The inhibition of nitric oxide-activated poly(ADP-ribose) synthetase attenuates transsynaptic alteration of spinal cord dorsal horn neurons and neuropathic pain in the rat

Pain

Volumn 72, Issue 3, 1997, Pages 355-366

  Mao, Jianren ^a   Price, Donald D ^a   Zhu, Jeipei ^a   Lu, Juan ^a   Mayer, David J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Benzamide; Nerve injury; Neuropathic pain; Nitric oxide; Poly(ADP ribose) synthetase; Transsynaptic degeneration

Indexed keywords

BENZAMIDE; BENZOIC ACID; N(G) NITROARGININE METHYL ESTER; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRIC OXIDE; NOVOBIOCIN; SODIUM CHLORIDE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DOSE RESPONSE; HYPERALGESIA; INTRATHECAL DRUG ADMINISTRATION; MALE; NERVE LIGATION; NEUROPATHY; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL CORD DORSAL HORN;

ADP RIBOSE TRANSFERASES; ANIMALS; BENZAMIDES; ENZYME ACTIVATION; ENZYME INHIBITORS; HYPERALGESIA; MALE; NERVOUS SYSTEM DISEASES; NEURONS; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; PAIN; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SYNAPSES;

EID: 0030821492     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-3959(97)00063-8     Document Type: Article

References (59)

