Evidence that nitric oxide-glutamate cascade modulates spinal antinociceptive effect of morphine: A behavioural and microdialysis study in rats

Brain Research

Volumn 990, Issue 1-2, 2003, Pages 77-86

  Watanabe, Chizuko ^a   Okuda, Kazuhiro ^b   Sakurada, Chikai ^c   Ando, Ryuichiro ^a   Sakurada, Tsukasa ^c   Sakurada, Shinobu ^a  

^a TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^b Department of Internal Medicine   (Japan)

^c DAIICHI UNIVERSITY OF PHARMACY   (Japan)

Author keywords

Antinociception; Glutamate; Intrathecal injection; L NAME; Morphine; Nitric oxide; Spinal cord

Indexed keywords

FORMALDEHYDE; GLUTAMIC ACID; MORPHINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; BITE; CONTROLLED STUDY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; LICKING; MALE; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

EID: 0141918795     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(03)03440-1     Document Type: Article

References (57)

1. Aanonsen L.M., Wilcox G.L. Nociceptive action of excitatory amino acids in the mouse: effects of spinally administered opioids, phencyclidine and sigma agonists. J. Pharmacol. Exp. Ther. 243:1987;9-19.
2. Aimi Y., Fujimura M., Vincent S.R., Kimura H. Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J. Comp. Neurol. 306:1991;382-392.
3. Barjavel M.J., Bhargava H.N. Effect of opioid receptor agonists on nitric oxide synthase activity in rat cerebral cortex homogenate. Neurosci. Lett. 181:1994;27-30.
4. Bredt D.S., Snyder S.H. Nitric oxide, a novel neuronal messenger. Neuron. 8:1992;3-11.
5. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH-diaphorase. Neuron. 7:1991;615-624.
6. Brown J.H., Kissel J.W., Lish P.M. Studies on the acute inflammatory response. I. Involvement of the central nervous system in certain models of inflammation. J. Pharmacol. Exp. Ther. 160:1968;231-242.
7. Cahusac P.M.B., Evans R.H., Hill R.G., Rodriquez R.E., Smith D.A.S. The behavioural effects of an N-methylaspartate receptor antagonist following application to the lumbar spinal cord of conscious rats. Neuropharmacology. 23:1984;719-724.
8. Coderre T.J., Melzack R. The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J. Neurosci. 12:1992;3665-3670.
9. Coderre T.J., Yashpal K. Intracellular messengers contributing to persistent nociception and hyperalgesia induced by L-glutamate and substance P in the rat formalin pain model. J. Neurosci. 6:1994;1328-1334.
10. Dickenson A.H., Sullivan A.F. Peripheral origins and central modulation of subcutaneous formalin-induced activity of rat dorsal horn neurones. Neurosci. Lett. 183:1987;207-211.
11. Dickenson A.H., Sullivan A.F. Subcutaneous formalin-induced activity of dorsal horn neurones in the rat: differential response to an intrathecal opiate administered pre or post formalin. Pain. 30:1987;349-360.
12. Dubuisson D., Dennis S.G. 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. Dun N.J., Dun S.L., Forstmann U., Tseng L.F. Nitric oxide synthase immunoreactivity in rat spinal cord. Neurosci. Lett. 147:1992;217-220.
14. Forstermann U., Kleinert H. Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedeberg's Arch. Pharmacol. 352:1995;351-364.
15. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;60-67.
16. Garthwaite J., Charles S.L., Chess-Willams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intracellular messenger in the brain. Nature. 326:1988;385-387.
17. Haley J.E., Sullivan A.F., Dickenson A.H. Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518:1990;218-226.
18. Haley J.E., Dickenson A.H., Schachter M. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology. 31:1992;251-258.
19. Hunskaar S., Hole K. Formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain. 30:1987;103-114.
20. Irwin S., Houde R.W., Bennett D.R., Hendershot L.C., Seevers M.H. The effect of morphine, methadone and meperidine on some reflex responses of spinal animals to nociceptive stimulation. J. Pharmacol. Exp. Ther. 10:1951;132-143.
21. Kangra I., Randic M. Outflow of endogenous aspartate and glutamate from the rat spinal dorsal horn in vitro by activation of low- and high-threshold primary afferent fibres. Modulation of μ opioids. Brain Res. 553:1991;347-352.
22. Kitto K.F., Haley J.E., Wilcox G.L. Involvement of nitric oxide in spinally mediated hyperalgesia in the mouse. Neurosci. Lett. 148:1992;1-5.
23. Lindoth P., Mopper K. High performance liquid chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivatization with o-phtaldialdehyde. Anal. Chem. 51:1997;1667-1674.
24. Litchfield J.T., Wilcoxon F.A. A simplified method of evaluating dose-effect experiments. J. Pharmacol. Exp. Ther. 96:1949;99-113.
25. Lombard M.C., Besson J.M. Attempts to gauge the relative importance of pre- and postsynaptic effects of morphine on the transmission of noxious messages in the dorsal horn of the rat spinal cord. Pain. 37:1989;335-345.
26. Machelska H., Labuz D., Przewlocki R., Przewlocka B. Inhibition of nitric oxide synthase enhances antinociception mediated by mu, delta and kappa opioid receptors in acute and prolonged pain in rat spinal cord. J. Pharmacol. Exp. Ther. 282:1997;977-984.
27. Malmberg A.B., Yaksh T.L. Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain. 54:1993;291-300.
