Cannabinoid Receptor 1 trafficking and the role of the intracellular pool: Implications for therapeutics

Biochemical Pharmacology

Volumn 80, Issue 7, 2010, Pages 1050-1062

  Grimsey, Natasha L ^a   Graham, E Scott ^a   Dragunow, Mike ^a   Glass, Michelle ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Cannabinoid Receptor CB1; Cell surface receptors; Downregulation; Endocytosis; Protein trafficking

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID; CANNABINOID RECEPTOR; G PROTEIN COUPLED RECEPTOR;

ANIMAL CELL; ARTICLE; CELL LINE; CELL POPULATION; CELL STRAIN HEK293; CELL SURFACE; CHO CELL; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; CELL MEMBRANE; CYTOPLASM; HAMSTER; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; CANNABINOIDS; CELL LINE; CELL MEMBRANE; CRICETINAE; CYTOPLASM; HUMANS; PROTEIN TRANSPORT; RATS; RECEPTORS, CANNABINOID; RECEPTORS, G-PROTEIN-COUPLED;

EID: 77955653663     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.06.007     Document Type: Article

References (58)

1. Fride E., Gobshtis N. Endocannabinoids and their receptors: physiology, pathology and pharmacology. Immunol Endocr Metab Agents Med Chem 2007, 7:157-173.
2. Maccarrone M., Battista N., Centonze D. The endocannabinoid pathway in Huntington's disease: a comparison with other neurodegenerative diseases. Prog Neurobiol 2007, 81:349-379.
3. Nantel F., Bouvier M., Strosberg A.D., Marullo S. Functional effects of long-term activation on human beta 2- and beta 3-adrenoceptor signalling. Br J Pharmacol 1995, 114:1045-1051.
4. Carman C.V., Benovic J.L. G-protein-coupled receptors: turn-ons and turn-offs. Curr Opin Neurobiol 1998, 8:335-344.
5. Cao T.T., Deacon H.W., Reczek D., Bretscher A., von Zastrow M. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2-adrenergic receptor. Nature 1999, 401:286-290.
6. Tanowitz M., von Zastrow M. A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 2003, 278:45978-45986.
7. Vargas G.A., Von Zastrow M. Identification of a novel endocytic recycling signal in the D1 dopamine receptor. J Biol Chem 2004, 279:37461-37469.
8. Hanyaloglu A.C., Zastrow Mv. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu Rev Pharmacol Toxicol 2008, 48:537-568.
9. Katona I., Sperlagh B., Sik A., Kafalvi A., Vizi E.S., Mackie K., et al. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999, 19:4544-4558.
10. Kawamura Y., Fukaya M., Maejima T., Yoshida T., Miura E., Watanabe M., et al. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 2006, 26:2991-3001.
11. Coutts A.A., Anavi-Goffer S., Ross R.A., MacEwan D.J., Mackie K., Pertwee R.G., et al. Agonist-induced internalization and trafficking of cannabinoid CB1 receptors in hippocampal neurons. J Neurosci 2001, 21:2425-2433.
12. Leterrier C., Laine J., Darmon M., Boudin H., Rossier J., Lenkei Z. Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 2006, 26:3141-3153.
13. McDonald N.A., Henstridge C.M., Connolly C.N., Irving A.J. An essential role for constitutive endocytosis, but not activity, in the axonal targeting of the CB1 cannabinoid receptor. Mol Pharmacol 2007, 71:976-984.
14. McIntosh H.H., Song C., Howlett A.C. CB1 cannabinoid receptor: cellular regulation and distribution in N18TG2 neuroblastoma cells. Mol Brain Res 1998, 53:163-173.
15. Graham E.S., Ball N., Scotter E.L., Narayan P., Dragunow M., Glass M. Induction of Krox-24 by endogenous cannabinoid type 1 receptors in Neuro2A cells is mediated by the MEK-ERK MAPK pathway and is suppressed by the phosphatidylinositol 3-kinase pathway. J Biol Chem 2006, 281:29085-29095.
