Effect of ACEA-a selective cannabinoid CB1 receptor agonist on the protective action of different antiepileptic drugs in the mouse pentylenetetrazole-induced seizure model

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 39, Issue 2, 2012, Pages 301-309

  Andres Mach, Marta ^a   Zolkowska, Dorota ^b   Barcicka Klosowska, Beata ^c   Haratym Maj, Agnieszka ^a   Florek Luszczki, Magdalena ^a   Luszczki, Jarogniew J ^a,c  

^a INSTITUTE OF AGRICULTURAL MEDICINE   (Poland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEDICAL UNIVERSITY OF LUBLIN   (Poland)

Author keywords

ACEA; Antiepileptic drugs; Cannabinoids; Pentylenetetrazole induced seizures; Pharmacokinetic pharmacodynamic interaction

Indexed keywords

ANTICONVULSIVE AGENT; ARACHIDONYL 2' CHLOROETHYLAMIDE; BENZYLSULFONYL FLUORIDE; CANNABINOID 1 RECEPTOR AGONIST; CLONAZEPAM; ETHOSUXIMIDE; FATTY ACID HYDROLASE; HYDROLASE; PENTETRAZOLE; PHENOBARBITAL; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; CHIMNEY TEST; CLONIC SEIZURE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DEGRADATION; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; DRUG SELECTIVITY; EXPERIMENTAL MODEL; EXPERIMENTAL TEST; GRIP STRENGTH; LONG TERM MEMORY; MALE; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; MUSCLE STRENGTH; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE; PHARMACODYNAMICS; SINGLE DRUG DOSE;

ANIMALS; ANTICONVULSANTS; ARACHIDONIC ACIDS; AVOIDANCE LEARNING; CANNABINOID RECEPTOR AGONISTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HAND STRENGTH; MALE; MICE; MOTOR ACTIVITY; PENTYLENETETRAZOLE; PHENYLMETHYLSULFONYL FLUORIDE; SEIZURES;

EID: 84867019421     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.07.001     Document Type: Article

References (73)

