Prolonged exposure to WIN55,212-2 causes downregulation of the CB1 receptor and the development of tolerance to its anticonvulsant effects in the hippocampal neuronal culture model of acquired epilepsy

Neuropharmacology

Volumn 57, Issue 3, 2009, Pages 208-218

  Blair, Robert E ^a   Deshpande, Laxmikant S ^a   Sombati, Sompong ^a   Elphick, Maurice R ^b   Martin, Billy R ^a   DeLorenzo, Robert J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cannabinoid; CB1; Culture; Endocannabinoid; Neuronal; Seizure; Tolerance

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID 1 RECEPTOR;

ANIMAL CELL; ANTICONVULSANT ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EXPOSURE; DRUG TOLERANCE; EPILEPSY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANTICONVULSANTS; BENZOXAZINES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MAGNESIUM; MORPHOLINES; NAPHTHALENES; NEURONS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RECEPTOR, CANNABINOID, CB1; TIME FACTORS;

EID: 67650680323     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.06.007     Document Type: Article

References (55)

1. Abood M.E., Rizvi G., Sallapudi N., and McAllister S.D. Activation of the CB1 cannabinoid receptor protects cultured mouse spinal neurons against excitotoxicity. Neurosci. Lett. 309 (2001) 197-201
2. Alger B.E. Not too excited? Thank your endocannabinoids. Neuron 51 (2006) 393-395
3. Bisogno T., and Di Marzo V. Short- and long-term plasticity of the endocannabinoid system in neuropsychiatric and neurological disorders. Pharmacol. Res. 56 (2007) 428-442
4. Blair R.E., Deshpande L.S., Sombati S., Falenski K.W., Martin B.R., and DeLorenzo R.J. Activation of the cannabinoid type-1 receptor mediates the anticonvulsant properties of cannabinoids in the hippocampal neuronal culture models of acquired epilepsy and status epilepticus. J. Pharmacol. Exp. Ther. 317 (2006) 1072-1078
5. Blair R.E., Sombati S., Lawrence D.C., McCay B.D., and DeLorenzo R.J. Epileptogenesis causes acute and chronic increases in GABAA receptor endocytosis that contributes to the induction and maintenance of seizures in the hippocampal culture model of acquired epilepsy. J. Pharmacol. Exp. Ther. 310 (2004) 871-880
6. Breivogel C.S., Childers S.R., Deadwyler S.A., Hampson R.E., Vogt L.J., and Sim-Selley L.J. Chronic delta9-tetrahydrocannabinol treatment produces a time-dependent loss of cannabinoid receptors and cannabinoid receptor-activated G proteins in rat brain. J. Neurochem. 73 (1999) 2447-2459
7. Breivogel C.S., Scates S.M., Beletskaya I.O., Lowery O.B., Aceto M.D., and Martin B.R. The effects of delta9-tetrahydrocannabinol physical dependence on brain cannabinoid receptors. Eur. J. Pharmacol. 459 (2003) 139-150
8. Cao Y., Wilcox K.S., Martin C.E., Rachinsky T.L., Eberwine J., and Dichter M.A. Presence of mRNA for glutamic acid decarboxylase in both excitatory and inhibitory neurons. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 9844-9849
9. Carter D.S., Haider S.N., Blair R.E., Deshpande L.S., Sombati S., and DeLorenzo R.J. Altered calcium/calmodulin kinase II activity changes calcium homeostasis that underlies epileptiform activity in hippocampal neurons in culture. J. Pharmacol. Exp. Ther. 319 (2006) 1021-1031
10. Consroe P. Brain cannabinoid systems as targets for the therapy of neurological disorders. Neurobiol. Dis. 5 (1998) 534-551
11. Consroe P., and Wolkin A. Cannabidiol-antiepileptic drug comparisons and interactions in experimentally induced seizures in rats. J. Pharmacol. Exp. Ther. 201 (1977) 26-32
12. Coutts A.A., Anavi-Goffer S., Ross R.A., MacEwan D.J., Mackie K., Pertwee R.G., and Irving A.J. Agonist-induced internalization and trafficking of cannabinoid CB1 receptors in hippocampal neurons. J. Neurosci. 21 (2001) 2425-2433
13. Deshpande L.S., Blair R.E., Ziobro J.M., Sombati S., Martin B.R., and Delorenzo R.J. Endocannabinoids block status epilepticus in cultured hippocampal neurons. Eur. J. Pharmacol. 558 (2007) 52-59
