanian, G. K. (2009) Modeling "psychosis" in vitro by inducing disordered neuronal network activity in cortical brain slices. Psychopharmacology 206, 575-585
22. Gordon, G. W., Berry, G., Liang, X. H., Levine, B., and Herman, B. (1998) Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74, 2702-2713
23. 2 adrenergic G-protein-coupled receptor. Nature 450, 383-387
24. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin. A G protein-coupled receptor. Science 289, 739-745
25. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37, D387-D392
26. 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
27. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific LLc, San Carlos, CA
28. González-Maeso, J., Weisstaub, N. V., Zhou, M., Chan, P., Ivic, L., Ang, R., Lira, A., Bradley-Moore, M., Ge, Y., Zhou, Q., Sealfon, S. C., and Gingrich, J. A. (2007) Hallucinogens recruit specific cortical 5-HT(2A) receptor-mediated signaling pathways to affect behavior. Neuron 53, 439-452
29. Yokoi, M., Kobayashi, K., Manabe, T., Takahashi, T., Sakaguchi, I., Katsuura, G., Shigemoto, R., Ohishi, H., Nomura, S., Nakamura, K., Nakao, K., Katsuki, M., and Nakanishi, S. (1996) Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2. Science 273, 645-647
30. American Psychiatric Association (eds) (1994) Diagnostic and Statistical Manual of Mental Disorders, DSM-IV, 4th Ed., Washington, D. C.
31. García-Sevilla, J. A., Alvaro-Bartolomé, M., Díez-Alarcia, R., Ramos-Miguel, A., Puigdemont, D., Pérez, V., Alvarez, E., and Meana, J. J. (2010) Reduced platelet G protein-coupled receptor kinase 2 in major depressive disorder. Antidepressant treatment-induced up-regulation of GRK2 protein discriminates between responder and nonresponder patients. Eur. Neuropsychopharmacol. 20, 721-730
32. Mortillo, S., Elste, A., Ge, Y., Patil, S. B., Hsiao, K., Huntley, G. W., Davis, R. L., and Benson, D. L. (2012) Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic β1-integrin. J. Comp. Neurol. 520, 2041-2052
33. Kurita, M., Holloway, T., García-Bea, A., Kozlenkov, A., Friedman, A. K., Moreno, J. L., Heshmati, M., Golden, S. A., Kennedy, P. J., Takahashi, N., Dietz, D. M., Mocci, G., Gabilondo, A. M., Hanks, J., Umali, A., Callado, L. F., Gallitano, A. L., Neve, R. L., Shen, L., Buxbaum, J. D., Han, M. H., Nestler, E. J., Meana, J. J., Russo, S. J., and González-Maeso, J. (2012) HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat. Neurosci. 15, 1245-1254
34. Hof, P. R., Young, W. G., Bloom, F. E., Belichenko, P. V., and Celio, M. R. (2000) Comparative Cytoarchitectonic Atlas of the C57BL/6 and 129/Sv Mouse Brains, pp. 129-239, Elsevier Science BV, Amsterdam, The Netherlands
35. González-Maeso, J., Yuen, T., Ebersole, B. J., Wurmbach, E., Lira, A., Zhou, M., Weisstaub, N., Hen, R., Gingrich, J. A., and Sealfon, S. C. (2003) Transcriptome fingerprints distinguish hallucinogenic and nonhallucinogenic 5-hydroxytryptamine 2A receptor agonist effects in mouse somatosensory cortex. J. Neurosci. 23, 8836-8843
36. Vollenweider, F. X., Leenders, K. L., Scharfetter, C., Maguire, P., Stadelmann, O., and Angst, J. (1997) Positron emission tomography and fluorodeoxyglucose studies of metabolic hyperfrontality and psychopathology in the psilocybin model of psychosis. Neuropsychopharmacology 16, 357-372
37. Carhart-Harris, R. L., Erritzoe, D., Williams, T., Stone, J. M., Reed, L. J., Colasanti, A., Tyacke, R. J., Leech, R., Malizia, A. L., Murphy, K., Hobden, P., Evans, J., Feilding, A., Wise, R. G., and Nutt, D. J. (2012) Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin. Proc. Natl. Acad. Sci. U.S.A. 109, 2138-2143
38. Marek, G. J., Wright, R. A., Schoepp, D. D., Monn, J. A., and Aghajanian, G. K. (2000) Physiological antagonism between 5-hydroxytryptamine(2A) and group II metabotropic glutamate receptors in prefrontal cortex. J. Pharmacol. Exp. Ther. 292, 76-87
39. 3H]LY459477 autoradiography. Neuropharmacology,
40. Pin, J. P., Neubig, R., Bouvier, M., Devi, L., Filizola, M., Javitch, J. A., Lohse, M. J., Milligan, G., Palczewski, K., Parmentier, M., and Spedding, M. (2007) 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
41. Ohishi, H., Neki, A., and Mizuno, N. (1998) Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse. An immunohistochemical study with a monoclonal antibody. Neurosci. Res. 30, 65-82
42. Jakab, R. L., and Goldman-Rakic, P. S. (1998) 5-Hydroxytryptamine 2A serotonin receptors in the primate cerebral cortex. Possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc. Natl. Acad. Sci. U.S.A. 95, 735-740
