Spinal α 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

Volumn 148, Issue 2, 2006, Pages 233-244

  Takasu, Keiko ^a   Honda, Motoko ^a   Ono, Hideki ^a   Tanabe, Mitsuo ^a  

^a NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

2 adrenergic receptors; Allodynia; Descending noradrenergic system; Gabapentin; Muscarinic receptors; Nitric oxide

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; ATROPINE; GABAPENTIN; IDAZOXAN; METHOCTRAMINE; MUSCARINIC RECEPTOR; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NALOXONE; NEOSTIGMINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; OPIATE RECEPTOR; PIRENZEPINE; YOHIMBINE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; HYPERSENSITIVITY; MALE; MECHANICAL HYPERSENSITIVITY; MOUSE; NERVE INJURY; NERVE LIGATION; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; SCIATIC NERVE; THERMAL HYPERSENSITIVITY;

ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; AMINES; ANALGESICS; ANIMALS; ATROPINE; CHOLINESTERASES; CYCLOHEXANECARBOXYLIC ACIDS; ENZYME ACTIVATION; GAMMA-AMINOBUTYRIC ACID; HEAT; HOT TEMPERATURE; HYPERALGESIA; IDAZOXAN; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MUSCARINIC ANTAGONISTS; NEOSTIGMINE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OMEGA-N-METHYLARGININE; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, MUSCARINIC; RECEPTORS, OPIOID; SCIATIC NERVE; SPINAL CORD; TOUCH; YOHIMBINE;

EID: 33745045753     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706731     Document Type: Article

References (63)