28. 2 using microdialysis in conscious rats. Br. J. Pharmacol. 114:1995;1069-1075.
29. Marsala M., Malmberg A.B., Yaksh T.L. The spinal loop dialysis catheter: characterization of use in the unanesthetized rat. J. Neurosci. Methods. 62:1995;43-53.
30. Meller S.T., Gebhart G.F. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain. 52:1993;127-136.
31. Meller S.T., Dykstra C., Gebhart G.F. Production of endogenous nitric oxide and activation of soluble guanylate cyclase are required for N-methyl-D-aspartate-produced facilitation of the nociceptive tailflick reflex. Eur. J. Pharmacol. 214:1992;93-96.
32. Meller S.T., Pechman P.S., Gebhart G.F., Maves T.J. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience. 50:1992;7-10.
33. Moore P.K., Oluyomi A.O., Babbedge R.C., Wallace P., Hart S.L. L-N-nitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br. J. Pharmacol. 102:1991;198-202.
34. Narayanan K., Griffith O.W. Synthesis of L-thiocitrullin, L-homocitrulline, and S-methyl-L-thiocitrulline: a new class of potent nitric oxide synthase inhibitiors. J. Med. Chem. 37:1994;885-887.
35. Okuda K., Sakurada C., Takahashi M., Yamada T., Sakurada T. Characterization of nociceptive responses and spinal releases of nitric oxide metabolites and glutamate evoked by different concentrations of formalin in rats. Pain. 92:2001;107-115.
36. Porro C.A., Cavazzuti M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog. Neurobiol. 41:1993;565-607.
37. Przewlocki R., Machelska H., Przewlocka B. Inhibition of nitric oxide synthase enhances morphine antinociception in the rat spinal cord. Life Sci. 53:1993;PL1-PL5.
38. Puig S., Sorkin L.S. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain. 64:1995;345-355.
39. Radhakrishnan V., Henry J.L. L-NAME blocks responses to NMDA, substance P and noxious cutaneous stimuli in cat dorsal horn. NeuroReport. 4:1993;323-326.
40. Rosland J.H., Tjolsen A., Mahle B., Hole K. The formalin test in mice: effect of formalin concentration. Pain. 42:1990;235-242.
41. Sakurada T., Manome Y., Tan-No K., Sakurada S., Kisara K. The effects of substance P analogues on the scratching, biting and licking response induced by intrathecal injection of N-methyl-D-aspartate in mice. Br. J. Pharmacol. 101:1990;307-310.
42. Sakurada T., Sugiyama A., Sakurada C., Tan-No K., Yonezawa A., Sakurada S., Kisara K. Effect of spinal nitric oxide inhibition on capsaicin-induced nociceptive response. Life Sci. 11:1996;921-930.
43. Sakurada T., Sugiyama A., Sakurada C., Tan-No K., Yonezawa A., Sakurada S., Kisara K., Hara A., Abiko Y. Involvement of nitric oxide in spinally mediated capsaicin- and glutamate-induced behavioural responses in the mouse. Neurochem. Int. 29:1996;271-278.
44. Sakurada C., Sugiyama A., Nakayama M., Yonezawa A., Sakurada S., Tan-No K., Kisara K., Sakurada T. Antinociceptive effect of spinally injected L-NAME on the acute nociceptive response induced by low concentrations of formalin. Neurochem. Int. 38:2001;417-423.
45. Schmidt H.H.H.W., Gagne G.D., Nakane M., Pollock J.S., Miller M.F., Murad F. Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J. Histochem. Cytochem. 40:1992;1439-1456.
46. Skilling S.R., Smullin D.H., Beits A.Z., Larson A.A. Extracellular amino acid concentrations in the dorsal spinal cord of freely moving rats following veratridine and nociceptive stimulation. J. Neurochem. 51:1988;127-132.
47. Sorkin L.S. NMDA evokes an L-NAME sensitive spinal release of glutamate and citrulline. NeuroReport. 4:1993;479-482.
48. Terenghi G., Riveros-Moreno V., Hudson L.D., Ibrahim N.B.N., Polak J.M. Immunohistochemistry of nitric oxide synthase demonstrates immunoreactive neurons in spinal cord and dorsal root ganglia of man and rat. J. Neurol. Sci. 118:1993;34-37.
49. Tjolsen A., Berge O.G., Hunskaar S., Rosland J.H., Hole K. The formalin test: an evaluation of the method. Pain. 51:1992;5-17.
50. Valtschanoff J.G., Weinberg R.J., Rustioni A., Schmidt H.H.H.W. Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord. Neurosci. Lett. 148:1992;6-10.
51. Wheeler-Aceto H., Porreca F., Cowan A. The rat paw formalin test: comparison of noxious agents. Pain. 40:1990;229-238.
52. Xu J.Y., Tseng L.F. Nitric oxide/cyclic guanosine monophosphate system in the spinal cord differentially modulates intracerebroventricularly administered morphine- and β-endorphin- induced antinociception in the mouse. J. Pharmacol. Exp. Ther. 274:1995;8-16.
53. Yaksh T.L., Jesell T.M., Gamse R., Leeman S.E. Intrathecal morphine inhibits substance P release from mammalian spinal cord in vivo. Nature. 286:1980;155-156.
54. ω nitro L-arginine methyl ester on thermal nociceptive tests in the rats. Can. J. Anaesth. 43:1996;975-981.
55. Yamamoto T., Shimoyama N. Role of nitric oxide in the development of thermal hyperesthesia induced by sciatic nerve constriction injury in the rat. Anesthesiology. 82:1995;1266-1273.
56. Yamamoto T., Yaksh T.L. Comparison of the antinociceptive effects of pre- and post-treatment with intrathecal morphine and MK-801, an NMDA antagonist, on the formalin test in the rat. Anesthesiology. 77:1992;757-776.
57. Yamamoto T., Shimoyama N., Mizuguchi T. Nitric oxide synthase inhibitor blocks spinal sensitization induced by formalin injection into the rat paw. Anesth. Analg. 77:1993;886-890.