Nitric oxide mediates the central sensitization of primate spinothalamic tract neurons

Journal of Neurophysiology

Volumn 81, Issue 3, 1999, Pages 1075-1085

  Lin, Qing ^a   Paleček, Jiri ^a,b   Palečková, Veronika ^a,c   Peng, Yuan Bo ^a,d   Wu, Jing ^a   Cui, Minglei ^a   Willis, William D ^a,e  

^a University of Texas Medical Branch School of Medicine   (United States)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 NITROINDAZOLE; ARGININE METHYL ESTER; CAPSAICIN; CYCLIC GMP; LINSIDOMINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; HYPERALGESIA; INFLAMMATION; MALE; MECHANICAL STIMULATION; MONKEY; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINOTHALAMIC TRACT; TISSUE INJURY;

EID: 0344848556     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.3.1075     Document Type: Article

References (92)

1. ANDERSON, C. R., EDWARDS, S. L., FURNESS, J. B., BREDT, D. S., AND SNYDER, S. H. The distribution of nitric oxide synthase-containing antonomic preganglionic terminals in the rat. Brain Res. 614: 78-85, 1993.
2. BAUMANN, T. K., SIMONE, D. A., SHAIN, C. N., AND LAMOTTE, R. H. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J. Neurophysiol. 66: 212-227, 1991.
3. BENVENISTE, H., HANSEN, A. J., AND OTTOSEN, N. S. Determination of brain interstitial concentrations by microdialysis. J. Neurochem. 52: 1741-1750, 1989.
4. BERNARDI, P. S., VALTSCHANOFF, J. G., WEINBERG, R. J., SCHMIDT, H.H.H.W., AND RUSTIONI, A. Synaptic interactions between primary afferent terminals and GABA and nitric oxide-synthesizing neurons in superficial laminae of the rat spinal cord. J. Neurosci. 15: 1363-1371, 1995.
5. BREDT, D. S. AND SNYDER, S. H. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. USA 86: 9030-9033, 1989.
6. BREDT, D. S. AND SNYDER, S. H. Isolation of nitric oxide synthase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87: 682-685, 1990.
7. BREDT, D. S. AND SNYDER, S. H. Nitric oxide, a novel neuronal messenger. Neuron 8: 3-11, 1992.
8. BUDAI, D., WILCOX, G. L., AND LARSON, A. A. Effects of nitric oxide availability on responses of spinal wide dynamic range neurons to excitatory amino acids. Eur. J. Pharmacol. 278: 39-47, 1995.
9. CHUNG, J. M., SURMEIER, D. J., LEE, K. H., SORKIN, L. S., HONDA, C. N., TSONG, Y., AND WILLIS, W. D. Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis. J. Neurophysiol. 56: 308-327, 1986.
10. CODERRE, T. J. AND YASHPAL, K. Intracellular messengers contributing to persistent nociception and hyperalgesia induced by L-glutamate and substance P in the rat formalin pain model. Eur. J. Pharmacol. 6: 1328-1334, 1994.
11. CUDEIRO, J., RIVADULLA, C., RODRIGUEZ, R., MARTINEZ-CONDE, S., ACUNA, C., AND ALONSO, J. M. Modulatory influence of putative inhibitors of nitric oxide synthase on visual processing in the cat lateral geniculate nucleus. J. Neurophysiol 71: 146-149, 1994.
12. DAVIES, S. N. AND LODGE, D. Evidence for involvement of N-methylaspartate receptors in "wind-up" of class 2 neurones in the dorsal horn of the rat. Brain Res. 424: 402-406, 1987.
13. DOUGHERTY, P. M., PALEČEK, J., PALEČKOVÁ, V., AND WILLIS, W. D. The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract neurons by mechanical, chemical, thermal, and electrical stimuli. J. Neurosci. 12: 3025-3041, 1992a.
14. DOUGHERTY, P. M., PALEČEK, J., PALEČKOVÁ, V., AND WILLIS, W. D. Neurokinin 1 and 2 antagonists attenuate the responses and NK1 antagonists prevent the sensitization of primate spinothalamic tract neurons after intradermal capsaicin. J. Neurophysiol. 72: 1464-1475, 1994.
15. DOUGHERTY, P. M., PALEČEK, J., ZORN, S., AND WILLIS, W. D. Combined application of excitatory amino acids and substance P produces long-lasting changes in responses of primate spinothalamic tract neurons. Brain Res. Rev. 18: 227-246, 1993.
16. DOUGHERTY, P. M., SLUKA, K. A., SORKIN, L. S., WESTLUND, K. N., AND WILLIS, W. D. Neural changes in acute arthritis in monkeys. I. Parallel enhancement of responses of spinothalamic tract neurons to mechanical stimulation and excitatory amino acids. Brain Res. Rev. 17: 1-13, 1992b.
17. DOUGHERTY, P. M. AND WILLIS, W. D. Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined microiontophoretic application of N-methyl-D-aspartic acid and substance P. Pain 47: 85-93, 1991.
18. DOUGHERTY, P. M. AND WILLIS, W. D. Enhanced responses of spinothalamic tract neurons to excitatory amino acids accompany capsaicin-induced sensitization in the monkey. J. Neurosci. 12: 883-894, 1992.
19. DUN, N. J., DUN, S. L., FORSTERMANN, U., AND TSENG, L. F. Nitric oxide synthase immunoreactivity in rat spinal cord. Neurosci. Lett. 147: 217-220, 1992.
20. G-nitroarginine inhibits NMDA-induced cyclic GMP formation in rat cerebellum. Eur. J. Pharmacol. 184: 311-313, 1990.