1. BACKONJA, M., BEYDOUN, A., EDWARDS, K.R., SCHWARTZ, S.L., FONSECA, V., HES, M., LAMOREAUX, L. & GAROFALO, E. (1998). Gabapentin for the symptomatic treatment of painful neuropathy in patients with diabetes mellitus: a randomized controlled trial. J. Am. Med. Assoc., 280, 1831-1836.
2. 2+ channels. Neuropharmacology, 46, 743-749.
3. BODNAR, R.J., PAUL, D., ROSENBLUM, M., LIU, L. & PASTERNAK, G.W. (1990). Blockade of morphine analgesia by both pertussis and cholera toxins in the periaqueductal gray and locus coeruleus. Brain Res., 529, 324-328.
4. G-nitro L-arginine methyl ester and other alkyl esters of arginine are muscarinic receptor antagonists. Circ. Res., 72, 387-395.
5. CHAPLAN, S.R., BACH, F.W., POGREL, J.W., CHUNG, J.M. & YAKSH, T.L. (1994). Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Math., 53, 55-63.
6. CHEN, S.R. & PAN, H.L. (2001). Spinal endogenous acetylcholine contributes to the analgesic effect of systemic morphine in rats. Anesthesiology, 95, 525-530.
7. CHEN, S.R. & PAN, H.L. (2003). Up-regulation of spinal muscarinic receptors and increased antinociceptive effect of intrathecal muscarine in diabetic rats. J. Pharmacol. Exp. Ther., 307, 676-681.
8. CHEN, S.R., KHAN, G.M. & PAN, H.L. (2001). Antiallodynic effect of intrathecal neostigmine is mediated by spinal nitric oxide in a rat model of diabetic neuropathic pain. Anesthesiology, 95, 1007-1012.
9. DE KOCK, M., EISENACH, J., TONG, C., SCHMITZ, A.L. & SCHOLTES, J.L. (1997). Analgesic doses of intrathecal but not intravenous clonidine increase acetylcholine in cerebrospinal fluid in humans. Anesth. Analg., 84, 800-803.
10. 2 adrenoceptor-mediated antinociception in sheep. J. Pharmacol. Exp. Ther., 265, 536-542.
11. DIXIT, R.K. & BHARGAVA, V.K. (2002). Neurotransmitter mechanisms in gabapentin anitnociception. Pharmacology, 65, 198-203.
12. DIXON, W.J. (1980). Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol., 20, 441-462.
13. DÖRJE, F., WESS, J., LAMBRECHT, G., TACKE, R., MUTSCHLER, E. & BRANN, M.R. (1991). Antagonist binding profiles of five cloned human muscarinic receptor subtypes. J. Pharmacol. Exp. Ther., 256, 727-733.
14. EISENACH, J.C. (1999). Muscarinic-mediated analgesia. Life Sci., 64, 549-554.
15. FIELD, M.J., OLES, R.J., LEWIS, A.S., MCCLEARY, S., HUGHES, J. & SINGH, L. (1997). Gabapentin (neurontin) and 5-(+)-3-isobutyl-gaba represent a novel class of selective antihyperalgesic agents. Br. J. Pharmacol., 121, 1513-1522.
16. 2δ subunit of a calcium channel. J. Biol. Chem., 271, 5768-5776.
17. GLANTZ, S.A. (1992). Alternatives to analysis of variance and the t test based on ranks. In: Primer of Biostatistics. 3rd edn. eds. Jeffers, J.D. & Englis, M.R., pp. 320-371. New York: McGraw-Hill.
18. 2 muscarinic receptor function in the lungs by extracellular nitric oxide. Br. J. Pharmacol., 131, 312-318.
19. HALEY, T.J. & MCCORMICK, W.G. (1957). Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br. J. Pharmacol., 12, 12-15.
20. HARGREAVES, K., DUBNER, R., BROWN, F., FLORES, C. & JORIS, J. (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32, 77-88.
21. HWANG, J.H. & YAKSH, T.L. (1997). Effect of subarachnoid gabapentin on tactile-evoked allodynia in a surgically induced neuropathic pain model in the rat. Reg. Anesth., 22, 249-256.
22. HWANG, J.H., HWANG, K.S., LEEM, J.K., PARK, P.H., HAN, S.M. & LEE, D.M. (1999). The antiallodynic effects of intrathecal cholinesterase inhibitors in a rat model of neuropathic pain. Anesthesiology, 90, 492-499.
23. HYLDEN, J.L. & WILCOX, G.L. (1980). Intrathecal morphine in mice: a new technique. Eur. J. Pharmacol., 67, 313-316.
24. INOUE, T., MASHIMO, T., SHIBATA, M., SHIBUTA, S. & YOSHIYA, I. (1998). Rapid development of nitric oxide-induced hyperalgesia depends on an alternate to the cGMP-mediated pathway in the rat neuropathic pain model. Brain Res., 792, 263-270.
25. IWAMOTO, E.T. & MARION, L. (1994). Pharmacologic evidence that spinal muscarinic analgesia is mediated by an L-arginine/nitric oxide/cyclic GMP cascade in rats. J. Pharmacol. Exp. Ther., 271, 601-608.
26. JI, R.R., KOHNO, T., MOORE, K.A. & WOOLF, C.J. (2003). Central sensitization and LTP: do pain and memory share similar mechanisms? Trends. Neurosci., 26, 696-705.
27. KANEKO, M., MESTRE, C., SÁNCHEZ, E.H. & HAMMOND, D.L. (2000). Intrathecally administered gabapentin inhibits formalin-evoked nociception and the expression of Fos-like immunoreactivity in the spinal cord of the rat. J. Pharmacol. Exp. Ther., 292, 743-751.
28. 1 receptor in streptozotocin-induced diabetic mice. Eur. J. Pharmacol., 505, 75-82.
29. LAUGHLIN, T.M., TRAM, K.V., WILCOX, G.L. & BIRNBAUM, A.K. (2002). Comparison of antiepileptic drugs tiagabine, lamotrigine, and gabapentin in mouse models of acute, prolonged, and chronic nociception. J. Pharmacol. Exp. Ther., 302, 1168-1175.
30. 2δ-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J. Pharmacol. Exp. Ther., 303, 1199-1205.
31. 2δ calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J. Neurosci., 21, 1868-1875.
32. MABUCHI, T., MATSUMURA, S., OKUDA-ASHITAKA, E., KITANO, T., KOJIMA, H., NAGANO, T., MINAMI, T. & ITO, S. (2003). Attenuation of neuropathic pain by the nociceptin/orphanin FQ antagonist JTC-801 is mediated by inhibition of nitric oxide production. Eur. J. Neurosci., 17, 1384-1392.
33. 2 receptor agonist in rats with nerve ligation injury. Brain Res., 932, 124-128.
34. PAN, H.L., CHEN, S.R. & EISENACH, J.C. (1998). Role of spinal NO in antiallodynic effect of intrathecal clonidine in neuropathic rats. Anesthesiology, 89, 1518-1523.
