Physical and functional interaction between CB1 cannabinoid receptors and β2-adrenoceptors

British Journal of Pharmacology

Volumn 160, Issue 3, 2010, Pages 627-642

  Hudson, Brian D ^a   Hébert, Terence E ^b   Kelly, Melanie Em ^a,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Bioluminescence resonance energy transfer; G protein coupled receptor; Trabecular meshwork

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3 (1 METHANESULFONYLAMINO 4 HEXYN 6 YL) 6A,7,10,10A TETRAHYDRO 6,6,9 TRIMETHYL 6H DIBENZO[B,D]PYRAN; BETA 2 ADRENERGIC RECEPTOR; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOPRENALINE; MITOGEN ACTIVATED PROTEIN KINASE; O 2050; UNCLASSIFIED DRUG; WIN 552121; (6AR,10AR)-3-(1-METHANSULFONYLAMINO-4-HEXYN-6-YL)6A,7,10,10A-TETRAHYDRO-6,6,9-TRIMETHYL-6H-DIBENZO(B,D)PYRAN; BETA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; DRONABINOL; PIPERIDINE DERIVATIVE; PYRAN DERIVATIVE; PYRAZOLE DERIVATIVE;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CONTROLLED STUDY; DIMERIZATION; DOSE RESPONSE; EMBRYO; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TRABECULAR MESHWORK; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; CELL LINE; DRUG EFFECTS; ENERGY TRANSFER; METABOLISM;

ADRENERGIC BETA-2 RECEPTOR ANTAGONISTS; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DRONABINOL; ENERGY TRANSFER; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; PIPERIDINES; PYRANS; PYRAZOLES; RECEPTOR CROSS-TALK; RECEPTOR, CANNABINOID, CB1; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION;

EID: 77952648547     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00681.x     Document Type: Article

References (82)

