The spinal nitric oxide involved in the inhibitory effect of midazolam on morphine-induced analgesia tolerance

Pharmacology Biochemistry and Behavior

Volumn 80, Issue 3, 2005, Pages 493-503

  Cao, Jun Li ^a,b   Ding, Hai Lei ^b   He, Jian Hua ^b   Zhang, Li Cai ^b   Duan, Shi Ming ^b   Zeng, Yin Ming ^a,b  

^a XUZHOU MEDICAL UNIVERSITY   (China)

^b The Key Anesthesiology Laboratory of Jiangsu Province   (China)

Author keywords

Midazolam; Morphine tolerance; Nitric oxide; Spinal cord

Indexed keywords

ARGININE; CYTOCHROME B5 REDUCTASE; FORMALDEHYDE; INDUCIBLE NITRIC OXIDE SYNTHASE; MIDAZOLAM; MORPHINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN FOS;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG TOLERANCE; EXPERIMENTAL MODEL; HISTOCHEMISTRY; HOT PLATE TEST; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; STATISTICAL SIGNIFICANCE; TAIL FLICK TEST; TIME SERIES ANALYSIS; WESTERN BLOTTING;

EID: 14544303137     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2005.01.009     Document Type: Article

References (70)

1. B.H. Bie, and Z.Q. Zhao Nitric oxide inhibits GABA-evoked current in dorsal root ganglion neuron via PKG-dependent pathway Brain Res Bull 55 2001 335 339
2. C.I. Bliss Statistics in biology 1967 McGraw-Hill New York
3. N.I. Boyadjieva, C.P. Chen, and D.K. Sarkar Role of nitric oxide in alcohol alteration of beta-endorphin release from hypothalamic cells in primary cultures Alcohol Clin Exp Res 27 2003 1813 1818
4. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
5. D.S. Bredt, C.E. Glatt, P.M. Hwang, M. Fotuhi, T.M. Dawson, and S.H. Snyder Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase Neuron 7 1991 615 624
6. J.L. Cao, L.C. Zhang, Y.M. Zeng, and S.M. Duan Increased expression of formalin-induced Fos and NADPH-d positive neurons in the spinal cord morphine-tolerant rats Acta Physiol Sin 52 2000 235 238
7. 1AR mRNA expression in the rat spinal cord during morphine withdrawal Acta Pharmacol Sin 22 2001 505 511
8. J.L. Cao, H.L. Ding, L.C. Zhang, S.M. Duan, and Y.M. Zeng Pretreatment with midazolam suppresses morphine withdrawal response in mice and rats Acta Pharm Sinica 23 2002 685 690
9. M. Chacur, E.D. Milligan, L.S. Gazda, C. Armstrong, H. Wang, and K.J. Tracey A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats Pain 94 2001 231 244
10. H.S. Chen, J. Chen, and Y.Y. Sun Contralateral heat hyperalgesia induced by unilaterally intraplantar bee venom injection is produced by central changes: a behavioral study in the conscious rat Neurosci Lett 284 2000 45 48
11. T.M. Dawson, D.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Snyder Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissue Proc Natl Acad Sci U S A 88 1991 7797 7801
12. D. Dubuisson, and S.G. Dennis The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats Pain 4 1977 161 174
13. H.F. Galley, and N.R. Webster Brain nitric oxide synthase activity is decreased by intravenous anesthetics Anesth Analg 83 1996 591 594
14. R. Guevara-Guzman, C.P. Emson, and K.M. Kendrick Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP J Neurochem 62 1994 807 810
15. B. Heinke, R. Ruscheweyh, L. Forsthuber, G. Wunderbaldinger, and J. Sandkuhler Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice J Physiol 560 2004 249 266
16. E.L. Heinzen, and G.M. Pollack The development of morphine antinociceptive tolerance in nitric oxide synthase-deficient mice Biochem Pharmacol 67 2004 735 741
17. B.T. Hope, G.J. Michael, K.M. Knigge, and S.R. Vincent Neuronal NADPH-diaphorase is a nitric oxide synthase Proc Natl Acad Sci U S A 88 1991 2811 2820
18. W.H. Hu, F.C. Lee, X.S.T. Wan, Y.T. Chen, and M.F. Jen Dynorphin neurotoxicity induced nitric oxide synthase expression in ventral horn cells of rat spinal cord Neurosci Lett 203 1996 13 16
19. J.L.K. Hylden, and G.L. Wilcox Intrathecal morphine in mice: a new technique Eur J Pharmacol 67 1980 313 316
20. H.M. Johnston, and B.J. Morris Nitric oxide alters proenkephalin and prodynorphin gene expression in hippocampal granule cells Neuroscience 61 1994 435 439