16. Rinaldi-Carmona M., Le Duigou A., Oustric D., Barth F., Bouaboula M., Carayon P., et al. Modulation of CB1 cannabinoid receptor functions after a long-term exposure to agonist or inverse agonist in the Chinese hamster ovary cell expression system. J Pharmacol Exp Ther 1998, 287:1038-1047.
17. Hsieh C., Brown S., Derleth C., Mackie K. Internalization and recycling of the CB1 cannabinoid receptor. J Neurochem 1999, 73:493-501.
18. Leterrier C., Bonnard D., Carrel D., Rossier J., Lenkei Z. Constitutive endocytic cycle of the CB1 cannabinoid receptor. J Biol Chem 2004, 279:36013-36021.
19. Tappe-Theodor A., Agarwal N., Katona I., Rubino T., Martini L., Swiercz J., et al. A molecular basis of analgesic tolerance to cannabinoids. J Neurosci 2007, 27:4165-4177.
20. Wu D.-F., Yang L.-Q., Goschke A., Stumm R., Brandenburg L.-O., Liang Y.-J., et al. Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J Neurochem 2008, 104:1132-1143.
21. Pettit D.A.D., Harrison M.P., Olson J.M., Spencer R.F., Cabral G.A. Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J Neurosci Res 1998, 51:391-402.
22. Tsou K., Brown S., Sañudo-Peña M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998, 83:393-411.
23. Rozenfeld R., Devi L.A. Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 2008, 22:2311-2322.
24. Parent J.L., Labrecque P., Driss Rochdi M., Benovic J.L. Role of the differentially spliced carboxyl terminus in thromboxane A2 receptor trafficking: identification of a distinct motif for tonic internalization. J Biol Chem 2001, 276:7079-7085.
25. Miserey-Lenkei S., Parnot C., Bardin S., Corvol P., Clauser E. Constitutive internalization of constitutively active angiotensin II AT1A receptor mutants is blocked by inverse agonists. J Biol Chem 2002, 277:5891-5901.
26. Marion S., Weiner D.M., Caron M.G. RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J Biol Chem 2004, 279:2945-2954.
27. Sim-Selley L.J. Regulation of cannabinoid CB1 receptors in the central nervous system by chronic cannabinoids. Crit Rev Neurobiol 2003, 15:91-119.
28. Martini L., Waldhoer M., Pusch M., Kharazia V., Fong J., Lee J.H., et al. Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1. FASEB J 2007, 21:802-811.
29. Grimsey N.L., Narayan P.J., Dragunow M., Glass M. A novel high-throughput assay for the quantitative assessment of receptor trafficking. Clin Exp Pharmacol Physiol 2008, 35:1377-1382.
30. Kearn C.S., Blake-Palmer K., Daniel E., Mackie K., Glass M. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk?. Mol Pharmacol 2005, 67:1697-1704.
31. Twitchell W., Brown S., Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 1997, 78:43-50.
32. Jordan J.D., He J.C., Eungdamrong N.J., Gomes I., Ali W., Nguyen T., et al. Cannabinoid receptor-induced neurite outgrowth is mediated by Rap1 activation through Gαo/i-triggered proteasomal degradation of Rap1GAPII. J Biol Chem 2005, 280:11413-11421.
33. Vickery R.G., von Zastrow M. Distinct dynamin-dependent and -independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. J Cell Biol 1999, 144:31-43.
34. Pertwee R.G. Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life Sci 2005, 76:1307-1324.
35. Mollenhauer H.H., James Morré D., Rowe L.D. Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity. Biochim Biophys Acta - Rev Biomembr 1990, 1031:225-246.
36. Mukhopadhyay S., Howlett A.C. CB1 receptor-G protein association. Subtype selectivity is determined by distinct intracellular domains. Eur J Biochem 2001, 268:499-505.
37. Compton S.J., Sandhu S., Wijesuriya S.J., Hollenberg M.D. Glycosylation of human proteinase-activated receptor-2 (hPAR2): role in cell surface expression and signalling. Biochem J 2002, 368:495-505.
