Spinal ERK activation via NO-cGMP pathway contributes to nociceptive behavior induced by morphine-3-glucuronide

Biochemical Pharmacology

Volumn 78, Issue 8, 2009, Pages 1026-1034

  Komatsu, Takaaki ^a   Sakurada, Shinobu ^b   Kohno, Kazuhiro ^b   Shiohira, Hideo ^a   Katsuyama, Sou ^a   Sakurada, Chikai ^c   Tsuzuki, Minoru ^c   Sakurada, Tsukasa ^a  

^a DAIICHI UNIVERSITY OF PHARMACY   (Japan)

^b TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^c NIHON PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Dorsal spinal cord; Extracellular signal regulated kinase (ERK); Mice; Morphine 3 glucuronide (M3G); Nitric oxide (NO) cGMP PKG pathway; NK1 receptor; NMDA receptor

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; KT 5823; MITOGEN ACTIVATED PROTEIN KINASE; MORPHINE; MORPHINE 3 GLUCURONIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME INHIBITION; LUMBAR SPINAL CORD; MALE; MOUSE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; BUTADIENES; CENTRAL NERVOUS SYSTEM STIMULANTS; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INJECTIONS, SPINAL; ISOINDOLES; MALE; MICE; MICE, INBRED STRAINS; MORPHINE DERIVATIVES; NITRIC OXIDE; NITRILES; NOCICEPTORS; PAIN; PEPTIDE FRAGMENTS; PIPERIDINES; PYRROLIDONECARBOXYLIC ACID; RECEPTORS, TACHYKININ; SPECIFIC PATHOGEN-FREE ORGANISMS; SPINAL CORD; STEREOISOMERISM; SUBSTANCE P;

EID: 69349095699     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.06.106     Document Type: Article

References (54)