21. T. Kano, M. Shimizu-Sasamata, P.L. Huang, M.A. Moskowitz, and E.H. Lo Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo Neuroscience 86 1998 695 699
22. S. Kumar, and H.N. Bhargava Time course of the changes in central nitric oxide synthase activity following chronic treatment with morphine in the mouse: reversal by naltrexone Gen Pharmacol 29 1997 223 227
23. I. Laing, A.J. Todd, C.W. Heizmann, and H.H. Schmidt Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin Neuroscience 61 1994 123 132
24. P.Y. Law, H.H. Loh, and L.N. Wei Insights into the receptor transcription andsignaling: implications in opioid tolerance and dependence Neuropharmacology 47 2004 300 311
25. J.H. Lee, R.H. Price, F.G. Williams, B. Mayer, and A.J. Beitz Nitric oxide synthase is found in some spinothalamic neurons and in neuronal processes that appose neurons that express Fos induced by noxious stimulation Brain Res 608 1993 324 333
26. Q. Lin, J. Wu, Y.B. Peng, M. Cui, and W.D. Willis Nitric oxide-mediated spinal disinhibition contributes to the sensitization of primate spinothalamic tract neurons J Neurophysiol 81 1999 1086 1094
27. Q. Lin, J. Wu, Y.B. Peng, M. Cui, and W.D. Willis Inhibition of primate spinothalamic tract neurons by spinal glycine and GABA is modulated by guanosine 3′,5′-cyclic monophosphate J Neurophysiol 81 1999 1095 1103
28. S.A. Lipton, Y.B. Choi, Z.H. Pan, S.Z. Lei, H.S.V. Chen, and N.J. Sucher A redox based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitro compounds Nature 346 1993 626 632
29. G. Lonart, J. Wang, and K.M. Johnson Nitric oxide induces neurotransmitter release from hippocampal slices Eur J Pharmacol 220 1992 271 272
30. H. Machelska, B. Ziolkowska, J. Mika, B. Przewlocka, and R. Przewlocki Chronic morphine increases biosynthesis of nitric oxide synthase in the rat spinal cord Neuroreport 8 1997 2743 2747
31. D.J. Mayer, J. Mao, J. Holt, and D.D. Price Cellular mechanisms of neuropathic pain morphine tolerance and their interactions Proc Natl Acad Sci U S A 96 1999 7731 7736
32. G.P. McNally Pain facilitatory circuits in the mammalian central nervous system: their behavioral significance and role in morphine analgesic tolerance Neurosci Biobehav Rev 23 1999 1059 1078
33. R. Munglani, B.G. Fleming, and S.P. Hunt Remembrance of times past: the significance of c-fos in pain Br J Anaesth 76 1996 1 4
34. A receptor and spinally mediated antinociception in rat J Pharmacol Exp Ther 278 1996 620 626
35. M. Ozek, Y. Uresin, and M. Gungor Comparison of the effects of specific and nonspecific inhibition of nitric oxide synthase on morphine analgesia, tolerance and dependence in mice Life Sci 72 2003 1943 1951
36. R. Radhakrishnan, S.A. Moore, and K.A. Sluka Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats Pain 104 2003 567 577
37. V. Raghavendra, M.D. Rutkowski, and J.A. DeLeo The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats J Neurosci 22 2002 9980 9989
38. N.G. Rainov, V. Heidecke, and W. Burkert Long-term intrathecal infusion of drug combinations for chronic back and leg pain J Pain Symptom Manage 22 2001 862 871
39. A.K. Rattan, and G.A. Tejwani Effect of chronic treatment with morphine, midazolam, and both together on β-endorphin levels in the rat Brain Res Bull 41 1996 335 341
40. A.K. Rattan, and G.A. Tejwani Effect of chronic treatment with morphine, midazolam and both together on dynorphin 1-13 levels in the rat Brain Res 754 1997 239 244
41. A. Rengasamy, T.N. Pajewski, and R.A. Johns Inhalational anesthetic effects on rat cerebellar nitric oxide and cyclic guanosine monophosphate production Anesthesiology 86 1997 689 698
42. V. Saano GABA-benzodiazepine receptor complex and drug actions Med Biol 65 1987 167 173
43. M. Schafer Cytokines and peripheral analgesia Adv Exp Med Biol 521 2003 40 50
44. G. Segovia, A. Porras, and F. Mora Effects of a nitric oxide donor on glutamate and GABA release in striatum and hippocampus of the conscious rat Neuroreport 5 1994 1937 1940
45. R.C. Spike, A.J. Todd, and H.M. Johnston Coexistence of NADPH diaphorase with GABA, glycine, and acetylcholine in rat spinal cord J Comp Neurol 335 1993 320 333