1. Adams I.B., Martin B.R. Cannabis: pharmacology and toxicology in animals and humans. Addiction 1996, 91:1585-1614.
2. Alger B.E. Endocannabinoids and their implications for epilepsy. Epilepsy Curr 2004, 4:169-173.
3. Andres-Mach M., Dudra-Jastrzebska M., Haratym-Maj A., Czerwonka A., Raszewski G., Luszczki J.J. No anticonvulsant effect of the water extract of Scutellariae radix on the anticonvulsant action of valproate, tiagabine and topiramate in two animal models of epilepsy. J Pre-Clin Clin Res 2009, 3:95-98.
4. Bahremand A., Shafaroodi H., Ghasemi M., Nasrabady S.E., Gholizadeh S., Dehpour A.R. The cannabinoid anticonvulsant effect on pentylenetetrazole-induced seizure is potentiated by ultra-low dose naltrexone in mice. Epilepsy Res 2008, 81:44-51.
5. Bahremand A., Nasrabady S.E., Shafaroodi H., Ghasemi M., Dehpour A.R. Involvement of nitrergic system in the anticonvulsant effect of the cannabinoid CB 1 agonist ACEA in the pentylenetetrazole-induced seizure in mice. Epilepsy Res 2009, 84:110-119.
6. Bhaskaran M.D., Smith B.N. Cannabinoid-mediated inhibition of recurrent excitatory circuitry in the dentate gyrus in a mouse model of temporal lobe epilepsy. PLoS One 2010, 5(e10683):1-10.
7. Bidaut-Russell M., Howlett A.C. Cannabinoid receptor-regulated cyclic AMP accumulation in the rat striatum. J Neurochem 1991, 57:1769-1773.
8. Blair R.E., Deshpande L.S., Sombati S., Falenski K.W., Martin B.R., 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 2006, 317:1072-1078.
9. Boissier J.R., Tardy J., Diverres J.C. Une nouvelle methode simple pour explorer l'action tranquilisante: le test de la cheminee. Med Exp (Basel) 1960, 3:81-84.
10. Breivogel C.S., Griffin G., Di Marzo V., Martin B.R. Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Mol Pharmacol 2001, 60:155-163.
11. Brodie M.J., Schachter S.C. Fast facts. Epilepsy 2001, Health Press, Oxford. 2nd ed.
12. Cakil D., Yildirim M., Ayyildiz M., Agar E. The effect of co-administration of the NMDA blocker with agonist and antagonist of CB1-receptor on penicillin-induced epileptiform activity in rats. Epilepsy Res 2011, 93:128-137.
13. Compton D.R., Martin B.R. The effect of the enzyme inhibitor phenylmethylsulfonyl fluoride on the pharmacological effect of anandamide in the mouse model of cannabimimetic activity. J Pharmacol Exp Ther 1997, 283:1138-1143.
14. Consroe P., Martin A., Singh V. Antiepileptic potential of cannabidiol analogs. J Clin Pharmacol 1981, 21(8-9 Suppl.):428S-436S.
15. Coulter D.A., Huguenard J.R., Prince D.A. Characterization of ethosuximide reduction of low-threshold calcium current in thalamic neurons. Ann Neurol 1989, 25:582-593.
16. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 1996, 384:83-87.
17. Czapinski P., Blaszczyk B., Czuczwar S.J. Mechanisms of action of antiepileptic drugs. Curr Top Med Chem 2005, 5:3-14.
18. Deadwyler S.A., Hampson R.E., Bennett B.A., Edwards T.A., Mu J., Pacheco M.A., et al. Cannabinoids modulate potassium current in cultured hippocampal neurons. Receptors Channels 1993, 1:121-134.
19. Deshpande L.S., Blair R.E., Nagarkatti N., Sombati S., Martin B.R., DeLorenzo R.J. Development of pharmacoresistance to benzodiazepines but not cannabinoids in the hippocampal neuronal culture model of status epilepticus. Exp Neurol 2007, 204:705-713.
20. Deshpande L.S., Blair R.E., Ziobro J.M., Sombati S., Martin B.R., DeLorenzo R.J. Endocannabinoids block status epilepticus in cultured hippocampal neurons. Eur J Pharmacol 2007, 558:52-59.
21. Dwivedi C., Harbison R.D. Anticonvulsant activities of delta-8 and delta-9 tetrahydrocannabinol and uridine. Toxicol Appl Pharmacol 1975, 31:452-458.
22. el Sayed M.A., Löscher W., Frey H.H. Pharmacokinetics of ethosuximide in the dog. Arch Int Pharmacodyn Ther 1978, 234:180-192.
23. Falenski K.W., Blair R.E., Sim-Selley L.J., Martin B.R., 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 2007, 146:1232-1244.
24. Gholizadeh S., Shafaroodi H., Ghasemi M., Bahremand A., Sharifzadeh M., Dehpour A.R. Ultra-low dose cannabinoid antagonist AM251 enhances cannabinoid anticonvulsant effects in the pentylenetetrazole-induced seizure in mice. Neuropharmacology 2007, 53:763-770.
25. Giang D.K., Cravatt B.F. Molecular characterization of human and mouse fatty acid amide hydrolases. Proc Natl Acad Sci U S A 1997, 94:2238-2242.
26. Gomora J.C., Daud A.N., Weiergräber M., Perez-Reyes E. Block of cloned human T-type calcium channels by succinimide antiepileptic drugs. Mol Pharmacol 2001, 60:1121-1132.