1. Alkon, D.L. and Rasmussen, H., A spatial-temporal model of cell activation, Science, 239 (1988) 998-1005.
2. Bennett, G.J. and Xie, Y.K., A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man, Pain, 33 (1988) 87-107.
3. Bennett, G.J., Hayashi, H., Abdelmoumene, M. and Dubner, R., Physiological properties of staked cells of substantial gelatinosa intracellularly stained with horseradish peroxidase, Brain Res., 164 (1979) 285-289.
4. Bennett, G.J., Abdelmoumene, M., Hayashi, H. and Dubner, R., Physiology and morphology of substantial gelatinosa neurons intracellularly stained with horseradish peroxidase, J. Comp. Neurol., 194 (1980) 809-827.
5. Bennett, G.J., Kajander, K.C., Sahara, Y., Iadarola, M.J. and Sugimoto, T., Neurochemical and anatomical changes in the dorsal horn of rats with an experimental painful peripheral neuropathy. In: F. Cervero, G.J. Bennett and P.M. Headley (Eds.), Proceedings of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord, Plenum Press, New York, 1989, pp. 463-471.
6. Bonica, J.J., Causalgia and other reflex sympathetic dystrophies. In: J.J. Bonica, J.C. Liebeskind and D.G. Albe-Fessard (Eds.), Advances in Pain Research and Therapy, 3rd Edn, Raven Press, New York, 1979, pp. 141-166.
7. Bredt, D. and Snyder, S.H., Nitric oxide, a novel neuronal messenger, Neuron, 8 (1992) 3-11.
8. Collingridge, G.L. and Singer, W., Excitatory amino acid receptors and synaptic plasticity, Trends Pharmacol. Sci., 11 (1990) 290-296.
9. Cosi, C., Suzuki, H., Milani, D., Facci, L., Menegazzi, M., Vantini, G., Kanai, Y. and Skaper, S.D., Poly(ADP-ribose) polymerase: early involvement in glutamate-induced neurotoxicity in cultured cerebellar granule cells, J. Neurosci. Res., 39 (1994) 38-46.
10. Davar, G., Hama, A., Deykin, A., Vos, B. and Maciewicz, R., MK-801 blocks the development of thermal hyperalgesia in a rat model of experimental painful neuropathy, Brain Res., 553 (1991) 327-330.
11. Favaron, M., Manev, H., Alho, H., Bertolino, M., Ferret, B., Guidotti, A. and Costa, E., Gangliosides prevent glutamate neurotoxicity in neuronal cultures, Proc. Natl. Acad. Sci. USA, 85 (1988) 7351-7355.
12. Gobel, S., Falls, W.M., Bennett, G.J., Abdelmoumene, M., Hayashi, H. and Humphery, E., An EM analysis of the synaptic connections of horseradish peroxidase-filled stalked cells and islet cells in the substantial gelatinosa of the adult cat spinal cord, J. Comp. Neurol., 194 (1980) 781-807.
13. Hama, A.T., Sagen, J. and Pappas, G.D., Spinal neurons in rats with unilateral constriction nerve injury: a preliminary study, Neurol. Res., 16 (1994) 297-304.
14. Hargreaves, K., Dubner, R., Brown, F., Flores, C. and Jones, J., A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia, Pain, 32 (1988) 77-88.
15. Kaczmarek, L.K., The role of protein kinase C in the regulation of ion channels and neurotransmitter release, Trends Neurosci., 10 (1987) 30-34.
16. Kajander, K.C., Wakisaka, S., Driasci, G. and Iadarola, M.J., Labeling of Fos protein increases in an experimental model of peripheral neuropathy in the rat, Soc. Neurosci. Abs., 16 (1990) 1281.
17. Kajander, K.C., Wakisaka, S. and Bennett, G.J., Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat, Neurosci. Lett., 138 (1992) 225-228.
18. Kajander, K.C. and Xu, J.X., Quantitative evaluation of calcitonin gene-related peptide and substance P levels in rat spinal cord following peripheral nerve injury, Neurosci. Lett., 186 (1995) 84-88.
19. Laird, J.M.A. and Bennett, G.J., An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy, J. Neurophysiol., 69 (1993) 2071-2085.
20. Madison, D.V., Malenka, R.C. and Nicoll, R.A., Mechanisms underlying long-term potentiation of synaptic transmission, Annu. Rev. Neurosci., 14 (1991) 379-397.
21. Mao, J., Mayer, D.J., Hayes, R.L., Lu, J. and Price, D.D., Differential roles of NMDA and non-NMDA receptor activation in induction and maintenance of thermal hyperalgesia in rats with painful peripheral mononeuropathy, Brain Res., 598 (1992a) 271-278.
22. Mao, J., Price, D.D., Coghill, R.C., Mayer, D.J. and Hayes, R.L., Spatial patterns of spinal cord 14C-2-deoxyglucose metabolic activity in a rat model of painful peripheral mononeuropathy, Pain, 50 (1992b) 89-100.
23. Mao, J., Price, D.D., Hayes, R.L., Lu, J. and Mayer, D.J., Intrathecal GM1 ganglioside and local nerve anesthesia reduce nociceptive behaviors in rats with experimental peripheral mononeuropathy, Brain Res., 584 (1992c) 28-35.
24. Mao, J., Price, D.D., Mayer, D.J. and Hayes, R.L., Pain-related increases in spinal cord membrane-bound protein kinase C following peripheral nerve injury, Brain Res., 588 (1992d) 144-149.
25. Mao, J., Price, D.D., Mayer, D.J., Lu, J. and Hayes, R.L., Intrathecal MK-801 and local nerve anesthesia synergistically reduce nociceptive behaviors in rats with experimental peripheral mononeuropathy, Brain Res., 576 (1992e) 254-262.
26. Mao, J., Mayer, D.J., Hayes, R.L. and Price, D.D., Spatial patterns of increased spinal cord membrane-bound protein kinase C and their relation to increases in 14C-2-deoxyglucose metabolic activity in rats with painful peripheral mononeuropathy, J. Neurophysiol., 70 (1993a) 470-481.
27. Mao, J., Price, D.D., Hayes, R.L., Lu, J., Mayer, D.J. and Frenk, H., Intrathecal treatment with dextrorphan or ketamine potently reduces pain-related behaviors in a rat model of peripheral mononeuropathy, Brain Res., 605 (1993b) 164-168.