43. Guo, W., Shi, L., Filizola, M., Weinstein, H., and Javitch, J. A. (2005) Cross-talk in G protein-coupled receptors. Changes at the transmembrane homodimer interface determine activation. Proc. Natl. Acad. Sci. U.S.A. 102, 17495-17500
44. Ballesteros, J. A., 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
45. Magalhaes, A. C., Holmes, K. D., Dale, L. B., Comps-Agrar, L., Lee, D., Yadav, P. N., Drysdale, L., Poulter, M. O., Roth, B. L., Pin, J. P., Anisman, H., and Ferguson, S. S. (2010) CRF receptor 1 regulates anxiety behavior via sensitization of 5-HT2 receptor signaling. Nat. Neurosci. 13, 622-629
46. Banning, C., Votteler, J., Hoffmann, D., Koppensteiner, H., Warmer, M., Reimer, R., Kirchhoff, F., Schubert, U., Hauber, J., and Schindler, M. (2010) A flow cytometry-based FRET assay to identify and analyse protein-protein interactions in living cells. PloS ONE 5, e9344
47. Filizola, M., and Weinstein, H. (2005) The structure and dynamics of GPCR oligomers.Anew focus in models of cell-signaling mechanisms and drug design. Curr. Opin. Drug Discov. Devel. 8, 577-584
48. Milligan, G., and Bouvier, M. (2005) Methods to monitor the quaternary structure of G protein-coupled receptors. FEBS J. 272, 2914-2925
49. Rovira, X., Pin, J. P., and Giraldo, J. (2010) The asymmetric/symmetric activation of GPCR dimers as a possible mechanistic rationale for multiple signaling pathways. Trends Pharmacol. Sci. 31, 15-21
50. Moreno, J. L., Holloway, T., Albizu, L., Sealfon, S. C., and González-Maeso, J. (2011) Metabotropic glutamate mGlu2 receptor is necessary for the pharmacological and behavioral effects induced by hallucinogenic 5-HT2A receptor agonists. Neurosci. Lett. 493, 76-79
51. Nestler, E. J., and Hyman, S. E. (2010) Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169
52. Vollenweider, F. X., Vollenweider-Scherpenhuyzen, M. F., Bäbler, A., Vogel, H., and Hell, D. (1998) Psilocybin induces schizophrenia-like psychosis in humans via a serotonin-2 agonist action. Neuroreport 9, 3897-3902
53. Muguruza, C., Moreno, J. L., Umali, A., Callado, L. F., Meana, J. J., and Gonzalez-Maeso, J. (2012) Dysregulated 5-HT2A receptor binding in post-mortem frontal cortex of schizophrenic subjects. Eur. Neuropsychopharmacol., in press
54. Shoichet, B. K., and Kobilka, B. K. (2012) Structure-based drug screening for G-protein-coupled receptors. Trends Pharmacol. Sci. 33, 268-272
55. Salom, D., Lodowski, D. T., Stenkamp, R. E., Le Trong, I., Golczak, M., Jastrzebska, B., Harris, T., Ballesteros, J. A., and Palczewski, K. (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 103, 16123-16128
56. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human β2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
57. Wu, H., Wacker, D., Mileni, M., Katritch, V., Han, G. W., Vardy, E., Liu, W., Thompson, A. A., Huang, X. P., Carroll, F. I., Mascarella, S. W., Westkaemper, R. B., Mosier, P. D., Roth, B. L., Cherezov, V., and Stevens, R. C. (2012) Structure of the human κ-opioid receptor in complex with JDTic. Nature 485, 327-332
58. Wu, B., Chien, E. Y., Mol, C. D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F. C., Hamel, D. J., Kuhn, P., Handel, T. M., Cherezov, V., and Stevens, R. C. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330, 1066-1071
59. Jaakola, V. P., Griffith, M. T., Hanson, M. A., Cherezov, V., Chien, E. Y., Lane, J. R., Ijzerman, A. P., and Stevens, R. C. (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322, 1211-1217
60. Fonseca, J. M., and Lambert, N. A. (2009) Instability of a class a G protein-coupled receptor oligomer interface. Mol. Pharmacol. 75, 1296-1299
61. Maurel, D., Comps-Agrar, L., Brock, C., Rives, M. L., Bourrier, E., Ayoub, M. A., Bazin, H., Tinel, N., Durroux, T., Prézeau, L., Trinquet, E., and Pin, J. P. (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies. Application to GPCR oligomerization. Nat. Methods 5, 561-567
62. Béïque, J. C., Imad, M., Mladenovic, L., Gingrich, J. A., and Andrade, R. (2007) Mechanism of the 5-hydroxytryptamine 2A receptor-mediated facilitation of synaptic activity in prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 104, 9870-9875
63. Celada, P., Puig, M. V., Díaz-Mataix, L., and Artigas, F. (2008) The hallucinogen DOI reduces low-frequency oscillations in rat prefrontal cortex. Reversal by antipsychotic drugs. Biol. Psychiatry 64, 392-400