Inhibition of brain oxidative stress and inducible nitric oxide synthase expression by thymoquinone attenuates the development of morphine tolerance and dependence in mice

European Journal of Pharmacology

Volumn 702, Issue 1-3, 2013, Pages 62-70

  Abdel Zaher, Ahmed O ^a   Mostafa, Mostafa G ^b   Farghly, Hanan M ^a   Hamdy, Mostafa M ^a   Omran, Ghada A ^a   Al Shaibani, Najlaà K M ^a  

^a Assiut University Faculty of Medicine   (Egypt)

^b ASSIUT UNIVERSITY   (Egypt)

Author keywords

Dependence; Morphine; Thymoquinone; Tolerance

Indexed keywords

ACETYLCYSTEINE; ARGININE; DIZOCILPINE; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MALONALDEHYDE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NALOXONE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; THYMOQUINONE;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HOT PLATE TEST; LATENT PERIOD; MALE; MORPHINE ADDICTION; MORPHINE TOLERANCE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; WITHDRAWAL SYNDROME;

ANIMALS; BENZOQUINONES; BRAIN; DRUG TOLERANCE; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MALE; MALONDIALDEHYDE; MICE; MORPHINE DEPENDENCE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; OXIDATIVE STRESS; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84875275350     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.01.036     Document Type: Article

References (52)

