G-protein-coupled receptor heteromer dynamics

Journal of Cell Science

Volumn 123, Issue 24, 2010, Pages 4215-4220

  Vilardaga, Jean Pierre ^a,b   Agnati, Luigi F ^c   Fuxe, Kjell ^d   Ciruela, Francisco ^e  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c IRCCS SAN CAMILLO HOSPITAL   (Italy)

^d KAROLINSKA INSTITUTE   (Sweden)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

G protein coupled receptors; Heterodimers; Signaling

Indexed keywords

G PROTEIN COUPLED RECEPTOR; OLIGOMER;

MOLECULAR DYNAMICS; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 78649759744     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.063354     Document Type: Note

References (63)

1. Agnati, L. F., Fuxe, K., Zini, I., Lenzi, P. and Hokfelt, T. (1980). Aspects on receptor regulation and isoreceptor identification. Med. Biol. 58, 182-187.
2. Agnati, L. F., Fuxe, K., Zoli, M., Rondanini, C. and Ogren, S. O. (1982). New vistas on synaptic plasticity: the receptor mosaic hypothesis of the engram. Med Biol. 60, 183-190.
3. Agnati, L. F., Ferre, S., Lluis, S., Franco, R. and Fuxe, K. (2003). Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol. Rev. 55, 509-550.
4. Agnati, L. F., Fuxe, K. and Ferre, S. (2005). How receptor mosaics decode transmitter signals. Possible relevance of cooperativity. Trends Biochem. Sci. 30, 188-193.
5. Agnati, L. F., Guidolin, D., Leo, G. and Fuxe, K. (2007). A boolean network modelling of receptor mosaics relevance of topology and cooperativity. J. Neural. Transm. 114, 77-92.
6. Albizu, L., Cottet, M., Kralikova, M., Stoev, S., Seyer, R., Brabet, I., Roux, T., Bazin, H., Bourrier, E., Lamarque, L. et al. (2010). Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat. Chem. Biol. 6, 587-594.
7. Bourne, H. R. (1997). How receptors talk to trimeric G proteins. Curr. Opin. Cell Biol. 9, 134-142.
8. Bünemann, M., Frank, M. and Lohse, M. J. (2003). Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. USA 100, 16077-16082. (Pubitemid 38021117)
9. Cabello, N., Gandía, J., Bertarelli, D. C., Watanabe, M., Lluís, C., Franco, R., Ferré, S., Luján, R. and Ciruela, F. (2009). Metabotropic glutamate type 5, dopamine D2 and adenosine A2a receptors form higher-order oligomers in living cells. J. Neurochem. 109, 1497-1507.
10. Canals, M., Marcellino, D., Fanelli, F., Ciruela, F., de Benedetti, P., Goldberg, S. R., Neve, K., Fuxe, K., Agnati, L. F., Woods, A. S. et al. (2003). Adenosine A2A-dopamine D2 receptor-receptor heteromerization: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J. Biol. Chem. 278, 46741-46749.
11. Carriba, P., Ortiz, O., Patkar, K., Justinova, Z., Stroik, J., Themann, A., Müller, C., Woods, A. S., Hope, B. T., Ciruela, F. et al. (2007). Striatal adenosine A2A and cannabinoid CB1 receptors form functional heteromeric complexes that mediate the motor effects of cannabinoids. Neuropsychopharmacology 32, 2249-2259.
12. Castro, M., Nikolaev, O. V., Palm, D., Lohse, M. J. and Vilardaga, J.-P. (2005). Turnon switch in parathyroid hormone receptor by a two-step PTH binding mechanism. Proc. Natl. Acad. Sci. USA 102, 16084-16089.
13. Chabre, M. and Le Maire, M. (2005). Monomeric G-protein-coupled receptors as a functional unit. Biochemistry 44, 9395-9403.
14. Chabre, M., Deterre, P. and Antonny, B. (2009). The apparent cooperativity of some GPCRs does not necessarily imply dimerization. Trends Pharmacol Sci. 30, 182-187.
15. Dalrymple, M. B., Pfleger, K. D. G. and Eidne, K. A. (2008). G protein-coupled receptor dimmers: functional consequences, disease states and drug targets. Pharmacol. Ther. 118, 359-371.
16. Dorsch, S., Klotz, K. N., Engelhardt, S., Lohse, M. J. and Bünemann, M. (2009). Analysis of receptor oligomerization by FRAP microscopy. Nat. Methods 6, 225-230.
17. Ferrandon, S., Feinstein, T. N., Castro, C., Bouley, R., Potts, J. T., Gardella, T. J. and Vilardaga, J.-P. (2009). Parathyroid hormone mediates sustained cyclic AMP production by endocytosis of ligand-receptor-G protein complexes. Nat. Chem. Biol. 5, 734-742.
