Inhibition of NMDA receptor/NO signaling blocked tolerance to the anticonvulsant effect of morphine on pentylenetetrazole-induced seizures in mice

Epilepsy Research

Volumn 91, Issue 1, 2010, Pages 39-48

  Ghasemi, Mehdi ^a   Shafaroodi, Hamed ^b   Nazarbeiki, Saeed ^c   Meskar, Hossein ^c   Ghasemi, Abbas ^a,d   Bahremand, Arash ^a   Ziai, Pouya ^a   Dehpour, Ahmad Reza ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c SHAHED UNIVERSITY   (Iran)

^d IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Morphine; N Methyl d aspartate (NMDA) receptor; Nitric oxide; Opioid tolerance; Seizure

Indexed keywords

DIZOCILPINE; IFENPRODIL; KETAMINE; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PENTETRAZOLE;

ACUTE DRUG ADMINISTRATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICONVULSANT ACTIVITY; ARTICLE; CHRONIC DRUG ADMINISTRATION; CLONIC SEIZURE; CONTROLLED STUDY; DOSE RESPONSE; DRUG ANTAGONISM; LOW DRUG DOSE; MALE; MORPHINE TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEIZURE; SEIZURE THRESHOLD; SWISS WEBSTER MOUSE;

ANIMALS; ANTICONVULSANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; MALE; MICE; MORPHINE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; PENTYLENETETRAZOLE; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; SIGNAL TRANSDUCTION;

EID: 77956011704     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2010.06.010     Document Type: Article

References (75)