1. A.M. Abdel-Fattah, K. Matsumoto, and H. Watanabe Antinociceptive effects of Nigella sativa oil and its major component, thymoquinone, in mice Eur. J. Pharmacol. 400 2000 89 97
2. A.O. Abdel-Zaher, M.M. Hamdy, S.A. Aly, R.H. Abdel-Hady, and S. Abdel-Rahman Attenuation of morphine tolerance and dependence by aminoguanidine in mice Eur. J. Pharmacol. 540 2006 60 66
3. A.V. Alekseenko, V.A. Kolos, T.V. Vasim, and S.V. Fedorovich Glutamate induces the formation of free radicals in rat brain synaptosomes Biofizika 54 2009 876 880
4. F.Q. Alenzi, S. El-Bolkiny Yel, and M.L. Salem Protective effects of Nigella sativa and thymoquinone against toxicity induced by the anticancer drug cyclophosamide Br. J. Biomed. Sci. 67 2010 20 28
5. S. Aydin, R. Ozaras, H. Uzun, A. Belce, E. Uslu, V. Tahan, T. Altug, E. Dumen, and H. Senturk N-acetylcysteine reduced the effect of ethanol on antioxidant system in rat plasma and brain tissue Tohoku J. Exp. Med. 198 2002 71 77
6. M. Bajo, E.F. Crawford, M. Roberto, S.G. Madamba, and G.R. Siggins Chronic morphine treatment alters expression of N-methyl-d-aspartate receptor subunits in the extended amygdale J. Neurosci. Res. 83 2006 532 537
7. C.F. Brosnan, L. Battistini, C.S. Raine, D.W. Dickson, A. Vall, and S.C. Lee Reactive nitrogen intermediates in human neuropathology. An overview Dev. Neurosci. 16 1994 152 161
8. G.C. Brown, and A. Bal-Price Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria Mol. Neurobiol. 27 2003 325 355
9. A.R. Dehpour, S.S. Sadr, M. Nouroddini, F. Shadan, A. Nourozi, M. Farahani, and M. Sahebgharani Comparison of simultaneous administration of lithium with L-NAME or l-arginine on morphine withdrawal syndrome in mice Hum. Psychopharmacol. 15 2000 87 93
10. A. El-Mahmoudy, H. Matsuyama, M.A. Borgan, Y. Shimizu, M.G. El-Sayed, N. Minamoto, and T. Takewaki Thymoquinone suppresses expression of inducible nitric oxide synthase in rat macrophages Int. Immunopharmacol. 2 2002 1603 1611
11. N. Gilhotra, and D. Dhingra Thymoquinone produced antianxiety-like effects in mice through modulation of GABA and NO levels Pharmacol. Rep. 63 2011 660 669
12. O.W. Grififith Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine Anal. Biochem. Pharmacol. 106 1980 207 212
13. G.R. Guzmán, A. Ortiz-Acevedo, A. Ricardo, L.V. Rojas, and J.A. Lasalde-Dominicci The polarity of lipid-exposed residues contributes to the functional differences between Torpedo and muscle-type nicotinic receptors J. Membr. Biol. 214 2006 131 138
14. G.K. Helal Thymoquinone supplementation ameliorates acute endotoxemia-induced liver dysfunction in rats Pak. J. Pharm. Sci. 23 2010 131 137
15. A. Hervera, R. Negrete, S. Leanez, J.M. Martin-Campos, and O. Pol The spinal cord expression of neuronal and inducible nitric oxide synthase and their contribution in the maintenance of neuropathic pain in mice Pain and Nitric Oxide 12 2010 1 8
16. H. Homayoun, S. Khavandgar, S. Mehr, N. Ejtemaei, K. Namiranian, and A.R. Dehpour The effects of FK506 on the development and expression of morphine tolerance and dependence in mice Behav. Pharmacol. 14 2003 121 127
17. H. Hosseinzadeha, S. Parvardeh, M. Nassiri Asl, H.R. Sadeghnia, and T. Ziaee Effect of thymoquinone and Nigella sativa seeds oil on lipid peroxidation level during global cerebral ischemia-reperfusion injury in rat hippocampus Phytomed. 14 2007 621 627
18. Y.N. Huang, R.Y. Tsai, S.L. Lin, C.C. Chein, C.H. Cherng, C.T. Wu, C.C. Yeh, and C.S. Wong Amitriptyline attenuates astrocyte activation and morphine tolerance in rats: Role of the PSD-95/NR1/nNOS/PKCy signaling pathway Behav. Brain Res 2012
19. M. Ibi, M. Matsumoto, M. Sasaki, T. Nakagawa, M. Katsuyama, K. Iwata, J. Zhang, S. Kaneko, and C. Yabe-Nishimura Involvement of NOX1/NADPH oxidase in morphine-induced analgesia and tolerance J. Neurosci. 31 2011 18094 18103
20. M. Kanter, O. Coskun, and H. Uysal The antioxidative and antihistaminic effect of Nigella sativa and its major constituent, thymoquinone on ethanol-induced gastric mucosal damage Arch. Toxicol. 21 2005 1 8
21. B.C. Kone, T. Kuncewicz, W. Zhang, and Z.Y. Yu Protein interactions with nitric oxide synthases: controlling the right time, the right place and the right amount of nitric oxide Am. J. Physiol. 285 2003 F178 F190
22. C.H. Liu, C.H. Cherng, S.L. Lin, C.C. Yeh, C.T. Wu, Y.H. Tai, and C.S. Wong N-methyl-d-aspartate receptor antagonist MK-801 suppresses glial pro-inflammatory cytokine expression in morphine-tolerant rats Pharmacol. Biochem. Behav. 99 2011 371 380
23. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408
24. P. Lund l-glutamine and l-glutamate: UV-method with glutaminase and glutamate dehydrogenase H.U. Bergmeyer, Methods of Enzymatic Analysis 1986 VCH verlagsgesellschaft Weinheim 357 363
25. M.A. Mansour, O.T. Ginawi, T. El-Hadiyah, A.S. El-Khatib, O.A. Al-Shabanah, and H.A. Al-Sawaf Effects of volatile oil constituents of Nigella sativa on carbon tetrachloride-induced hepatotoxicity in mice: evidence for antioxidant effects of thymoquinone Res. Commun. Mol. Pathol. Pharmacol. 110 2001 239 251
26. K.M. Miranda, M.G. Espey, and D.A. Wink A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide 5 2001 62 71
27. T. Mori, S. Ito, K. Matsubayashi, and T. Sawaguchi Comparison of nitric oxide synthase inhibitors, phospholipase A2 inhibitor and free radical scavengers as attenuators of opioid withdrawal syndrome Behav. Pharmacol. 18 2007 725 729