38. Ashton C.H. Pharmacology and effects of cannabis: a brief review. Br J Psychiatry 2001, 178:101-106.
39. Raimund M. The impact of lipophilicity in drug research: a case report on β-blockers. Mini Rev Med Chem 2005, 5:197-205.
40. Andersson H., D'Antona A.M., Kendall D.A., Von Heijne G., Chin C.N. Membrane assembly of the cannabinoid receptor 1: impact of a long N-terminal tail. Mol Pharmacol 2003, 64:570-577.
41. Gaborik Z., Hunyady L. Intracellular trafficking of hormone receptors. Trends Endocrinol Metab 2004, 15:286-293.
42. Seachrist J.L., Anborgh P.H., Ferguson S.S.G. β2-Adrenergic receptor internalization, endosomal sorting, and plasma membrane recycling are regulated by Rab GTPases. J Biol Chem 2000, 275:27221-27228.
43. Trapaidze N., Gomes I., Bansinath M., Devi L.A. Recycling and resensitization of delta opioid receptors. DNA Cell Biol 2000, 19:195-204.
44. Volpicelli L.A., Lah J.J., Fang G., Goldenring J.R., Levey A.I. Rab11a and Myosin Vb regulate recycling of the M4 muscarinic acetylcholine receptor. J Neurosci 2002, 22:9776-9784.
45. Hein L., Ishii K., Coughlin S.R., Kobilka B.K. Intracellular targeting and trafficking of thrombin receptors. A novel mechanism for resensitization of a G protein-coupled receptor. J Biol Chem 1994, 269:27719-27726.
46. Rodriguez A., Flemington E.K. Transfection-mediated cell-cycle signaling: considerations for transient transfection-based cell-cycle studies. Anal Biochem 1999, 272:171-181.
47. Tsao P., von Zastrow M. Downregulation of G protein-coupled receptors. Curr Opin Neurobiol 2000, 10:365-369.
48. Gonzalez S., Cebeira M., Fernandez-Ruiz J. Cannabinoid tolerance and dependence: a review of studies in laboratory animals. Pharmacol Biochem Behav 2005, 81:300-318.
49. Sim-Selley L.J., Schechter N.S., Rorrer W.K., Dalton G.D., Hernandez J., Martin B.R., et al. Prolonged recovery rate of CB1 receptor adaptation after cessation of long-term cannabinoid administration. Mol Pharmacol 2006, 70:986-996.
50. Dupre D.J., Robitaille M., Ethier N., Villeneuve L.R., Mamarbachi A.M., Hebert T.E. Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking. J Biol Chem 2006, 281:34561-34573.
51. Bacci A., Huguenard J.R., Prince D.A. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 2004, 431:312-316.
52. Bodor A.L., Katona I., Nyiri G., Mackie K., Ledent C., Hajos N., et al. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 2005, 25:6845-6856.
53. Matyas F., Yanovsky Y., Mackie K., Kelsch W., Misgeld U., Freund T.F. Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 2006, 137:337-361.
54. Waksman Y., Olson J.M., Carlisle S.J., Cabral G.A. The central cannabinoid receptor (CB1) mediates inhibition of nitric oxide production by rat microglial cells. J Pharmacol Exp Ther 1999, 288:1357-1366.
55. Galiegue S., Mary S., Marchand J., Dussossoy D., Carriere D., Carayon P., et al. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 1995, 232:54-61.
56. Petäjä-Repo U.E., Hogue M., Laperriere A., Walker P., Bouvier M. Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human δ opioid receptor. J Biol Chem 2000, 275:13727-13736.
57. Milojevic T., Reiterer V., Stefan E., Korkhov V.M., Dorostkar M.M., Ducza E., et al. The ubiquitin-specific protease Usp4 regulates the cell surface level of the A2A receptor. Mol Pharmacol 2006, 69:1083-1094.
58. Petäjä-Repo U.E., Bouvier M. GPCR folding and maturation: the effect of pharmacological chaperones. The G protein-coupled receptors handbook 2005, 71-93. Humana Press, Totowa. L.A. Devi (Ed.).