1. Alexander SPH, Mathie A, Peters JA (2009). Guide to Receptors and Channels (GRAC), 4th edn. Br J Pharmacol 158 (Suppl. 1 S1 S254.
2. Angers S, Salahpour A, Joly E, Hilairet S, Chelsky D, Dennis M et al. (2000). Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc Natl Acad Sci USA 97 : 3684 3689.
3. Ayoub MA, Pfleger KD (2009). Recent advances in bioluminescence resonance energy transfer technologies to study GPCR heteromerization. Curr Opin Pharmacol 10 : 44 52.
4. Ayoub MA, Couturier C, Lucas-Meunier E, Angers S, Fossier P, Bouvier M et al. (2002). Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J Biol Chem 277 : 21522 21528.
5. Azzi M, Charest PG, Angers S, Rousseau G, Kohout T, Bouvier M et al. (2003). Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc Natl Acad Sci USA 100 : 11406 11411.
6. Bab I, Zimmer A (2008). Cannabinoid receptors and the regulation of bone mass. Br J Pharmacol 153 : 182 188.
7. Baker JG, Hall IP, Hill SJ (2003). Agonist and inverse agonist actions of beta-blockers at the human beta 2-adrenoceptor provide evidence for agonist-directed signaling. Mol Pharmacol 64 : 1357 1369.
8. Bohn LM (2007). Constitutive trafficking - more than just running in circles? Mol Pharmacol 71 : 957 958.
9. Borthne A (1976). The treatment of glaucoma with propranolol (inderal). A clinical trial. Acta Ophthalmol (Copenh) 54 : 291 300.
10. Breit A, Lagace M, Bouvier M (2004). Hetero-oligomerization between beta2- and beta3-adrenergic receptors generates a beta-adrenergic signaling unit with distinct functional properties. J Biol Chem 279 : 28756 28765.
11. Canals M, Milligan G (2008). Constitutive activity of the cannabinoid CB1 receptor regulates the function of co-expressed mu opioid receptors. J Biol Chem 283 : 11424 11434.
12. Carriba P, Ortiz O, Patkar K, Justinova Z, Stroik J, Themann A 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.
13. Casu MA, Pisu C, Sanna A, Tambaro S, Spada GP, Mongeau R et al. (2005). Effect of delta9-tetrahydrocannabinol on phosphorylated CREB in rat cerebellum: an immunohistochemical study. Brain Res 1048 : 41 47.
14. Cota D (2007). CB1 receptors: emerging evidence for central and peripheral mechanisms that regulate energy balance, metabolism, and cardiovascular health. Diabetes Metab Res Rev 23 : 507 517.
15. Demuth DG, Molleman A (2006). Cannabinoid signalling. Life Sci 78 : 549 563.
16. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G et al. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 : 1946 1949.
17. Dupre DJ, Baragli A, Rebois RV, Ethier N, Hebert TE (2007). Signalling complexes associated with adenylyl cyclase II are assembled during their biosynthesis. Cell Signal 19 : 481 489.
18. Ellis J, Pediani JD, Canals M, Milasta S, Milligan G (2006). Orexin-1 receptor-cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and -independent coordinated alterations of receptor localization and function. J Biol Chem 281 : 38812 38824.
19. Erickson-Lamy KA, Nathanson JA (1992). Epinephrine increases facility of outflow and cyclic AMP content in the human eye in vitro. Invest Ophthalmol Vis Sci 33 : 2672 2678.
20. Ferrer E (2006). Trabecular meshwork as a new target for the treatment of glaucoma. Drug News Perspect 19 : 151 158.
21. Gardiner SM, March JE, Kemp PA, Bennett T (2005). Involvement of CB1-receptors and beta-adrenoceptors in the regional hemodynamic responses to lipopolysaccharide infusion in conscious rats. Am J Physiol Heart Circ Physiol 288 : H2280 H2288.
22. Hashimotodani Y, Ohno-Shosaku T, Kano M (2007). Endocannabinoids and synaptic function in the CNS. Neuroscientist 13 : 127 137.
23. Hebert TE, Moffett S, Morello JP, Loisel TP, Bichet DG, Barret C et al. (1996). A peptide derived from a beta2-adrenergic receptor transmembrane domain inhibits both receptor dimerization and activation. J Biol Chem 271 : 16384 16392.
24. Hepler RS, Frank IR (1971). Marihuana smoking and intraocular pressure. JAMA 217 : 1392.
25. James JR, Oliveira MI, Carmo AM, Iaboni A, Davis SJ (2006). A rigorous experimental framework for detecting protein oligomerization using bioluminescence resonance energy transfer. Nat Methods 3 : 1001 1006.
26. Jampel HD, Lynch MG, Brown RH, Kuhar MJ, De Souza EB (1987a). Beta-adrenergic receptors in human trabecular meshwork. Identification and autoradiographic localization. Invest Ophthalmol Vis Sci 28 : 772 779.
27. Jampel HD, Lynch MG, Brown RH, Kuhar MJ, De Souza EB (1987b). Beta-adrenergic receptors in human trabecular meshwork. identification and autoradiographic localization. Invest Ophthalmol Vis Sci 28 : 772 779.
28. Jarrahian A, Watts VJ, Barker EL (2004). D2 dopamine receptors modulate galpha-subunit coupling of the CB1 cannabinoid receptor. J Pharmacol Exp Ther 308 : 880 886.
29. Kaufman PL, Gabelt B, Tian B, Liu X (1999). Advances in glaucoma diagnosis and therapy for the next millennium: new drugs for trabecular and uveoscleral outflow. Semin Ophthalmol 14 : 130 143.