27. Hájos N., Ledent C., Freund T.F. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 2001, 106:1-4.
28. Howlett A.C. Pharmacology of cannabinoid receptors. Annu Rev Pharmacol Toxicol 1995, 35:607-634.
29. Howlett A.C., Breivogel C.S., Childers S.R., Deadwyler S.A., Hampson R.E., Porrino L.J. Cannabinoid physiology and pharmacology: 30years of progress. Neuropharmacology 2004, 47(Suppl. 1):345-358.
30. Johannessen-Landmark C., Patsalos P.N. Interactions between antiepileptic drugs and herbal medicines. Bol Latinoam Caribe Plant Med Aromaticas 2008, 7:108-118.
31. Karanian D.A., Karim S.L., Wood J.T., Williams J.S., Lin S., Makriyannis A., et al. Endocannabinoid enhancement protects against kainic acid-induced seizures and associated brain damage. J Pharmacol Exp Ther 2007, 322:1059-1066.
32. Karler R., Cely W., Turkanis S.A. The anticonvulsant activity of cannabidiol and cannabiol. Life Sci 1973, 13:1527-1531.
33. Karler R., Cely W., Turkanis S.A. Anticonvulsant properties of delta-9-tetrahydrocannabinol and other cannabinoids. Life Sci 1974, 15:931-947.
34. Kelly K.M., Gross R.A., Macdonald R.L. Valproic acid selectively reduces the low-threshold (T) calcium current in rat nodose neurons. Neurosci Lett 1990, 116:233-238.
35. Ko G.Y., Brown-Croyts L.M., Teyler T.J. The effects of anticonvulsant drugs on NMDA-EPSP, AMPA-EPSP, and GABA-IPSP in the rat hippocampus. Brain Res Bull 1997, 42:297-302.
36. Kozan R., Ayyildiz M., Agar E. The effects of intracerebroventricular AM-251, a CB1-receptor antagonist, and ACEA, a CB1-receptor agonist, on penicillin-induced epileptiform activity in rats. Epilepsia 2009, 50:1760-1767.
37. Kwan P., Brodie M.J. Phenobarbital for the treatment of epilepsy in the 21st century: a critical review. Epilepsia 2004, 45:1141-1149.
38. Leresche N., Parri H.R., Erdemli G., Guyon A., Turner J.P., Williams S.R., et al. On the action of the anti-absence drug ethosuximide in the rat and cat thalamus. J Neurosci 1998, 18:4842-4853.
39. Litchfield J.T., Wilcoxon F. A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 1949, 96:99-113.
40. Löscher W. Basic pharmacology of valproate. CNS Drugs 2002, 10:669-694.
41. Löscher W., Nau H. Distribution of valproic acid and its metabolites in various brain areas of dogs and rats after acute and prolonged treatment. J Pharmacol Exp Ther 1983, 226:845-854.
42. Löscher W., Hönack D., Fassbender C.P., Nolting B. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. III. Pentylenetetrazole seizure models. Epilepsy Res 1991, 8:171-189.
43. Luszczki J.J., Wojcik-Cwikla J., Andres M.M., Czuczwar S.J. Pharmacological and behavioral characteristics of interactions between vigabatrin and conventional antiepileptic drugs in pentylenetetrazole-induced seizures in mice: an isobolographic analysis. Neuropsychopharmacology 2005, 30:958-973.
44. Luszczki J.J., Czuczwar P., Cioczek-Czuczwar A., Czuczwar S.J. Arachidonyl-2'-chloroethylamide, a highly selective cannabinoid CB1 receptor agonist, enhances the anticonvulsant action of valproate in the mouse maximal electroshock-induced seizure model. Eur J Pharmacol 2006, 547:65-74.
45. Luszczki J.J., Antkiewicz-Michaluk L., Czuczwar S.J. Isobolographic analysis of interactions between 1-methyl-1,2,3,4-tetrahydroisoquinoline and four conventional antiepileptic drugs in the mouse maximal electroshock-induced seizure model. Eur J Pharmacol 2009, 602:298-305.
46. Luszczki J.J., Wojda E., Andres-Mach M.M., Cisowski W., Glensk M., Glowniak K., et al. Anticonvulsant and acute neurotoxic effects of imperatorin, osthole and valproate in the maximal electroshock seizure and chimney tests in mice: a comparative study. Epilepsy Res 2009, 85:293-299.
47. Luszczki J.J., Andres-Mach M., Glensk M., Skalicka-Wozniak K. Anticonvulsant effects of four linear furanocoumarins, bergapten, imperatorin, oxypeucedanin, and xanthotoxin, in the mouse maximal electroshock-induced seizure model: a comparative study. Pharmacol Rep 2010, 62:1231-1236.
48. Luszczki J.J., Czuczwar P., Cioczek-Czuczwar A., Dudra-Jastrzebska M., Andres-Mach M., Czuczwar S.J. Effect of arachidonyl-2'-chloroethylamide, a selective cannabinoid CB1 receptor agonist, on the protective action of the various antiepileptic drugs in the mouse maximal electroshock-induced seizure model. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:18-25.