28. F. Murray, N.J. Harrison, S. Grimwood, L.J. Bristow, and P.H. Hutson Nucleous accumbens NMDA receptor subunit expression and function is enhanced in mophrine-dependent rats Eur. J. Pharmacol. 21 2007 191 197
29. M.N. Nagi, H.A. Almakki, M.M. Sayed-Ahmed, and A.M. Al-Bekairi Thymoquinone supplenmentation reverses acetaminophen-induced oxidative stress, nitric oxide production and energy decline in mice liver Food Chem. Toxicol. 48 2010 2361 2365
30. S. Oguz, M. Kanter, M. Erboga, and C. Erenoglu Protective effects of thymoquinone against cholestatic oxidative stress and hepatic damage after biliary obstruction in rats. J. Mol. M. in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 2012 351 358
31. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358
32. E. Ozdemir, I. Bagcivan, N. Durmus, A. Altun, and S. Gursoy The nitric oxide-cGMp signaling pathway plays a significant role in tolerance to the analgesic effect of morphine Can. J. Physiol. Pharmacol. 89 2011 89 95
33. M. Ozek, Y. Uresin, and M. Güngör Comparison of the effects of specific and nonspecific inhibition of nitric oxide synthase on morphine analgesia, tolerance and dependence in mice Life Sci. 14 2003 1943 1951
34. I. Ozmen, M. Naziroǧlu, H.A. Alici, F. Sahin, M. Cengiz, and I. Eren Spinal morphine administration reduces the fatty acid contents in spinal cord and brain by increasing oxidative stress Neurochem. Res. 32 2007 19 25
35. D.E. Paglia, and W.N. Valentine Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase J. Lab. Clin. Med. 70 1967 158 170
36. S. Penugonda, S. Mare, G. Goldstein, W.A. Banks, and N. Ercal Effects of N-acetylcysteine amide (NACA), anovel thiol antioxidant against glutamate-induced cytotoxicity in neuronal cell line PC12 Brain Res. 21 2005 132 138
37. F.J. Perez-Asensio, O. Hurtado, M.C. Burguete, M.A. Moro, J.B. Salom, I. Lizasoain, G. Torregrosa, J.C. Leza, E. Alborch, J. Castillo, R.G. Knowles, and P. Lorenzo Inhibition of iNOS activity by 1400 W decreases glutamate release and ameliorates stroke outcome after experimental ischemia Neurobiol. Dis. 18 2005 375 384
38. P. Popik, E. Kozela, and W. Danysz Clinically available NMDA receptor antagonists memantine and dextromethorphan reverse existing tolerance to the antinociceptive effects of morphine in mice Naunyn-Schmiedeberg Arch. Pharmacol. 361 2000 425 432
39. A. Romero, L. Hernandez, P. Garcia-Nogales, and M.M. Puig Deletion of the inducible nitric oxide synthase gene reduces peripheral morphine tolerance in a mouse model of chronic inflammation Fundam. Clin. Pharmacol. 24 2010 317 323
40. B.G. Rosser, and G.J. Gores Liver cell necrosis: cellular mechanisms and clinical implications Gastroenterol. 108 1995 252 275
41. M.M. Sayed-Ahmed, A.M. Aleisa, S.S. Al-Rejaie, A.A. Al-Yahya, O.A. Al-Shabanah, M.M. Hafez, and Mn. Nagi Thymoquinone attenuates diethylnitrosamine induction of hepatic carcinogenesis through antioxidant signaling Oxid. Med. Cell. Longevity 3 2010 251 261
42. M.M. Sayed-Ahmed, and M.N. Nagi Thymoquinone supplementation prevents the development of gentamicin-induced acute renal toxicity in rats Clin. Exp. Pharmacol. Physiol. 34 2007 399 405
43. M.J. Sepulveda, L. Hernandez, P. Rada, S. Tucci, and E. Contreras Effect precipitated withdrawal on extracellular glutamate and aspartate in the nucleus accumbens of chronically morphine-treated rats: an in vivo microdialysis study Pharmacol. Biochem. Behav. 60 1998 255 262
44. L.H. Shang, Z.Q. Luo, X.D. Deng, M.J. Wang, F.R. Huang, D.D. Feng, and S.J. Yue Expression of N-methyl-D-aspartate receptor and its effect on nitric oxide production of rat alveolar macrpophages Nitric Oxide 15 2010 327 331
45. T. Song, N. Hatano, K. Sugimoto, M. Horii, F. Yamaguchi, M. Tokuda, Y. Miyamoto, T. Kambe, and Y. Watanabe Nitric oxide prevents phosphorylation of neuronal nitric oxide synthase at serine 1412 by inhibiting the Akt/PKB and CaM-K II signaling pathways Int. J. Mol. Med. 30 2012 15 20
46. E. Uz, O. Bayrak, E. Uz, A. Kaya, R. Bayrak, B. Uz, F.H. Turgut, N. Bavbek, M. Kanbay, and A. Akcay Nigella sativa oil for prevention of chronic cyclosporine nephrotoxicity: an experimental model Am. J. Nephrol. 28 2008 517 522
47. D.B. Vaupel, A.S. Kimes, and E.D. London Further in vivo studies on attenuating morphine withdrawal: isoform-selective nitric oxide synthase inhibitors differ in efficacy Eur. J. Pharmacol. 324 1997 11 20
48. H. Wang, Y. Zhao, X.H. Xiang, H.S. Wang, and W.R. Wu Blockade of ionotropic glutamatergic transmission in the ventral tegmental area attenuates the physical signs of morphine withdrawal in rats Prog. Neuropsychopharmacol. Biol. Psychiatry. 28 2004 1079 1087
49. L. Wang, J.B. Xu, Y. Tian, H.S. Wu, and Y.L. Liu Protective effect of N-acetylcysteine against lipopolysaccharide injury in hepatocytes of neonatal mice Zhonghua Er Ke Za Zhi 45 2007 30 33
50. Z.H. Wen, Y.C. Chang, C.H. Cherng, L.L. Wang, P.L. Tao, and C.S. Wong Increase of intrathecal CSF excitatory amino acids concentration following morphine challenge in morphine-tolerance rats Brain Res. 9 2004 253 259
51. C.S. Yang, P.J. Tsai, N.N. Lin, and J.S. Kuo Elevated extracellular glutamate concentrations increased malondialdehyde production in anesthetized rat brain cortex Neurosci. Lett. 27 1998 33 36
52. J. Zhou, Y. Li, G. Yan, Q. Bu, L. Lv, Y. Yang, J. Zhao, X. Shao, Y. Deng, R. Zhu, Y. Zhao, and X. Cen Protective role of taurine against morphine-induced neurotoxicity in C6 cells via inhibition of oxidative stress Neurotox. Res. 20 2011 334 342