Pharmacological assessments of nitric oxide synthase isoforms and downstream diversity of NO signaling in the maintenance of thermal and mechanical hypersensitivity after peripheral nerve injury in mice

Neuropharmacology

Volumn 56, Issue 3, 2009, Pages 702-708

  Tanabe, Mitsuo ^a   Nagatani, Yoshinori ^a   Saitoh, Kazuya ^a   Takasu, Keiko ^a   Ono, Hideki ^a  

^a NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

Cyclic GMP; Free radicals; Neuropathic pain; Nitric oxide; Nitric oxide synthase; Peroxynitrite

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 2 AMINO 5,6 DIHYDRO 6 METHYL 4H 1,3 THIAZINE; 8 (4 CHLOROPHENYLTHIO) CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANOSINE TRIPHOSPHATE DERIVATIVE; GUANYLATE CYCLASE INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE INHIBITOR; ISOPROTEIN; N TERT BUTYL ALPHA PHENYLNITRONE; N(G) NITROARGININE METHYL ESTER; N(G) PROPYLARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TEMPOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG POTENCY; HEAT SENSITIVITY; MECHANICAL HYPERSENSITIVITY; MOUSE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCIATIC NERVE;

ANIMALS; ENZYME INHIBITORS; HYPERALGESIA; ISOENZYMES; MALE; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; PERIPHERAL NERVES; SCIATIC NEUROPATHY; SIGNAL TRANSDUCTION;

EID: 58749088198     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.12.003     Document Type: Article

References (45)

1. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochemical Journal 357 (2001) 593-615
2. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., and Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences of the United States of America 87 (1990) 1620-1624
3. Brenner G.J., Ji R.R., Shaffer S., and Woolf C.J. Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. European Journal of Neuroscience 20 (2004) 375-384
4. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. Journal of Neuroscience Methods 53 (1994) 55-63
5. Chen S.R., Khan G.M., and Pan H.L. Antiallodynic effect of intrathecal neostigmine is mediated by spinal nitric oxide in a rat model of diabetic neuropathic pain. Anesthesiology 95 (2001) 1007-1012
6. De Alba J., Clayton N.M., Collins S.D., Colthup P., Chessell I., and Knowles R.G. GW274150, a novel and highly selective inhibitor of the inducible isoform of nitric oxide synthase (iNOS), shows analgesic effects in rat models of inflammatory and neuropathic pain. Pain 120 (2006) 170-181
7. Dixon W.J. Efficient analysis of experimental observations. Annual Review of Pharmacology and Toxicology 20 (1980) 441-462
8. Ferreira J., Santos A.R., and Calixto J.B. The role of systemic, spinal and supraspinal l-arginine-nitric oxide-cGMP pathway in thermal hyperalgesia caused by intrathecal injection of glutamate in mice. Neuropharmacology 38 (1999) 835-842
9. Gao X., Kim H.K., Chung J.M., and Chung K. Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats. Pain 116 (2005) 62-72
10. Gao X., Kim H.K., Chung J.M., and Chung K. Reactive oxygen species (ROS) are involved in enhancement of NMDA-receptor phosphorylation in animal models of pain. Pain 131 (2007) 262-271
11. Glantz S.A. Alternatives to analysis of variance and the t test based on ranks. Primer of Biostatistics. third ed. (1992), McGraw-Hill, New York 320-371
12. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
13. Hua X.Y., Chen P., and Yaksh T.L. Inhibition of spinal protein kinase C reduces nerve injury-induced tactile allodynia in neuropathic rats. Neuroscience Letters 276 (1999) 99-102
14. Hylden J.L., and Wilcox G.L. Intrathecal morphine in mice: a new technique. European Journal of Pharmacology 67 (1980) 313-316
15. Ji R.R., Kohno T., Moore K.A., and Woolf C.J. Central sensitization and LTP: do pain and memory share similar mechanisms?. Trends in Neurosciences 26 (2003) 696-705
16. Kawamata T., and Omote K. Activation of spinal N-methyl-d-aspartate receptors stimulates a nitric oxide/cyclic guanosine 3′,5′-monophosphate/glutamate release cascade in nociceptive signaling. Anesthesiology 91 (1999) 1415-1424
17. Kim H.K., Park S.K., Zhou J.L., Taglialatela G., Chung K., Coggeshall R.E., and Chung J.M. Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111 (2004) 116-124
18. LaBuda C.J., Koblish M., Tuthill P., Dolle R.E., and Little P.J. Antinociceptive activity of the selective iNOS inhibitor AR-C102222 in rodent models of inflammatory, neuropathic and post-operative pain. European Journal of Pain 10 (2006) 505-512
19. Mabuchi T., Matsumura S., Okuda-Ashitaka E., Kitano T., Kojima H., Nagano T., Minami T., and Ito S. Attenuation of neuropathic pain by the nociceptin/orphanin FQ antagonist JTC-801 is mediated by inhibition of nitric oxide production. European Journal of Neuroscience 17 (2003) 1384-1392
20. Meller S.T., Dykstra C., and 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 tail-flick reflex. European Journal of Pharmacology 214 (1992) 93-96
21. Meller S.T., Pechman P.S., Gebhart G.F., and Maves T.J. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience 50 (1992) 7-10
22. Murphy R.M., Dutka T.L., and Lamb G.D. Hydroxyl radical and glutathione interactions alter calcium sensitivity and maximum force of the contractile apparatus in rat skeletal muscle fibres. Journal of Physiology 586 (2008) 2203-2216
23. Muscoli C., Mollace V., Wheatley J., Masini E., Ndengele M., Wang Z.Q., and Salvemini D. Superoxide-mediated nitration of spinal manganese superoxide dismutase: a novel pathway in N-methyl-d-aspartate-mediated hyperalgesia. Pain 111 (2004) 96-103
24. Nakane M., Klinghofer V., Kuk J.E., Donnelly J.L., Budzik G.P., Pollock J.S., Basha F., and Carter G.W. Novel potent and selective inhibitors of inducible nitric oxide synthase. Molecular Pharmacology 47 (1995) 831-834
25. Nathan C., and Xie Q.W. Regulation of biosynthesis of nitric oxide. Journal of Biological Chemistry 269 (1994) 13725-13728
26. Osborne M.G., and Coderre T.J. Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. British Journal of Pharmacology 126 (1999) 1840-1846
27. Pan H.L., Chen S.R., and Eisenach J.C. Role of spinal NO in antiallodynic effect of intrathecal clonidine in neuropathic rats. Anesthesiology 89 (1998) 1518-1523
28. Pitcher G.M., and Henry J.L. Second phase of formalin-induced excitation of spinal dorsal horn neurons in spinalized rats is reversed by sciatic nerve block. European Journal of Neuroscience 15 (2002) 1509-1515
29. Sasaki A., Mabuchi T., Serizawa K., Takasaki I., Andoh T., Shiraki K., Ito S., and Kuraishi Y. Different roles of nitric oxide synthase-1 and -2 between herpetic and postherpetic allodynia in mice. Neuroscience 150 (2007) 459-466
30. Schmidtko A., Ruth P., Geisslinger G., and Tegeder I. Inhibition of cyclic guanosine 5′-monophosphate-dependent protein kinase I (PKG-I) in lumbar spinal cord reduces formalin-induced hyperalgesia and PKG upregulation. Nitric Oxide 8 (2003) 89-94
31. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 (1990) 205-218
32. Song H.K., Pan H.L., and Eisenach J.C. Spinal nitric oxide mediates antinociception from intravenous morphine. Anesthesiology 89 (1998) 215-221
33. 2-adrenergic and muscarinic receptors and the NO release cascade mediate supraspinally produced effectiveness of gabapentin at decreasing mechanical hypersensitivity in mice after partial nerve injury. British Journal of Pharmacology 148 (2006) 233-244
34. Tal M. A novel antioxidant alleviates heat hyperalgesia in rats with an experimental painful peripheral neuropathy. Neuroreport 7 (1996) 1382-1384
35. Tanabe M., Sakaue A., Takasu K., Honda M., and Ono H. Centrally mediated antihyperalgesic and antiallodynic effects of zonisamide following partial nerve injury in the mouse. Naunyn-Schmiedeberg's Archives of Pharmacology 372 (2005) 107-114
36. Tao Y.X., Hassan A., Haddad E., and Johns R.A. Expression and action of cyclic GMP-dependent protein kinase Iα in inflammatory hyperalgesia in rat spinal cord. Neuroscience 95 (2000) 525-533
37. Tao F., Tao Y.X., Mao P., Zhao C., Li D., Liaw W.J., Raja S.N., and Johns R.A. Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience 120 (2003) 847-854
38. Tao F., Tao Y.X., Zhao C., Doré S., Liaw W.J., Raja S.N., and Johns R.A. Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia. Neuroscience 128 (2004) 421-430
39. Tegeder I., Del Turco D., Schmidtko A., Sausbier M., Feil R., Hofmann F., Deller T., Ruth P., and Geisslinger G. Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proceedings of the National Academy of Sciences of the United States of America 101 (2004) 3253-3257
40. Wang X., and Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. Journal of Neurochemistry 68 (1997) 443-456
41. Xu L., Mabuchi T., Katano T., Matsumura S., Okuda-Ashitaka E., Sakimura K., Mishina M., and Ito S. Nitric oxide (NO) serves as a retrograde messenger to activate neuronal NO synthase in the spinal cord via NMDA receptors. Nitric Oxide 17 (2007) 18-24
42. Xu Z., Tong C., Pan H.L., Cerda S.E., and Eisenach J.C. Intravenous morphine increases release of nitric oxide from spinal cord by an α-adrenergic and cholinergic mechanism. Journal of Neurophysiology 78 (1997) 2072-2078
43. Yoon Y.W., Sung B., and Chung J.M. Nitric oxide mediates behavioral signs of neuropathic pain in an experimental rat model. Neuroreport 9 (1998) 367-372
44. ω-propyl-l-arginine. Journal of Medicinal Chemistry 40 (1997) 3869-3870
45. Zhuo M., Meller S.T., and Gebhart G.F. Endogenous nitric oxide is required for tonic cholinergic inhibition of spinal mechanical transmission. Pain 54 (1993) 71-78