30. Kearn CS, Blake-Palmer K, Daniel E, Mackie K, Glass M (2005). Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk? Mol Pharmacol 67 : 1697 1704.
31. Kunos G, Jarai Z, Batkai S, Goparaju SK, Ishac EJ, Liu J et al. (2000). Endocannabinoids as cardiovascular modulators. Chem Phys Lipids 108 : 159 168.
32. Lauckner JE, Hille B, Mackie K (2005). The cannabinoid agonist WIN 55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc Natl Acad Sci USA 102 : 19144 19149.
33. Lavoie C, Mercier JF, Salahpour A, Umapathy D, Breit A, Villeneuve LR et al. (2002). Beta 1/beta 2-adrenergic receptor heterodimerization regulates beta 2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem 277 : 35402 35410.
34. Le Foll B, Forget B, Aubin HJ, Goldberg SR (2008). Blocking cannabinoid CB1 receptors for the treatment of nicotine dependence: insights from pre-clinical and clinical studies. Addict Biol 13 : 239 252.
35. Leterrier C, Bonnard D, Carrel D, Rossier J, Lenkei Z (2004). Constitutive endocytic cycle of the CB1 cannabinoid receptor. J Biol Chem 279 : 36013 36021.
36. Mccarty CA, Burmester JK, Mukesh BN, Patchett RB, Wilke RA (2008). Intraocular pressure response to topical beta-blockers associated with an ADRB2 single-nucleotide polymorphism. Arch Ophthalmol 126 : 959 963.
37. Mcgraw DW, Mihlbachler KA, Schwarb MR, Rahman FF, Small KM, Almoosa KF et al. (2006). Airway smooth muscle prostaglandin-EP1 receptors directly modulate beta2-adrenergic receptors within a unique heterodimeric complex. J Clin Invest 116 : 1400 1409.
38. Mcintosh BT, Hudson B, Yegorova S, Jollimore CA, Kelly ME (2007). Agonist-dependent cannabinoid receptor signalling in human trabecular meshwork cells. Br J Pharmacol 152 : 1111 1120.
39. Mackie K (2005). Cannabinoid receptor homo- and heterodimerization. Life Sci 77 : 1667 1673.
40. Mcvey M, Ramsay D, Kellett E, Rees S, Wilson S, Pope AJ et al. (2001). Monitoring receptor oligomerization using time-resolved fluorescence resonance energy transfer and bioluminescence resonance energy transfer. the human delta-opioid receptor displays constitutive oligomerization at the cell surface, which is not regulated by receptor occupancy. J Biol Chem 276 : 14092 14099.
41. Maneuf YP, Brotchie JM (1997). Paradoxical action of the cannabinoid WIN 55,212-2 in stimulated and basal cyclic AMP accumulation in rat globus pallidus slices. Br J Pharmacol 120 : 1397 1398.
42. Marion S, Weiner DM, Caron MG (2004). RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J Biol Chem 279 : 2945 2954.
43. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 : 561 564.
44. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR et al. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50 : 83 90.
45. Mercier JF, Salahpour A, Angers S, Breit A, Bouvier M (2002). Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J Biol Chem 277 : 44925 44931.
46. Miller JW (2004). Tracking G protein-coupled receptor trafficking using odyssey imaging. Li-Cor Bioscience Available at http://www.licor.com/bio/PDF/ Miller-GPCR.pdf (accessed August 2008).
47. Milligan G (2004). G protein-coupled receptor dimerization: function and ligand pharmacology. Mol Pharmacol 66 : 1 7.
48. Milligan G, Smith NJ (2007). Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol Sci 28 : 615 620.
49. Mukhopadhyay P, Batkai S, Rajesh M, Czifra N, Harvey-White J, Hasko G et al. (2007). Pharmacological inhibition of CB1 cannabinoid receptor protects against doxorubicin-induced cardiotoxicity. J Am Coll Cardiol 50 : 528 536.
50. Njie YF, Kumar A, Qiao Z, Zhong L, Song ZH (2006). Noladin ether acts on trabecular meshwork cannabinoid (CB1) receptors to enhance aqueous humor outflow facility. Invest Ophthalmol Vis Sci 47 : 1999 2005.
51. Njie YF, He F, Qiao Z, Song ZH (2008). Aqueous humor outflow effects of 2-arachidonylglycerol. Exp Eye Res 87 : 106 114.
52. Pacher P, Hasko G (2008). Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 153 : 252 262.
53. Pakdeechote P, Dunn WR, Ralevic V (2007). Cannabinoids inhibit noradrenergic and purinergic sympathetic cotransmission in the rat isolated mesenteric arterial bed. Br J Pharmacol 152 : 725 733.
54. Pate DW, Jarvinen K, Urtti A, Mahadevan V, Jarvinen T (1998). Effect of the CB1 receptor antagonist, SR141716A, on cannabinoid-induced ocular hypotension in normotensive rabbits. Life Sci 63 : 2181 2188.
55. Pfeiffer M, Koch T, Schroder H, Laugsch M, Hollt V, Schulz S (2002). Heterodimerization of somatostatin and opioid receptors cross-modulates phosphorylation, internalization, and desensitization. J Biol Chem 277 : 19762 19772.
56. Pfleger KD, Eidne KA (2005). Monitoring the formation of dynamic G-protein-coupled receptor-protein complexes in living cells. Biochem J 385 : 625 637.