1. Sakurada T., Wako K., Sakurada C., Manome Y., Tan-No K., Sakurada S., et al. Spinally-mediated behavioral responses evoked by intrathecal high-dose morphine: possible involvement of substance P in the mouse spinal cord. Brain Res 724 (1996) 213-221
2. Woolf F.J. Intrathecal high dose morphine produces hyperalgesia in the rat. Brain Res 209 (1981) 491-495
3. Yaksh T.L., Harty G.J., Burton M., and Onofrio B.M. High doses of spinal morphine produce a nonopiate receptor-mediated hyperesthesia: clinical and theoretical implications. Anesthesiology 64 (1986) 590-597
4. Watanabe C., Sakurada T., Okuda K., Sakurada C., Ando R., and Sakurada S. The role of spinal nitric oxide and glutamate in nociceptive behaviour evoked by high-dose intrathecal morphine in rats. Pain 106 (2003) 269-283
5. Boerner U., Abbott S., and Roe R.L. The metabolism of morphine and heroin in man. Drug Metab Rev 4 (1975) 39-73
6. Christensen C.B., and Jorgensen L.N. Morphine-6-glucronide has high affinity for the opioid receptor. Pharmacol Toxicol 60 (1987) 75-76
7. Pasternak G.W., Bodnar R.J., Clark J.A., and Intrurrisi C.E. Morphine-6-glucuronide, a potent mu agonist. Life Sci 41 (1987) 2845-2849
8. Smith M.T. Neuroexcitatory effects of morphine and hydromorphine: evidence inmplicating the 3-glucuronide metabolites. Clin Exp Pharmacol Physiol 27 (2000) 524-528
9. Yaksh T.L., and Harty G.J. Parmacology of the allodynia in rats evoked by high dose intrathecal morphine. J Pharmacol Exp Ther 244 (1988) 501-507
10. Komatsu T., Sakurada C., Sasaki M., Sanai K., Tsuzuki M., Bagetta G., et al. Extracellular signal-regulated kinase (ERK) and nitric oxide synthase mediate intrathecal morphine-induced nociceptive behavior. Neuropharmacology 52 (2007) 1237-1243
11. Qian Y., Chao D.S., Santillano D.R., Cornwell T.L., Narin A.C., Greengard P., et al. cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16 (1996) 3130-3138
12. 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
13. Garry M.G., Richardson J.D., and Hargreaves K.M. Carrageenan induced inflammation alters the content of i-cGMP and i-cAMP in the dorsal horn of the spinal cord. Brain Res 646 (1994) 135-139
14. Siegan J.B., Hama A.T., and Sagen J. Alterations in rat spinal cord cGMP by peripheral nerve injury and adrenal medullary transplantation. Neurosci Lett 215 (1996) 49-52
15. Tao Y.X., Hassan A., Haddad E., and Johns R.A. Expression and action of cyclic GMP-dependent protein kinase Ialpha in inflammatory hyperalgesia in rat spinal cord. Neuroscience 95 (2000) 525-533
16. Tegeder I., Schmidtko A., Niederberger E., Ruth P., and Geisslinger G. Dual effects of spinally delivered 8-bromo-cyclic guanosine mono-phosphate (8-bromo-cGMP) in formalin-induced nociception in rats. Neurosci Lett 332 (2002) 146-150
17. Tegeder I., Del-Turco D., Schmidtko A., Sausbier M., Feil R., Hofmann F., et al. Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Nati Acad Sci USA 101 (2004) 3253-3257
18. Morita K., Kitayama T., Morioka N., and Dohi T. Glycinergic mediation of tactile allodynia induced by platelet-activating factor (PAF) through glutamate-NO-cyclic GMP signalling in spinal cord in mice. Pain 138 (2008) 525-536
19. Ji R.R., Baba H., Brenner G.J., and Woolf C.J. Nociceptive specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2 (1999) 1114-1119
20. Karim F., Wang C.C., and Gereau R.W. Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 21 (2001) 3771-3779
21. Galan A., Lopez-Garcia J.A., Cervero F., and Laird J.M.A. Activation of spinal extracellular signaling-regulated kinase-1 and -2 by intraplantar carrageenan in rodents. Neurosci Lett 322 (2002) 37-40
22. Hylden J.L.K., and Wilcox G.L. Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67 (1980) 191-194
23. Sakurada T., Manome Y., Tan-No K., Sakurada S., Kisara K., Ohba M., et al. A selective and extremely potent antagonist of the nerokinin-1 receptor. Brain Res 593 (1992) 319-322
24. Sakurada T., Watanabe C., Okuda K., Sugiyama A., Moriyama T., Sakurada C., et al. Intrathecal high-dose morphine induces spinally-mediated behavioral responses through NMDA receptors. Mol Brain Res 98 (2002) 111-118
25. Yamada H., Ishi K., Ishii Y., Ieiri I., Nishimoto S., Morioka T., et al. Formation of highly analgesic morphine-6-gluclonide following physiologic concentration of morphine in human brain. J Toxicol Sci 28 (2003) 395-401
26. 7,9-substance P. Neuropharmacology 22 (1983) 1397-1400
27. Meller S.T., and Gebhart G.F. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52 (1993) 127-136
28. Wu J., Lin Q., McAdoo D.J., and Willis W.D. Nitric oxide contributes to central sensitization following intradermal injection of capsaicin. NeuroReport 9 (1998) 589-592