14. Deshpande L.S., Sombati S., Blair R.E., Carter D.S., Martin B.R., and DeLorenzo R.J. Cannabinoid CB1 receptor antagonists cause status epilepticus-like activity in the hippocampal neuronal culture model of acquired epilepsy. Neurosci. Lett. 411 (2007) 11-16
15. Devane W.A., Dysarz III F.A., Johnson M.R., Melvin L.S., and Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 34 (1988) 605-613
16. Di Marzo V., Melck D., Bisogno T., and De Petrocellis L. Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci. 21 (1998) 521-528
17. Docagne F., Muneton V., Clemente D., Ali C., Loria F., Correa F., Hernangomez M., Mestre L., Vivien D., and Guaza C. Excitotoxicity in a chronic model of multiple sclerosis: neuroprotective effects of cannabinoids through CB1 and CB2 receptor activation. Mol. Cell. Neurosci. 34 (2007) 551-561
18. Egertová M., and Elphick M.R. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J. Comp. Neurol. 422 (2000) 159-171
19. Elphick M.R., and Egertová M. The neurobiology and evolution of cannabinoid signalling. Philos. Trans. R Soc. Lond. B Biol. Sci. 356 (2001) 381-408
20. Falenski K.W., Blair R.E., Sim-Selley L.J., Martin B.R., and DeLorenzo R.J. Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience 146 (2007) 1232-1244
21. Fried P.A., and McIntyre D.C. Electrical and behavioral attenuation of the anti-convulsant properties of delta 9-TNC following chronic administrations. Psychopharmacologia 31 (1973) 215-227
22. Gonzalez S., Cebeira M., and Fernandez-Ruiz J. Cannabinoid tolerance and dependence: a review of studies in laboratory animals. Pharmacol. Biochem. Behav. 81 (2005) 300-318
23. Hanyaloglu A.C., and von Zastrow M. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48 (2008) 537-568
24. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., and Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11 (1991) 563-583
25. Hoch D.B., and Dingledine R. GABAergic neurons in rat hippocampal culture. Brain Res. 390 (1986) 53-64
26. Howlett A.C.,. Pharmacology of cannabinoid receptors. Annu. Rev. Pharmacol. Toxicol. 35 (1995) 607-634
27. Howlett A.C., Breivogel C.S., Childers S.R., Deadwyler S.A., Hampson R.E., and Porrino L.Jm. Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacology 47 Suppl 1 (2004) 345-358
28. Hsieh C., Brown S., Derleth C., and Mackie K. Internalization and recycling of the CB1 cannabinoid receptor. J. Neurochem. 73 (1999) 493-501
29. Karler R., and Turkanis S.A. The cannabinoids as potential antiepileptics. J. Clin. Pharmacol. 21 (1981) 437S-448S
30. Kim S.H., Won S.J., Mao X.O., Jin K., and Greenberg D.A. Molecular mechanisms of cannabinoid protection from neuronal excitotoxicity. Mol. Pharmacol. 69 (2006) 691-696
31. Kouznetsova M., Kelley B., Shen M., and Thayer S.A. Desensitization of cannabinoid-mediated presynaptic inhibition of neurotransmission between rat hippocampal neurons in culture. Mol. Pharmacol. 61 (2002) 477-485
32. Lothman E.W., Bertram E.H., and Stringer J.L. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37 (1991) 1-82
33. Lundberg D.J., Daniel A.R., and Thayer S.A. Delta(9)-tetrahydrocannabinol-induced desensitization of cannabinoid-mediated inhibition of synaptic transmission between hippocampal neurons in culture. Neuropharmacology (2005)
34. Mackie K. Cannabinoid receptors as therapeutic targets. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 101-122
35. Mackie K., and Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J. 8 (2006) E298-E306
36. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutierrez S.O., van der Stelt M., Lopez-Rodriguez M.L., Casanova E., Schutz G., Zieglgansberger W., Di Marzo V., Behl C., and Lutz B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302 (2003) 84-88
37. Martin B.R., Sim-Selley L.J., and Selley D.E. Signaling pathways involved in the development of cannabinoid tolerance. Trends Pharmacol. Sci. 25 (2004) 325-330