49. Luszczki J.J., Andres-Mach M., Barcicka-Klosowska B., Florek-Luszczki M., Haratym-Maj A., Czuczwar S.J. Effects of WIN 55,212-2 mesylate (a synthetic cannabinoid) on the protective action of clonazepam, ethosuximide, phenobarbital and valproate against pentylenetetrazole-induced clonic seizures in mice. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1870-1876.
50. Luszczki J.J., Misiuta-Krzesinska M., Florek M., Tutka P., Czuczwar S.J. Synthetic cannabinoid WIN 55,212-2 mesylate enhances the protective action of four classical antiepileptic drugs against maximal electroshock-induced seizures in mice. Pharmacol Biochem Behav 2011, 98:261-267.
51. Mackie K., Hille B. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci U S A 1992, 89:3825-3829.
52. Mackie K., Devane W.A., Hille B. Anandamide, an endogenous cannabinoid, inhibits calcium currents as a partial agonist in N18 neuroblastoma cells. Mol Pharmacol 1992, 44:498-503.
53. Mackie K., Lai Y., Westenbroek R., Mitchell R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 1995, 15:6552-6561.
54. Maneuf Y.P., Nash J.E., Crossman A.R., Brotchie J.M. Activation of the cannabinoid receptor by delta 9-tetrahydrocannabinol reduces gamma-aminobutyric acid uptake in the globus pallidus. Eur J Pharmacol 1996, 308:161-164.
55. Mathers D.A., Wan X., Puil E. Barbiturate activation and modulation of GABA(A) receptors in neocortex. Neuropharmacology 2007, 52:1160-1168.
56. McCaughran J.A., Corcoran M.E., Wada J.A. Anticonvulsant activity of delta-8- and delta-9-tetrahydrocannabinol in rats. Pharmacol Biochem Behav 1974, 2:227-233.
57. McLean M.J., Macdonald L. Sodium valproate, but not ethosuximide, produces use- and voltage-dependent limitation of high frequency repetitive firing of action potentials of mouse central neurons in cell culture. J Pharmacol Exp Ther 1986, 237:1001-1011.
58. Meyer O.A., Tilson H.A., Byrd W.C., Riley M.T. A method for the routine assessment of fore- and hindlimb grip strength of rats and mice. Neurobehav Toxicol 1979, 1:233-236.
59. Nieoczym D., Socala K., Luszczki J.J., Czuczwar S.J., Wlaź P. Sildenafil influences the anticonvulsant activity of vigabatrin and gabapentin in the timed pentylenetetrazole infusion test in mice. Prog Neuropsychopharmacol Biol Psychiatry 2012, 10.1016/j.pnpbp. 2012.05.020.
60. Patsalos P.N. Properties of antiepileptic drugs in the treatment of idiopathic generalized epilepsies. Epilepsia 2005, 46(Suppl. 9):140-148.
61. Richardson J.D., Aanonsen L., Hargreaves K.M. Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J Neurosci 1998, 18:451-457.
62. Romigi A., Bari M., Placidi F., Marciani M.G., Malaponti M., Torelli F., et al. Cerebrospinal fluid levels of the endocannabinoid anandamide are reduced in patients with untreated newly diagnosed temporal lobe epilepsy. Epilepsia 2010, 51:768-772.
63. Shafaroodi H., Samini M., Moezi L., Homayoun H., Sadeghipour H., Tavacoli S., et al. The interaction of cannabinoids and opioids on pentylenetetrazole-induced seizure threshold in mice. Neuropharmacology 2004, 47:390-400.
64. Shen M., Thayer S.A. The cannabinoid agonist WIN 55,212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res 1998, 783:77-84.
65. Shen M., Thayer S.A. Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 1999, 55:8-13.
66. Sieradzan K.A., Fox S.H., Hill M., Dick J.P., Crossman A.R., Brotchie J.M. Cannabinoids reduce levodopa-induced dyskinesia in Parkinson's disease: a pilot study. Neurology 2001, 57:2108-2111.
67. Smith P.F. Cannabinoids as potential anti-epileptic drugs. Curr Opin Investig Drugs 2005, 6:680-685.
68. 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.
69. Venault P., Chapouthier G., de Carvalho L.P., Simiand J., Morre M., Dodd R.H., et al. Benzodiazepine impairs and beta-carboline enhances performance in learning and memory tasks. Nature 1986, 321:864-866.
70. Wallace M.J., Wiley J.L., Martin B.R., DeLorenzo R.J. Assessment of the role of CB1 receptors in cannabinoid anticonvulsant effects. Eur J Pharmacol 2001, 428:51-57.
71. Wallace M.J., Martin B.R., DeLorenzo R.J. Evidence for a physiological role of endocannabinoids in the modulation of seizure threshold and severity. Eur J Pharmacol 2002, 452:295-301.
72. Wallace M.J., Blair R.E., Falenski K.W., Martin B.R., DeLorenzo R.J. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther 2003, 307:129-137.
73. Wendt H., Soerensen J., Wotjak C.T., Potschka H. Targeting the endocannabinoid system in the amygdala kindling model of temporal lobe epilepsy in mice. Epilepsia 2011, 52:e62-e65.