1. Abdel-Zaher A.O., Hamdy M.M., Aly S.A., Abdel-Hady R.H., Abdel-Rahman S. Attenuation of morphine tolerance and dependence by aminoguanidine in mice. Eur. J. Pharmacol. 2006, 540:60-66.
2. Ahmed M.M., Arif M., Chikuma T., Kato T. Pentylenetetrazol-induced seizures affect the levels of prolyl oligopeptidase, thimet oligopeptidase and glial proteins in rat brain regions, and attenuation by MK-801 pretreatment. Neurochem. Int. 2005, 47:248-259.
3. Bahremand A., Nasrabady S.E., Shafaroodi H., Ghasemi M., Dehpour A.R. Involvement of nitrergic system in the anticonvulsant effect of the cannabinoid CB1 agonist ACEA in the pentylenetetrazole-induced seizure in mice. Epilepsy Res. 2009, 84:110-119.
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. Bajo M., Crawford E.F., Roberto M., Madamba S.G., Siggins G.R. Chronic morphine treatment alters expression of N-methyl-d-aspartate receptor subunits in the extended amygdala. J. Neurosci. Res. 2006, 83:532-537.
6. Ben-Eliyahu S., Marek P., Vaccarino A.L., Mogil J.S., Sternberg W.F., Liebeskind J.C. The NMDA receptor antagonist MK-801 prevents long-lasting non-associative morphine tolerance in the rat. Brain Res. 1992, 575:304-308.
7. Borris D.J., Bertram E.H., Kapur J. Ketamine controls prolonged status epilepticus. Epilepsy Res. 2000, 42:117-122.
8. Chen L., Huang L.Y.M. Sustained potentiation of NMDA receptor mediated glutamate responses through activation of protein kinase C by a μ-opioid. Neuron 1991, 7:319-326.
9. Croucher M.J., Collins J.F., Meldrum B.S. Anticonvulsant action of excitatory amino acid antagonists. Science 1982, 216:899-901.
10. Dawson T.M., Dawson V.L., Snyder S.H. Nitric oxide as a mediator of neurotoxicity. NIDA Res. Monogr. 1993, 136:258-271. (discussion 271-253).
11. Dawson V.L., Dawson T.M. Nitric oxide in neuronal degeneration. Proc. Soc. Exp. Biol. Med. 1996, 211:33-40.
12. Dawson V.L., Dawson T.M. Nitric oxide neurotoxicity. J. Chem. Neuroanat. 1996, 10:179-190.
13. Dodson W.E. Felbamate in the treatment of Lennox-Gastaut syndrome: results of a 12-month open-label study following a randomized clinical trial. Epilepsia 1993, 34:S18-S24.
14. Elliott K., Minami N., Kolesnikov Y.A., Pasternak G.W., Inturrisi C.E. The NMDA receptor antagonists, LY274614 and MK-801, and the nitric oxide synthase inhibitor, NG-nitro-l-arginine, attenuate analgesic tolerance to the mu-opioid morphine but not to kappa opioids. Pain 1994, 56:69-75.
15. Esplugues J.V. NO as a signalling molecule in the nervous system. Br. J. Pharmacol. 2002, 135:1079-1095.
16. Faught E., Sachdeo R.C., Remler M.P., et al. Felbamate monotherapy for partial-onset seizures: an active-control trial. Neurology 1993, 43:688-692.
17. Fitzgerald L.W., Ortiz J., Hamedani A.G., Nestler E.J. Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents. J. Neurosci. 1996, 16:274-282.
18. Folbergrová J. Anticonvulsant action of both NMDA and non-NMDA receptor antagonists against seizures induced by homocysteine in immature rats. Exp. Neurol. 1997, 145:442-450.
19. Ghasemi M., Montaser-Kouhsari L., Shafaroodi H., Nezami B.G., Ebrahimi F., Dehpour A.R. NMDA receptor/nitrergic system blockage augments antidepressant-like effects of paroxetine in the mouse forced swimming test. Psychopharmacology 2009, 206:325-333.
20. Ghasemi M., Raza M., Dehpour A.R. NMDA receptor antagonists augment antidepressant-like effects of lithium in the mouse forced swimming test. J. Psychopharmacol. 2010, 24:585-594.
21. Gmiro V.E., Serdyuk S.E. Combined blockade of AMPA and NMDA receptors in the brain of rats prevents pentylenetetrazole-induced clonic and tonic-clonic seizures without ataxia. Bull. Exp. Biol. Med. 2008, 145:728-730.
22. Hironaka N., Niki H. Effects of N-methyl-d-aspartate receptor subunit antagonists on regulation of susceptibility to audiogenic seizures in rats. Neurosci. Lett. 2000, 288:139-142.
23. Homayoun H., Khavandgar S., Namiranian K., Gaskari S.A., Dehpour A.R. The role of nitric oxide in anticonvulsant and proconvulsant effects of morphine in mice. Epilepsy Res. 2002, 48:33-41.
24. Honar H., Riazi K., Homayoun H., Demehri S., Dehghani M., Vafaie K., Ebrahimkhani M.R., Rashidi N., Gaskari S.A., Dehpour A.R. Lithium inhibits the modulatory effects of morphine on susceptibility to pentylenetetrazole-induced clonic seizure in mice: involvement of a nitric oxide pathway. Brain Res. 2004, 1029:48-55.
25. Honar H., Riazi K., Homayoun H., Sadeghipour H., Rashidi N., Ebrahimkhani M.R., Mirazi N., Dehpour A.R. Ultra-low dose naltrexone potentiates the anticonvulsant effect of low dose morphine on clonic seizures. Neuroscience 2004, 129:733-742.
26. Inoue M., Mishina M., Ueda H. Locus-specific rescue of GluRepsilon1 NMDA receptors in mutant mice identifies the brain regions important for morphine tolerance and dependence. J. Neurosci. 2003, 23:6529-6536.