28. Mao, J., Price, D.D. and Mayer, D.J., Mechanisms of hyperalgesia and opiate tolerance: a current view of their possible interactions, Pain, 62 (1995a) 259-274.
29. Mao, J., Price, D.D., Phillips, L.L., Lu, J. and Mayer, D.J., Increases in protein kinase C gamma immunoreactivity in the spinal cord dorsal horn of rats with painful peripheral mononeuropathy, Neurosci. Lett., 198 (1995b) 75-78.
30. 2+ in mammalian neurons, Trends Pharmacol. Sci., 11 (1990) 254-260.
31. Meller, S.T., Pechman, P.S., Gebhart, G.F. and Maves, T.J., Nitric oxide mediates the thermal hyperalgesia produced in a rat model of neuropathic pain in the rat, Neuroscience, 50 (1992) 7-10.
32. Molander, C., Xu, Q. and Grant, G., The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord, J. Comp. Neurol., 230 (1984) 133-141.
33. Moncada, C., Lekieffre, D., Arvin, B. and Meldrum, B., Effect of NO synthase inhibition on NMDA- and ischaemia- induced hippocampal lesions, NeuroReport, 3 (1992) 530-532.
34. Nishizuka, Y., The family of protein kinase C for signal transduction, J. Am. Med. Assoc., 262 (1989) 1826-1833.
35. Numann, R., Catterall, W.A. and Scheuer, T., Functional modulation of brain sodium channels by protein kinase C phosphorylation, Science, 254 (1991) 115-118.
36. Olds, J.L., Anderson, M.L., McPhie, D.L., Ataten, L.D. and Alkon, D.L., Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus, Science, 245 (1989) 866-869.
37. Palecek, J., Paleckova, V., Dougherty, P.M., Carlton, S.M. and Willis, W.D., Responses of spinothalamic tract cells to mechanical and thermal stimulation of skin in rats with experimental peripheral neuropathy, J. Neurophysiol., 67 (1992) 1562-1573.
38. Price, D.D., Hayashi, H., Dubner, R. and Ruda, M.A., Functional relationships between neurons of marginal and substantia gelatinosa layers of primate dorsal horn, J. Neurophysiol., 42 (1979) 1590-1608.
39. Price, D.D., Psychological and Neural Mechanisms of Pain, Raven Press, New York, 1988.
40. Price, D.D., Bennett, G.J. and Rafii, A., Psychophysical observations on patients with neuropathic pain relieved by a sympathetic block, Pain, 36 (1989) 273-288.
41. Price, D.D., Mao, J., Coghill, R.C., d'Avella, D., Cicciarello, R., Fiori, M., Mayer, D.J. and Hayes, R.L., Regional changes in spinal cord glucose metabolism in a rat model of painful neuropathy, Brain Res., 564 (1991) 314-318.
42. Price, D.D., Long, S. and Huitt, C., Sensory testing of pathophysiological mechanisms of pain in patients with reflex sympathetic dystrophy, Pain, 49 (1992) 163-174.
43. Raaphorst, G.P. and Azzam, E.I., Poly(ADP-ribose) synthetase inhibitors increase radiation and thermal sensitivity but do not affect thermotolerance, Radiat. Res., 116 (1988) 442-452.
44. Rankin, P.W., Jacobson, E.L., Benjamin, R.C., Moss, J. and Jacobson, M.K., Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo, J. Biol. Chem., 264 (1989) 4312-4317.
45. Seltzer, Z., Cohn, S., Ginzgurg, R. and Berlin, B., Modulation of neuropathic pain behavior in rats by spinal disinhibition and NMDA receptor blockade of injury discharge, Pain, 45 (1991) 69-75.
46. Stevens, C.W., Kajander, K.C., Bennett, G.J. and Seybold, V.S., Bilateral and differential changes in spinal cord mu, delta and kappa opioid binding in rats with a painful, unilateral neuropathy, Pain, 46 (1991) 315-326.
47. Sugimoto, T., Bennett, G.J. and Kajander, K.C., Strychnine-enhanced transsynaptic degeneration of dorsal horn neurons in rats with an experimental painful peripheral neuropathy, Neurosci. Lett., 98 (1989) 139-143.
48. Sugimoto, T., Bennett, G.J. and Kajander, K.C., Trans-synaptic degeneration in the superficial dorsal horn after sciatic nerve injury: effects of a chronic constriction injury, transection, and strychnine, Pain, 42 (1990) 205-213.
49. Tal, M. and Bennett, G.J., Dextrorphan relieves neuropathic heat-evoked hyperalgesia in the rat, Neurosci. Lett., 151 (1993) 107-110.
50. Tal, M. and Bennett, G.J., Neuropathic pain sensations are differentially sensitive to dextrorphan, NeuroReport, 5 (1994a) 1438-1440.
51. Tal, M. and Bennett, G.J., Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve, Pain, 57 (1994b) 275-282.
52. Thomas, P.K., Clinical features and differential diagnosis of peripheral neuropathy. In: P.J. Dyck, P.K. Thomas, E.H. Lambert and R. Bunge (Eds.), Peripheral Neuropathy, 2nd Edn., W.B. Saunders Company, Philadelphia, 1984, pp. 1169-1190.
53. Vaccarino, F., Guidotti, A. and Costa, E., Ganglioside inhibition of glutamate-mediated protein kinase C translocation in primary cultures of cerebellar neurons, Proc. Natl. Acad. Sci. USA, 34 (1987) 8707.
54. Wallis, R.A., Panizzon, K. and Wasterlain, C.G., Inhibition of nitric oxide synthase protects against hypoxic neuronal injury, NeuroReport, 3 (1992) 645-648.
55. + channel required for modulation by protein kinase C, Science, 254 (1991) 866-868.
56. Willis, W.D., The Pain System, Karger, New York, 1985.
57. Yamamoto, T. and Yaksh, T.L., Spinal pharmacology of thermal hyperalgesia induced by constriction injury of sciatic nerve. Excitatory amino acid antagonists, Pain, 49 (1992) 121-128.
58. Yamamoto, T. and Yaksh, T.L., Effects of intrathecal strychnine and bicuculline on nerve compression-induced thermal hyperalgesia and selective antagonism by MK-801, Pain, 54 (1993) 79-84.
59. Zhang, J., Dawson, V.L., Dawson, T.M. and Snyder, S.H., Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity, Science, 263 (1994) 687-689.