46. P. Sribanditmongkol, M.J. Sheu, and G.A. Tejwani Inhibition of morphine tolerance and dependence by diazepam and its relation to the CNS met-enkephalin levels Brain Res 645 1994 1 12
47. S. Talarek, and S. Fidecka Role of nitric oxide in benzodiazepines- induced antinociception in mice Pol J Pharmacol 54 2002 27 34
48. R.J. Tallarida, and R.B. Murray Manual of pharmacologic calculations with computer programs 1981 Springer Verlag New York
49. G.A. Tejwani, A.K. Rattan, S. Pongrak, M.J. Shen, J. Znniya, and J.S. MacDonald Inhibition of morphine-induced tolerance and dependence by a benzodiazepine receptor agonist midazolam in rat Anesth Analg 76 1993 1052 1060
50. G.A. Tejwani, P. Sribanditmongkul, and M.J. Sheu Inhibition of morphine tolerance and dependence by diazepam and its relation to CNS opioid peptides Regul Pept 54 1994 299 300
51. G.A. Tejwani, and A.K. Rattan Met-enkephalin alteration in the rat during chronic injection of morphine and/or midazolam Brain Res 775 1997 119 126
52. J.L. Thomas, H.L. Ingo, G.W. Christina, and H. Takahiko Effect of the NMDA-antagonist, MK 801, on benzodiazepine-opioid interactions at the spinal and supraspinal level in rats Br J Pharmacol 114 1995 1097 1103
53. M.K. Ticku Benzodiazepine-GABA receptor-ionophore complex. Current concepts Neuropharmacology 22 1983 1459 1470
54. J.R. Tobin, L.D. Martin, M.J. Breslow, and R.J. Traystman Selective anesthetic inhibition of brain nitric oxide synthase Anesthesiology 81 1994 1264 1269
55. ω-nitro-L-arginine blocks the release of met-enkephalin and antinociception induced by supraspinally administered β-endorphin in the rat Neuroscience 78 1997 461 467
56. J.G. Valtschanoff, R.J. Weinberg, A. Rustioni, and H.H. Schmidt Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord Neurosci Lett 148 1992 6 10
57. J.G. Valthschanoff, R.J. Weinberg, V.N. Kharazia, H.H. Schmidt, M. Nakane, and A. Rustioni Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA Neurosci Lett 157 1993 157 161
58. S.R. Vincent, and H. Kimura Histochemical mapping of nitric oxide synthase in the rat brain Neuroscience 46 1992 755 784
59. M.A. Vizzard, S.L. Erdman, V.L. Erickson, R.J. Stewart, J.R. Roppolo, and W.C. De Groat Localization of NADPH diaphorase in the lumbosacral spinal cord and dorsal root ganglia of the rat J Comp Neurol 339 1994 62 75
60. M. Waldhoer, S.E. Bartlett, and J.L. Whistler Opioid receptors Annu Rev Biochem 73 2004 953 990
61. C. Watanabe, T. Sakurada, K. Okuda, C. Sakurada, R. Ando, and S. Sakurada The role of spinal nitric oxide and glutamate in nociceptive behavior evoked by high-dose intrathecal morphine in rats Pain 106 2003 269 283
62. L.R. Watkins, and S.F. Maier Beyond neurons: evidence that immune and glial cells contribute to pathological pain states Physiol Rev 82 2002 981 1011
63. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial proinflammatory cytokines mediate exaggerated pain states: Implications for clinical pain Adv Exp Med Biol 521 2003 1 21
64. G.S. Watson, K.J. Sufka, and T.J. Coderre Optimal scoring strategies and weights for the formalin test in rats Pain 70 1997 53 58
65. H. Wilms, J. Claasen, C. Rohl, J. Sievers, G. Deuschl, and R. Lucius Involvement of benzodiazepine receptors in neuroinflammatory and neurodegenerative diseases: evidence from activated microglial cells in vitro Neurobiol Dis 14 2003 417 424
66. J.Y. Xu, and L.F. Tseng Increase of nitric oxide by L-arginine potentiates β-endorphin-but not μ-, δ-, or κ-opioid agonist-induced antinociception in the mouse Eur J Pharmacol 236 1993 137 142
67. J.Y. Xu, and L.F. Tseng Role of nitric oxide/cyclic GMP in i.c.v. administered endorphin- and (+)-cis-dioxolane-induced antinociception in the mouse Eur J Pharmacol 262 1994 223 231
68. J.Y. Xu, G.M. Pieper, and L.F. Tseng Activation of a NO-cyclic GMP system by NO donors potentiates β-endorphin-induced antinociception in the mouse Pain 63 1995 377 383
69. I. Yano, and A.E. Takemori Inhibition by naloxone of tolerance and dependence in mice treated acutely and chronically with morphine Res Commun Chem Pathol Pharmacol 16 1977 721 734
70. A receptors Neurosci Lett 180 1994 239 242