29. Sakurada T., Sugiyama A., Sakurada C., Tan-No K., Sakurada S., Kisara K., et al. Involvement of nitric oxide in spinally mediated capsaicin- and glutamate-induced behavioural responses in the mouse. Neurochem Int 29 (1996) 271-278
30. Sakurada C., Sugiyama A., Nakayama M., Yonezawa A., Sakurada S., Tan-No K., et al. Antinociceptive effect of spinally injected L-NAME on the acute nociceptive response induced by low concentrations of formalin. Neurochem Int 38 (2001) 417-423
31. Berridge M.J. Inositol trisphosphate and calcium signaling. Nature 361 (1993) 315-325
32. Wu J., Fang L., Lin Q., and Willis W.D. Nitric oxide synthase in spinal cprd cemtral sensitization following intradermal injection of capsaicin. Pain 94 (2001) 47-58
33. Osborne M.G., and Coderre T.J. Effect of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. Br J Pharmacol 126 (1999) 1840-1846
34. Sakaue G., Shimaoka M., Fukuoka T., Hiroi T., Inoue T., Hashimoto N., et al. NF-Kappa B decoy suppresses cytokine expression and themal hyperalgesia in a rat neuropathic pain model. NeuroReport 12 (2001) 2079-2084
35. Meller S.T., Dykstra C., Grzybycki D., Murphy S., and Gebhart G.F. The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology 33 (1994) 1471-1478
36. Xu J., Kim G.M., Chen S., Yan P., Ahmed S.H., Ku G., et al. iNOS and nitrotyrosine expression after spinal cord injury. J Neurotrauma 18 (2001) 523-532
37. Hamada Y., Ikata T., Katoh S., Tsuchiya K., Niwa M., Tsutsumishita Y., et al. Role of nitric oxide in compression injury of rat spinal cord. Free Radic Biol Med 20 (1996) 1-9
38. Wieseler-Frank J., Maier S.F., and Watkins L.R. Central proinflammatory cytokines and pain enhancement. Neuro-signal 14 (2005) 166-174
39. Sung C.S., Wen Z.H., Chang W.K., Ho S.T., Tsai S.K., Chang Y.C., et al. Intrathecal interleukin-1beta administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord. Brain Res 1015 (2004) 145-153
40. Martin F.C., Charles A.C., Sanderson M.J., and Merrill J.E. Substance P stimulate IL-1 production by astrocyte via intracellular calcium. Brain Res 599 (1992) 13-18
41. Holguin A, O'connor KA, Biedenkapp J, Campisi J, Wieseler-Frank J, Milligan ED, et al. HIV-1 gp120 stimulates proinflammatory cytokine-mediated pain facilitation via activation of nitric oxide synthase-I (nNOS). Pain 2004;110:517-30.
42. Guo W., Wang H., Watanabe M., Shimizu K., Zou S., LaGraize S.C., et al. Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27 (2007) 6006-6018
43. Watkins L.R., Hutchison M.R., Ledeboer A., Wieseler-Frank J., Milligan E.D., and Maier S.F. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids. Brain Behav Immun 21 (2007) 131-146
44. Kawasaki Y., Kohno T., Zhuang Z.Y., Brenner G.J., Wang H., Van DerMeerC, et al. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci 24 (2004) 8310-8321
45. Lever I.J., Pezet S., McMahon S.B., and Malcangio M. The signaling components of sensory fiber transmission involved in the activation of ERK MAP kinase in the mouse dorsal horn. Mol Cell Neurosci 24 (2003) 259-270
46. Callsen D., Pfeilschifter J., and Brune B. Rapid and delayed p42/p44 mitogen-activated protein kinase activation by nitric oxide: the role of cyclic GMP and tyrosine phosphatase inhibition. J Immunol 161 (1998) 4852-4858
47. Parenti A., Morbidelli L., Cui X.L., Douglas J.G., Hood J.D., Granger H.J., et al. Nitiric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase 1/2 acdtivation in postcapillary endothelium. J Biol Chem 273 (1998) 4220-4226
48. Yamazaki M., Chiba K., Mohri T., and Hatanaka H. Activation of the mitogen-activated protein kinase cascade through nitric oxide synthesis as a mechanism of neuritogenic effect of genipin in PC12 cells. J Neurochem 79 (2001) 45-54
49. Sung Y.J., Walters E.T., and Ambron R.T. A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear important to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24 (2004) 7583-7595
50. Chien W.J., Liang K.C., Teng C.M., Kuo S.C., Lee F.Y., and Fu W.M. Enhancement of long-term potentiation by a potent nitric oxide-guanylyl cyclase activator 3-(5-hydroxymethyl-2-furyl)-1-benzyl imidazole. Mol Pharmacol 63 (2003) 1322-1328
51. Hu H.J., Glauner K.S., and Gereau R.W. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K currents. J Neurophysiol 90 (2003) 1671-1679
52. Morozov A., Muzzio I.A., Bourtchouladze R., Van-strien N., Lapidus K., Yin D., et al. Rap1 couples camp signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39 (2003) 309-325
53. Zhu J.J., Qin Y., Zhao M., Van-Aelst L., and Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110 (2002) 443-455
54. Ji R.R., Kohno T., Moore K.A., and Woolf C.J. Central sensitization and longterm potentiation-do pain and memory share similar mechanism?. Trends Neurosci 26 (2003) 696-705