18. Fonseca, J. M. and Lambert, N. A. (2009). Instability of a class A G protein-coupled receptor interface. Mol. Pharmacol. 75, 1296-1299.
19. Fung, J. J., Deupi, X., Pardo, L., Yao, X. J., Velez-Ruiz, G. A., Devree, B. T., Sunahara, R. K. and Kobilka, B. K. (2009). Ligand-specific regulation of beta(2)-adrenoceptors in a model lipid bilayer. EMBO J. 28, 3315-3328.
20. Fuxe, K. and Agnati, L. F. (1985). Receptor-receptor interactions in the central nervous system. A new integrative mechanism in synapses. Med. Res. Rev. 5, 441-482.
21. Fuxe, K., Agnati, L. F., Benfenati, F., Cimmino, M., Algeri, S., Hökfelt, T. and Mutt, V. (1981). Modulation by cholecystokinins of 3H-spiroperidol binding in rat striatum: evidence for increased affinity and reduction in the number of binding sites. Acta Physiol. Scand. 113, 567-569.
22. Fuxe, K., Agnati, L. F., Benfenati, F., Celani, M., Zini, I., Zoli, M. and Mutt, V. (1983). Evidence for the existence of receptor-receptor interactions in the central nervous system. Studies on the regulation of monoamine receptors by neuropeptides. J. Neural. Transm. 18, 165-179.
23. Fuxe, K., von Euler, G., van der Ploeg, I., Fredholm, B. B. and Agnati, L. F. (1989). Pertussis toxin treatment counteracts the cardiovascular effects of neuropeptide Y and clonidine in the awake unrestrained rat. Neurosci. Lett. 101, 337-341.
24. Fuxe, K., Marcellino, D., Genedani, S. and Aganti, L. F. (2007). Adenosine A2A receptors, dopamine D2 receptors and their interactions in Parkinson's disease. Mov. Disord. 22, 1990-2014.
25. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M. and Javitch, J. A. (2008). Dopamine D2 receptor form higher order oligomers at physiological expression levels. EMBO J. 27, 2293-2304.
26. Hanson, M. A. and Stevens, R. C. (2009). Discovery of New GPCR biology - one receptor structure at a time. Structure 17, 8-14.
27. Hein, P., Rochais, F., Hoffmann, C., Dorsch, S., Nikolaev, V. O., Engelhardt, S., Berlot, C. H., Lohse, M. J. and Bünemann, M. (2006). Gs activation is time-limiting in initiating receptor-mediated signaling. J. Biol. Chem. 281, 33345-33351.
28. Hofmann, K. P., Scheerer, P., Hildebrand, P. W., Choe, H. W., Park, J. H., Heck, M. and Ernst, O. P. (2009). A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem. Sci. 34, 540-552.
29. Jordan, B. A., Gomes, C., Rios, J., Filipovska, J. and Devi, L. A. (2003). Functional interaction between μ-opioid and a2A-adrenergic receptors receptors. Mol. Pharmacol. 64, 1317-1324.
30. Kenakin, T. and Miller, L. J. (2010). Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery. Pharmacol. Rev. 62, 265-304.
31. Kuszak, A. J., Pitchiaya, S., Anand, J. P., Mosberg, H. I., Walter, N. G. and Sunahara, R. K. (2008). Purification and functional reconstitution of monomeric μ-opioid receptors: allosteric modulation of agonist binding by Gi2. J. Biol. Chem. 284, 26732-26741.
32. Lamb, T. (1996). Gain and kinetics of activation in the G-protein cascade of phototransduction. Proc. Natl. Acad. Sci. USA 93, 566-570.
33. Limbird, L. E., Meyts, P. D. and Lefkowitz, R. J. (1975). Beta-adrenergic receptors: evidence for negative cooperativity. Biochem. Biophys. Res. Commun. 64, 1160-1168.
34. Lohse, M. J., Nikolaev, N. O., Hein, P., Hoffmann, C., Vilardaga, J.-P. and Bünemann, M. (2008). Optical techniques to analyze real-time activation and signaling of Gprotein-coupled receptors. Trends Pharmacol. Sci. 29, 159-165.
35. Maier-Peuschel, M., Frolich, N., Dees, C., Hommers, L. G., Hoffmann, C., Nikolaev, V. O. and Lohse, M. J. (2010). A FRET-based M2 muscarinic receptor sensor reveals rapid kinetics of allosteric modulation. J. Biol. Chem. 285, 8793-8800.
36. B receptorsthe first 7TM heterodimers. Trends Pharmacol. Sci. 20, 396-399.
37. Milligan, G. (2009). G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br. J. Pharmacol. 158, 5-14.
38. Mueller, K. L., Hoon, M. A., Erlenbach, I., Chandrashekar, J., Zuker, C. S. and Ryba, N. J. P. (2005). The receptors and coding for bitter taste. Nature 434, 225-229.
39. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J. P. and Zuker, C. S. (2001). Mammalian sweet taste receptors. Cell 106, 381-390.