35. PAN, H.L., CHEN, S.R. & EISENACH, J.C. (1999a). Intrathecal clonidine alleviates allodynia in neuropathic rats: interaction with spinal muscarinic and nicotinic receptors. Anesthesiology, 90, 509-514.
36. PAN, H.L., EISENACH, J.C. & CHEN, S.R. (1999b). Gabapentin suppresses ectopic nerve discharges and reverses allodynia in neuropathic rats. J. Pharmacol. Exp. Ther., 288, 1026-1030.
37. PAQUERON, X., CONKLIN, D. & EISENACH, J.C. (2003). Plasticity in action of intrathecal clonidine to mechanical but not thermal nociception after peripheral nerve injury. Anesthesiology, 99, 199-204.
38. PAQUERON, X., LI, X., BANTEL, C., TOBIN, J.R., VOYTKO, M.L. & EISENACH, J.C. (2001). An obligatory role for spinal cholinergic neurons in the antiallodynic effects of clonidine after peripheral nerve injury. Anesthesiology, 94, 1074-1081.
39. PATEL, M.K., GONZALEZ, M.I., BRAMWELL, S., PINNOCK, R.D. & LEE, K. (2000). Gabapentin inhibits excitatory synaptic transmission in the hyperalgesic spinal cord. Br. J. Pharmacol., 130, 1731-1734.
40. 2C receptor agonist, in two rat models of sustained pain. Anesth. Analg., 96, 1072-1078.
41. SAWYNOK, J. & REID, A. (1987). Effect of 6-hydroxydopamine-induced lesions to ascending and noradrenergic pathways on morphine analgesia. Brain Res., 419, 156-165.
42. SEGAL, A.Z. & RORDORF, G. (1996). Gabapentin as a novel treatment for postherpetic neuralgia. Neurology, 46, 1175-1176.
43. SELTZER, Z., DUBNER, R. & SHIR, Y. (1990). A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain, 43, 205-218.
44. SHIMOYAMA, M., SHIMOYAMA, N. & HORI, Y. (2000). Gabapentin affects glutamatergic excitatory neurotransmission in the rat dorsal horn. Pain, 85, 405-414.
45. SINGH, L., FIELD, M.J., FERRIS, P., HUNTER, J.C., OLES, R.J., WILLIAMS, R.G. & WOODRUFF, G.N. (1996). The antiepileptic agent gabapentin (Neurontin) possesses anxiolytic-like and antinociceptive actions that are reversed by D-serine. Psvchopharmacology, 127, 1-9.
46. SONG, H.K., PAN, H.L. & EISENACH, J.C. (1998). Spinal nitric oxide mediates antinociception from intravenous morphine. Anesthesiology, 89, 215-221.
47. SOUSA, A.M. & PRADO, W.A. (2001). The dual effect of a nitric oxide donor in nociception. Brain Res., 897, 9-19.
48. SUTTON, K.G., MARTIN, D.J., PINNOCK, R.D., LEE, K. & SCOTT, R.H. (2002). Gabapentin inhibits high-threshold calcium channel currents in cultured rat dorsal root ganglion neurones. Br. J. Pharmacol., 135, 257-265.
49. SUZUKI, R., RAHMAN, W., RYGH, L.J., WEBBER, M., HUNT, S.P. & DICKENSON, A.H. (2005). Spinal-supraspinal serotonergic circuits regulating neuropathic pain and its treatment with gabapentin. Pain, 117, 292-303.
50. TANABE, M., SAKAUE, A., TAKASU, K., HONDA, M. & ONO, H. (2005b). Centrally mediated antihyperalgesic and antiallodynic effects of zonisamide following partial nerve injury in the mouse. Naunyn Schmiedebergs Arch. Pharmacol., 372, 107-114.
51. 2- adrenergic receptors in the effects of gabapentin on thermal and mechanical nociception after partial nerve injury in the mouse. Br. J. Pharmacol., 144, 703-714.
52. TAO, F., TAO, Y.X., MAO, P., ZHAO, C., LI, D., LIAW, W.J., RAJA, S.N. & JOHNS, R.A. (2003). Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience, 120, 847-854.
53. TAO, F., TAO, Y.X., ZHAO, C., DORE, S., LIAW, W.J., RAJA, S.N. & JOHNS, R.A. (2004). Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia. Neuroscience, 128, 421-430.
54. TEGEDER, I., DEL TURCO, D., SCHMIDTKO, A., SAUSBIER, M., FEIL, R., HOFMANN, F., DELLER, T., RUTH, P. & GEISSLINGER, G. (2004). Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc. Natl. Acad. Sci. U.S.A., 101, 3253-3257.
55. TEGEDER, I., SCHMIDTKO, A., NIEDERBERGER, E., RUTH, P. & GEISSLINGER, G. (2002). Dual effects of spinally delivered 8-bromo-cyclic guanosine mono-phosphate (8-bromo-cGMP) in formalin-induced nociception in rats. Neurosci. Lett., 332, 146-150.
56. TSENG, L.L. & TANG, R. (1989). Differential actions of the blockade of spinal opioid, adrenergic and serotonergic receptors on the tail-flick inhibition induced by morphine microinjected into dorsal raphe and central gray in rats. Neuroscience, 33, 93-100.
57. WIGDOR, S. & WILCOX, G.L. (1987). Central and systemic morphine-induced antinociception in mice: contribution of descending serotonergic and noradrenergic pathways. J. Pharmacol. Exp. Ther., 242, 90-95.
58. XU, Z., CHEN, S.R., EISENACH, J. & PAN, H.L. (2000). Role of spinal muscarinic and nicotinic receptors in clonidine-induced nitric oxide release in a rat model of neuropathic pain. Brain Res., 861, 390-398.
59. XU, Z., TONG, C., PAN, H.L., CERDA, S.E. & EISENACH, J.C. (1997). Intravenous morphine increases release of nitric oxide from spinal cord by an α-adrenergic and cholinergic mechanism. J. Neurophysiol., 78, 2072-2078.
60. YANG, L., ZHANG, F.X., HUANG, F., LU, Y.J., LI, G.D., BAO, L., XIAO, H.S. & ZHANG, X. (2004). Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur. J. Neurosci., 19, 871-883.
61. ZHUO, M. & GEBHART, G.F. (1990). Spinal cholinergic and monoaminergic receptors mediate descending inhibition from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Res., 535, 67-78.
62. ZHUO, M. & GEBHART, G.F. (1991). Tonic cholinergic inhibition of spinal mechanical transmission. Pain, 46, 211-222.
63. ZHUO, M., MELLER, S.T. & GEBHART, G.F. (1993). Endogenous nitric oxide is required for tonic cholinergic inhibition of spinal mechanical transmission. Pain, 54, 71-78.