57. Ramsay D, Kellett E, Mcvey M, Rees S, Milligan G (2002). Homo- and hetero-oligomeric interactions between G-protein-coupled receptors in living cells monitored by two variants of bioluminescence resonance energy transfer (BRET): hetero-oligomers between receptor subtypes form more efficiently than between less closely related sequences. Biochem J 365 : 429 440.
58. Rios C, Gomes I, Devi LA (2006). Mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol 148 : 387 395.
59. Roy AA, Baragli A, Bernstein LS, Hepler JR, Hebert TE, Chidiac P (2006). RGS2 interacts with gs and adenylyl cyclase in living cells. Cell Signal 18 : 336 348.
60. Schlicker E, Timm J, Zentner J, Gothert M (1997). Cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in the human and guinea-pig hippocampus. Naunyn Schmiedebergs Arch Pharmacol 356 : 583 589.
61. Schultheiss T, Flau K, Kathmann M, Gothert M, Schlicker E (2005). Cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in guinea-pig vessels, but not in rat and mouse aorta. Naunyn Schmiedebergs Arch Pharmacol 372 : 139 146.
62. Shenoy SK, Drake MT, Nelson CD, Houtz DA, Xiao K, Madabushi S et al. (2006). Beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J Biol Chem 281 : 1261 1273.
63. Stamer WD, Golightly SF, Hosohata Y, Ryan EP, Porter AC, Varga E et al. (2001). Cannabinoid CB(1) receptor expression, activation and detection of endogenous ligand in trabecular meshwork and ciliary process tissues. Eur J Pharmacol 431 : 277 286.
64. Straiker AJ, Maguire G, Mackie K, Lindsey J (1999). Localization of cannabinoid CB1 receptors in the human anterior eye and retina. Invest Ophthalmol Vis Sci 40 : 2442 2448.
65. Sunaguchi M, Nishi M, Mizobe T, Kawata M (2003). Real-time imaging of green fluorescent protein-tagged beta 2-adrenergic receptor distribution in living cells. Brain Res 984 : 21 32.
66. Szczesniak AM, Kelly ME, Whynot S, Shek PN, Hung O (2006). Ocular hypotensive effects of an intratracheally delivered liposomal delta9-tetrahydrocannabinol preparation in rats. J Ocul Pharmacol Ther 22 : 160 167.
67. Tam J, Trembovler V, Di Marzo V, Petrosino S, Leo G, Alexandrovich A et al. (2008). The cannabinoid CB1 receptor regulates bone formation by modulating adrenergic signaling. FASEB J 22 : 285 294.
68. Terrillon S, Bouvier M (2004). Roles of G-protein-coupled receptor dimerization. EMBO Rep 5 : 30 34.
69. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 : 393 411.
70. Van Diepen H, Schlicker E, Michel MC (2008). Prejunctional and peripheral effects of the cannabinoid CB(1) receptor inverse agonist rimonabant (SR 141716). Naunyn Schmiedebergs Arch Pharmacol 378 : 345 369.
71. Vasquez C, Lewis DL (1999). The CB1 cannabinoid receptor can sequester G-proteins, making them unavailable to couple to other receptors. J Neurosci 19 : 9271 9280.
72. Vasquez C, Lewis DL (2003). The beta2-adrenergic receptor specifically sequesters gs but signals through both gs and Gi/o in rat sympathetic neurons. Neuroscience 118 : 603 610.
73. Vemuri VK, Janero DR, Makriyannis A (2008). Pharmacotherapeutic targeting of the endocannabinoid signaling system: drugs for obesity and the metabolic syndrome. Physiol Behav 93 : 671 686.
74. Wager-Miller J, Westenbroek R, Mackie K (2002). Dimerization of G protein-coupled receptors: CB1 cannabinoid receptors as an example. Chem Phys Lipids 121 : 83 89.
75. Wanaka A, Kiyama H, Murakami T, Matsumoto M, Kamada T, Malbon CC et al. (1989). Immunocytochemical localization of beta-adrenergic receptors in the rat brain. Brain Res 485 : 125 140.
76. Wang H, Guo Y, Wang D, Kingsley PJ, Marnett LJ, Das SK et al. (2004). Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat Med 10 : 1074 1080.
77. Wax MB, Molinoff PB, Alvarado J, Polansky J (1989). Characterization of beta-adrenergic receptors in cultured human trabecular cells and in human trabecular meshwork. Invest Ophthalmol Vis Sci 30 : 51 57. (Pubitemid 19039879)
78. Woodward DF, Gil DW (2004). The inflow and outflow of anti-glaucoma drugs. Trends Pharmacol Sci 25 : 238 241.
79. Xiao RP, Ji X, Lakatta EG (1995). Functional coupling of the beta 2-adrenoceptor to a pertussis toxin-sensitive G protein in cardiac myocytes. Mol Pharmacol 47 : 322 329.
80. Xie S, Furjanic MA, Ferrara JJ, Mcandrew NR, Ardino EL, Ngondara A et al. (2007). The endocannabinoid system and rimonabant: a new drug with a novel mechanism of action involving cannabinoid CB1 receptor antagonism - or inverse agonism - as potential obesity treatment and other therapeutic use. J Clin Pharm Ther 32 : 209 231.
81. von Zastrow M, Kobilka BK (1992). Ligand-regulated internalization and recycling of human beta 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors. J Biol Chem 267 : 3530 3538.
82. Zhu WZ, Chakir K, Zhang S, Yang D, Lavoie C, Bouvier M et al. (2005). Heterodimerization of beta1- and beta2-adrenergic receptor subtypes optimizes beta-adrenergic modulation of cardiac contractility. Circ Res 97 : 244 251.