40. 2A-adrenergic receptor and Gi-protein heterotrimer. J. Biol. Chem. 281, 24506-24511.
41. Pierce, K. L., Premont, R. T. and Lefkowitz, R. J. (2002). Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650.
42. Pin, J.-P., Galvez, T. and Prezeau, L. (2003). Evolution, structure and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol. Ther. 98, 325-354.
43. Pin, J.-P., Kniazeff, J., Liu, J., Binet, V., Goudet, C., Rondard, P. and Prezeau, L. (2005). Allosteric functioning of dimeric class C G-protein-coupled receptors. FEBS J. 272, 2947-2955.
44. Prinster, S. C., Hague, C. and Hall, R. A. (2005). Heterodimerization of G protein-coupled receptors: specificity and functional significance. Pharmacol. Rev. 57, 289-298.
45. Ray, K. and Hauschild, B. C. (2000). Cys-140 is critical for metabotropic glutamate receptr-1 (mGlu-1) dimerization. J. Biol. Chem. 275, 34245-34251.
46. 2+ receptor. J. Biol. Chem. 274, 27642-27650.
47. Rivero-Muller, A., Chou, Y. Y., Ji, I., Lajic, S., Hanyaloglu, A. C., Jonas, K., Rahman, N., Ji, T. H. and Huhtaniemi, I. (2010). Rescues of defective G protein-coupled receptor function in vivo by intermolecular cooperation. Proc. Natl. Acad. Sci. USA 107, 2319-2324.
48. Romano, C., Yan, W.-L. and O'Malley, K. L. (1996). Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271, 28612-28616.
49. Rozenfeld, R. and Devi, L. A. (2010). Receptor heteromerization and drug discovery. Trends Pharmacol. Sci. 31, 124-130.
50. Schöneberg, T., Schulz, A., Biebermann, H., Hermsdorf, T., Rompler, H. and Sangkuhl, K. (2004). Mutant G protein-coupled receptord as a cause of human diseases. Pharmacol. Ther. 104, 173-206.
51. Soriano, A., Ventura, R., Molero, A., Hoen, R., Casadó, V., Cortés, A., Fanelli, F., Albericio, F., Lluís, C., Franco, R. et al. (2009). Adenosine A2A receptorantagonist/ dopamine D2 receptor-agonist bivalent ligands as pharmacological tools to detect A2A-D2 receptor heteromers. J. Med. Chem. 52, 5590-5602.
52. Vilardaga, J.-P. (2010). Theme and variations on kinetics of GPCR activation/deactivation. J. Recept. Signal Transduct. Res. 30, 304-312.
53. Vilardaga, J. P., Bünemann, M., Krasel, C., Castro, M. and Lohse, M. J. (2003). Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat. Biotechnol. 21, 807-812.
54. 2A-adrenergic and μ-opioid receptors. Nat. Chem. Biol. 4, 126-131.
55. Vilardaga, J.-P., Bünemann, M., Feinstein, T. N., Lambert, N., Nikolaev, V. O., Engelhardt, S., Lohse, M. J. and Hoffmann, C. (2009). GPCR and G proteins: drug efficacy and activation in live cells. Mol. Endocrinol. 23, 590-599.
56. Vilardaga, J.-P., Romero, G., Friedman, P. A. and Gardella, T. J. (2010). Molecular basis of parathyroid hormone receptor signaling and trafficking: a family B GPCR paradigm. Cell. Mol. Life Sci. Epub ahead of print. PMID: 20703892
57. Waldhoer, M., Fong, J., Jones, R. M., Lunzer, M. M., Sharma, S. K., Kostenis, E., Portoghese, P. S. and Whistler, J. L. (2005). heterodimer- selective agonist shows in vivo relevance of G protein-coupled receptor dimers. Proc. Natl. Acad. Sci. USA 102, 9050-9055.
58. 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. USA 104, 7682-7687.
59. 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.
60. Yang, S. N., Fior, D. R., Hedlund, P. B., Agnati, L. F. and Fuxe, K. (1994). Antagonistic regulation of alpha 2-adrenoceptors by neuropeptide Y receptor subtypes in the nucleus tractus solitarii. Eur. J. Pharmacol. 271, 201-212.
61. Yao, X., Parnot, C., Deupi, X., Ratnala, V. R., Swaminath, G., Farrens, D. and Kobilka, B. (2006). Coupling ligand structure to specific conformational switches in the beta2-adrenoreceptor. Nat. Chem. Biol. 2, 417-422.
62. Zhao, G. Q., Zhang, Y., Hoon, M. A., Chandrashekar, J., Erlenbach, I., Ryba, N. J. P. and Zuker, C. S. (2003). Mammalian sweet taste receptors. Cell 115, 255-266.
63. Zoli, M., Agnati, L. F., Hedlund, P. B., Li, X. M., Ferre, S. and Fuxe, K. (1993). Receptor-receptor interactions as an integrative mechanism in nerve cells. Mol. Neurobiol. 7, 293-334.