27. Inturrisi C.E. NMDA receptors, nitric oxide and opioid tolerance. Regul. Pept. 1994, 54:129-130.
28. Jones A.W., Croucher M.J., Meldrum B.S., Watkins J.C. Suppression of audiogenic seizures in DBA/2 mice by two new dipeptide NMDA receptor antagonists. Neurosci. Lett. 1984, 45:157-161.
29. Khavandgar S., Homayoun H., Dehpour A.R. Mediation of nitric oxide in inhibitory effect of morphine against electroshock-induced convulsions in mice. Pharmacol. Biochem. Behav. 2003, 74:795-801.
30. Kleckner N.W., Glazewski J.C., Chen C.C., Moscrip T.D. Subtypeselective antagonism of N-methyl-d-aspartate receptors by felbamate: insights into the mechanism of action. J. Pharmacol. Exp. Ther. 1999, 289:886-894.
31. Ko S.W., Wu L.J., Shum F., Quan J., Zhuo M. Cingulate NMDA NR2B receptors contribute to morphine-induced analgesic tolerance. Mol. Brain 2008, 1:2-12.
32. Kolesnikov Y.A., Pick C.G., Ciszewska G., Pasternak G.W. Blockade of tolerance to morphine but not to kappa opioids by a nitric oxide synthase inhibitor. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:5162-5166.
33. G-nitro-l-arginine prevents morphine tolerance. Eur. J. Pharmacol. 1992, 221:399-400.
34. Kozela E., Popik P. A complete analysis of NMDA receptor subunits in periaqueductal grey and ventromedial medulla of morphine tolerant mice. Drug Alcohol Depend. 2007, 86:290-293.
35. Krystal A.D., Weiner R.D., Dean M.D., Lindahl V.H., Tramontozzi L.A., Falcone G., Coffey C.E. Comparison of seizure duration, ictal EEG, and cognitive effects of ketamine and methohexital anesthesia with ECT. J. Neuropsychiatry Clin. Neurosci. 2003, 15:27-34.
36. Lauretti G.R., Ahmad I., Pleuvry B.J. The activity of opioid analgesics in seizure models utilizing N-methyl-dl-aspartic acid, kainic acid, bicuculline and pentylenetetrazole. Neuropharmacology 1994, 33:155-160.
37. Leppik I.E., Dreifuss F.E., Pledger G.W., et al. Felbamate for partial seizures: results of a controlled clinical trial. Neurology 1991, 41:1785-1789.
38. Lim G., Wang S., Zeng Q., Sung B., Yang L., Mao J. Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor. J. Neurosci. 2005, 25:11145-11154.
39. 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.
40. Mandhane S.N., Aavula K., Rajamannar T. Timed pentylenetetrazol infusion test: a comparative analysis with s.c.PTZ and MES models of anticonvulsant screening in mice. Seizure 2007, 16:636-644.
41. Marek P., Ben-Eliyahu S., Gold M., Liebeskind J.C. Excitatory amino acid antagonists (kynurenic acid and MK-801) attenuate the development of morphine tolerance in the rat. Brain Res. 1991, 547:77-81.
42. Marek P., Ben-Eliyahu S., Vaccarino A.L., Liebeskind J.C. Delayed application of MK-801 attenuates development of morphine tolerance in rats. Brain Res. 1991, 558:163-165.
43. Mareš P., Mikulecka A. Different effects of two N-methyl-d-aspartate receptor antagonists on seizures, spontaneous behavior, and motor performance in immature rats. Epilepsy Behav. 2009, 14:32-39.
44. Martin G., Nie S., Siggins G.R. μ-Opioid receptors modulate NMDA receptor-mediated responses in nucleus accumbens neurons. J. Neurosci. 1997, 17:11-22.
45. Martin G., Przewlocki R., Siggins G.R. Chronic morphine treatment selectively augments metabotropic glutamate receptor-induced inhibition of N-methyl-d-aspartate receptor-mediated neurotransmission in nucleus accumbens. J. Pharmacol. Exp. Ther. 1999, 288:30-35.
46. Martin G.S., Ahmed S.H., Blank T., Spiess J., Koob G.F., Siggins G.B. Chronic morphine treatment alters NMDA receptor-mediated synaptic transmission in the nucleus accumbens. J. Neurosci. 1999, 19:9081-9089.
47. Massotti M., Sagratella S., Argiolas L., Mele L. Influence of morphine and cyclazocine on the cortical epileptic foci in rabbits. Brain Res. 1984, 310:201-212.
48. Murray F., Harrison N.J., Grimwood S., Bristow L.J., Huston P.H. Nucleus accumbens NMDA receptor subunit expression and function is enhanced in morphine-dependent rats. 2007, 562:191-197.
49. Niaki S.E., Shafaroodi H., Ghasemi M., Shakiba B., Fakhimi A., Dehpour A.R. Mouth breathing increases the pentylenetetrazole-induced seizure threshold in mice: a role for ATP-sensitive potassium channels. Epilepsy Behav. 2008, 13:284-289.
50. Nidhi G., Balakrishnan S., Pandhi P. Role of nitric oxide in electroshock and pentylenetetrazole seizure threshold in rats. Methods Find. Exp. Clin. Pharmacol. 1999, 21:609-612.
51. Osonoe K., Mori N., Suzuki K., Osonoe M. Antiepileptic effects of inhibitors of nitric oxide synthase examined in pentylenetetrazole-induced seizures in rats. Brain Res. 1994, 663:338-340.
52. Pasternak G.W., Inturrisi C. Pharmacological modulation of opioid tolerance. Expert Opin. Investig. Drugs 1995, 4:271-281.