38. Martini L., Waldhoer M., Pusch M., Kharazia V., Fong J., Lee J.H., Freissmuth C., and Whistler J.L. Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1. FASEB J. 21 (2007) 802-811
39. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., and Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990) 561-564
40. McKinney D.L., Cassidy M.P., Collier L.M., Martin B.R., Wiley J.L., Selley D.E., and Sim-Selley L.J. Dose-related differences in the regional pattern of cannabinoid receptor adaptation and in vivo tolerance development to delta9-tetrahydrocannabinol. J. Pharmacol. Exp. Ther. 324 (2008) 664-673
41. Mechoulam R., Spatz M., and Shohami E. Endocannabinoids and neuroprotection. Sci. STKE 2002 (2002) RE5
42. Micale V., Mazzola C., and Drago F. Endocannabinoids and neurodegenerative diseases. Pharmacol. Res. 56 (2007) 382-392
43. Monory K., Massa F., Egertová M., Eder M., Blaudzun H., Westenbroek R., Kelsch W., Jacob W., Marsch R., Ekker M., Long J., Rubenstein J.L., Goebbels S., Nave K.A., During M., Klugmann M., Wolfel B., Dodt H.U., Zieglgansberger W., Wotjak C.T., Mackie K., Elphick M.R., Marsicano G., and Lutz B. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51 (2006) 455-466
44. Paquette J.J., Wang H.Y., Bakshi K., and Olmstead M.C. Cannabinoid-induced tolerance is associated with a CB1 receptor G protein coupling switch that is prevented by ultra-low dose rimonabant. Behav. Pharmacol. 18 (2007) 767-776
45. Sim-Selley L.J., and Martin B.R. Effect of chronic administration of R-(+)-[2,3-dihydro-5-methyl-3-[(morpholinyl)methyl]pyrrolo[1,2,3-de]-1,4-b enzoxazinyl]-(1-naphthalenyl)methanone mesylate (WIN55,212-2) or delta(9)-tetrahydrocannabinol on cannabinoid receptor adaptation in mice. J. Pharmacol. Exp. Ther. 303 (2002) 36-44
46. Sim-Selley L.J., Schechter N.S., Rorrer W.K., Dalton G.D., Hernandez J., Martin B.R., and Selley D.E. Prolonged recovery rate of CB1 receptor adaptation after cessation of long-term cannabinoid administration. Mol. Pharmacol. 70 (2006) 986-996
47. Smith P.A., Selley D.E., Sim-Selley L.J., and Welch S.P. Low dose combination of morphine and delta9-tetrahydrocannabinol circumvents antinociceptive tolerance and apparent desensitization of receptors. Eur. J. Pharmacol. 571 (2007) 129-137
48. Sombati S., and DeLorenzo R.J. Recurrent spontaneous seizure activity in hippocampal neuronal networks in culture. J. Neurophysiol. 73 (1995) 1706-1711
49. Tappe-Theodor A., Agarwal N., Katona I., Rubino T., Martini L., Swiercz J., Mackie K., Monyer H., Parolaro D., Whistler J., Kuner T., and Kuner R. A molecular basis of analgesic tolerance to cannabinoids. J. Neurosci. 27 (2007) 4165-4177
50. Wallace M.J., Blair R.E., Falenski K.W., Martin B.R., and DeLorenzo R.J. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J. Pharmacol. Exp. Ther. 307 (2003) 129-137
51. Wallace M.J., Martin B.R., and DeLorenzo R.J. Evidence for a physiological role of endocannabinoids in the modulation of seizure threshold and severity. Eur. J. Pharmacol. 452 (2002) 295-301
52. Wallace M.J., Wiley J.L., Martin B.R., and DeLorenzo R.J. Assessment of the role of CB1 receptors in cannabinoid anticonvulsant effects. Eur. J. Pharmacol. 428 (2001) 51-57
53. Wu D.F., Yang L.Q., Goschke A., Stumm R., Brandenburg L.O., Liang Y.J., Hollt V., and Koch T. Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J. Neurochem. 104 (2008) 1132-1143
54. Zani A., Braida D., Capurro V., and Sala M. Delta9-tetrahydrocannabinol (THC) and AM 404 protect against cerebral ischaemia in gerbils through a mechanism involving cannabinoid and opioid receptors. Br. J. Pharmacol. 152 (2007) 1301-1311
55. Zhuang S.Y., Bridges D., Grigorenko E., McCloud S., Boon A., Hampson R.E., and Deadwyler S.A. Cannabinoids produce neuroprotection by reducing intracellular calcium release from ryanodine-sensitive stores. Neuropharmacology 48 (2005) 1086-1096