53. Pasternak G.W., Kolesnikov Y. The NMDA/nitric oxide synthase cascade in opioid analgesia and tolerance. Contemporary Clinical Neuroscience: Glutamate and Addiction 2005, 409-416. Humana Press, Totowa, NJ.
54. Przewlocki R., Parsons K.L., Sweeney D.D., Trotter C., Netzeband J.G., Siggins G.R., Gruol D.L. Opioid enhancement of calcium oscillations and burst events involving NMDA receptors and L-type calcium channels in cultured hippocampal neurons. J. Neurosci. 1999, 19:9705-9715.
55. Riazi K., Honar H., Homayoun H., Rashidi N., Kiani S., Ebrahimkhani M.R., Noorian A.R., Ghaffari K., Jannati A., Dehpour A.R. The synergistic anticonvulsant effect of agmatine and morphine: possible role of alpha 2-adrenoceptors. Epilepsy Res. 2005, 65:33-40.
56. Rosenblum A., Marsch L.A., Joseph H., Portenoy R.K. Opioids and the treatment of chronic pain: controversies, current status, and future directions. Exp. Clin. Psychopharmacol. 2008, 16:405-416.
57. Roshanpour M., Ghasemi M., Riazi K., Rafiei-Tabatabaei N., Ghahremani M.H., Dehpour A.R. Tolerance to the anticonvulsant effect of morphine in mice: blockage by ultra-low dose naltrexone. Epilepsy Res. 2009, 83:261-264.
58. Sachdeo R., Kramer L.D., Rosenberg A., Sachdeo S. Felbamate monotherapy: controlled trial in patients with partial onset seizures. Ann. Neurol. 1992, 32:386-392.
59. Sepehrizadeh Z., Sahebgharani M., Ahmadi S., Shapourabadi M.B., Bozchlou S.H., Zarrindast M.R. Morphine-induced behavioral sensitization increased the mRNA expression of NMDA receptor subunits in the rat amygdala. Pharmacology 2008, 81:333-343.
60. Shafaroodi H., Asadi S., Sadeghipour H., Ghasemi M., Ebrahimi F., Tavakoli S., Hajrasouliha A.R., Dehpour A.R. Role of ATP-sensitive potassium channels in the biphasic effects of morphine on pentylenetetrazole-induced seizure threshold in mice. Epilepsy Res. 2007, 75:63-69.
61. Shafaroodi H., Ghasemi M., Dehpour A.R. Elevation of pentylenetetrazole-induced seizure threshold in cholestatic mice: interaction between opioid and cannabinoid systems. J. Gastroenterol. Hepatol. 2008, 23:e251-e257.
62. Snyder S.H. Clinical relevance of opiate receptor and opioid peptide research. Nature 1979, 279:13-14.
63. Stephens D.N. A glutamatergic hypothesis of drug dependence: extrapolations from benzodiazepine receptor ligands. Behav. Pharmacol. 1995, 6:425-446.
64. Trujillo K.A. Are NMDA receptors involved in opiate-induced neural and behavioral plasticity? A review of preclinical studies. Psychopharmacology (Berl.) 2000, 151:121-141.
65. Trujillo K.A., Akil H. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 1991, 251:85-87.
66. Tso P.H., Wong Y.H. Molecular basis of opioid dependence: role of signal regulation by G-proteins. Clin. Exp. Pharmacol. Physiol. 2003, 30:307-316.
67. Tsuda M., Suzuki T., Misawa M. Aggravation of DMCM-induced seizure by nitric oxide synthase inhibitors in mice. Life Sci. 1997, 60:PL339-PL343.
68. Velisek L., Veliskova J., Ptachewich Y., Shinnar S., Moshe S.L. Effects of MK-801 and phenytoin on flurothyl-induced seizures during development. Epilepsia 1995, 36:179-185.
69. Wikler A., Altschul S. Effects of methadone and morphine on the electroencephalogram of the dog. J. Pharmacol. Exp. Ther. 1950, 98:437-446.
70. Yajima Y., Narita M., Takahashi-Nakano Y., Misawa M., Nagase H., Mizoguchi H., Tseng L.F., Suzuki T. Effects of differential modulation of mu-, delta- and kappa-opioid systems on bicuculline-induced convulsions in the mouse. Brain Res. 2000, 862:120-126.
71. Yokoyama H., Mori N., Osone K., Kasai N., Hiramatsu M., Yoshimura T., Matsue T., Uchida I., Kobayashi N., Tsuchihashi N. Increase of central nitric oxide during pentylenetetrazole-induced seizures in rats. Psychiatry Clin. Neurosci. 1995, 49:S277-S279.
72. Yu L., Xue F.S., Li C.W., Xu Y.C., Zhang G.H., Liu K.P., Liu Y., Sun H.T. N(omega)-nitro-l-arginine methyl ester inhibits the up-regulated expression of neuronal nitric oxide synthase/NMDA receptor in the morphine analgesia tolerance rats. Sheng Li Xue Bao 2006, 58:593-598.
73. Zhang H.N., Ko M.C. Seizure activity involved in the up-regulation of BDNF mRNA expression by activation of central mu opioid receptors. Neuroscience 2009, 161:301-310.
74. Zhu H., Jang C.G., Ma T., Oh S., Rockhold R.W., Ho I.K. Region specific expression of NMDA receptor NR1 subunit mRNA in hypothalamus and pons following chronic morphine treatment. Eur. J. Pharmacol. 1999, 365:47-54.
75. Zhu H., Brodsky M., Gorman A.L., Inturrisi C.E. Region-specific changes in NMDA receptor mRNA induced by chronic morphine treatment are prevented by the co-administration of the competitive NMDA receptor antagonist LY274614. Brain Res. Mol. Brain Res. 2003, 114:154-162.