21. FERRINGTON, D. G., SORKIN, L. S., AND WILLIS, W. D. Responses of spinothalamic tract cells in the superficial dorsal horn of the primate lumbar spinal cord. J. Physiol. (Lond.) 388: 681-703, 1987.
22. GAMSE, R., MOLNAR, A., AND LEMBECK, F. Substance P release from spinal cord slices by capsaicin. Life Sci. 25: 629-636, 1979.
23. GARTHWAITE, J. AND BALAZS, R. Supersensitivity to the cyclic GMP response to glutamate during cerebellar maturation. Nature 275: 328-329, 1978.
24. GARTHWAITE, J., CHARLES, S. L., AND CHESS-WILLIAMS, R. Endothelium-derived relaxing factors released on activation of NMDA receptors suggests role as intracellular messenger in the brain. Nature 336: 385-388, 1988.
25. GARTHWAITE, J., SOUTHAM, E., AND ANDERTON, M. A kainate receptor linked to nitric oxide synthesis from arginine. J. Neurochem. 53: 1952-1954, 1989.
26. HALEY, J. E., DICKENSON, A. H., AND SCHACHTER, M. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology 31: 251-258, 1992.
27. HALEY, J. E., SULLIVAN, A. F., AND DICKENSON, A. H. Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518: 218-226, 1990. 251-258, 1992.
28. HALEY, J. E., SULLIVAN, A. F., AND DICKENSON, A. H. Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518: 218-226, 1990. 251-258, 1992.
29. HÖKFELT, T., KELLERTH, J. O., NILSSON, G., AND PERNOW, B. Substance P: localization in the central nervous system and in some primary sensory neurons. Science 190: 889-890, 1975.
30. HUANG, P. L., DAWSON, T. M., BREDT, D. S., SNYDER, S. H., AND FISHMAN, M. C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75: 1273-1286, 1993.
31. INOUE, T., MASHIMO, T., SHIBATA, M., SHIBUTA, S., AND YOSHIYA, I. 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, 1998.
32. KITTO, K. F., HALEY, J. E., AND WILCOX, G. L. Involvement of nitric oxide in spinally mediated hyperalgesia in the mouse. Neurosci. Lett. 148: 1-5, 1992.
33. KNOWLES, R. G., PALACIOS, M., PALMER, R. M., AND MONCADA, S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA 86: 5159-5162, 1989.
34. LAM, H. H., HANLEY, D. F., TRAPP, B. D., SAITO, S., RAJA, S., DAWSON, T. M., AND YAMAGUCHI, H. Induction of spinal cord neuronal nitric oxide synthase (NOS) after formalin injection in the rat hind paw. Neurosci. Lett. 210: 201-204, 1996.
35. LEE, J.-H., PRICE, R. H., WILLIAMS, F. G., MAYER, B., AND BEITZ, A. J. Nitric oxide synthase is found in some spinothalamic neurons and in neuronal processes that appose spinal neurons that express Fos induced by noxious stimulation. Brain Res. 608: 324-333, 1993.
36. LEE, J. H., WILCOX, G. L., AND BEITZ, A. J. Nitric oxide mediates Fos expression in the spinal cord induced by mechanical noxious stimulation. Neuroreport 3: 841-844, 1992.
37. LI, J. AND IADECOLA, C. Nitric oxide and adenosine mediate vasodilation during functional activation in cerebellar cortex. Neuropharmacology 33: 1453-1462, 1994.
38. LIN, Q., PENG, Y. B., AND WILLIS, W. D. Possible role of protein kinase C in the sensitization of primate spinothalamic tract neurons. J. Neurosci, 16: 3026-3034, 1996a.
39. LIN, Q., PENG, Y. B., AND WILLIS, W. D. Inhibition of primate spinothalamic tract neurons by spinal glycine and GABA is reduced during central sensitization. J. Neurophysiol. 76: 1005-1014, 1996b.
40. LIN, Q., PENG, Y. B., WU, J., AND WILLIS, W. D. Role of nitric oxide-cGMP system in the sensitization of spinothalamic neurons after intradermal injection of capsaicin in primates. Soc. Neurosci. Abstr. 22: 1812, 1996c.
41. LIN, Q., PENG, Y. B., WU, J., AND WILLIS, W. D. Involvement of cGMP in nociceptive processing by and sensitization of spinothalamic neurons in primates. J. Neurosci. 17: 3293-3302, 1997.
42. LINCOLN, T. M., KOMALAVILAS, P., AND CORNWELL, T. L. Pleiotropic regulation of vascular smooth muscle tone by cyclic GMP-dependent protein kinase. Hypertension 23: 1141-1147, 1994.
43. LINDEN, D. J. Long-term synaptic depression in the mammalian brain. Neuron 12: 457-472, 1994.
44. MACDERMOTT, A. B. AND DALE, N. Receptors, ion channels, and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends Neurosci. 10: 280-284, 1987.
45. MACDERMOTT, A. B., MAYER, M. L., WESTBROOK, G. L., SMITH, S. J., AND BARKER, J. L. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature 321: 519-522, 1986.
46. MALMBERG, A. B. AND YAKSH, T. L. Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain 54: 291-300, 1993.
47. MANZONI, O.J.J., FINIELS-MARLIER, F., SASSETTI, I., BLOCKAERT, J., LE PEUCH, C., AND SLADECZEK, F.A.J. The glutamate receptor of the Qp-type activates protein kinase C and is regulated by protein kinase C. Neurosci. Lett. 109: 146-151, 1990.
48. MAYER, B., KLATT, P., WERNER, E. R., AND SCHMIDT, K. Molecular mechanisms of inhibition of porcine brain nitric oxide synthase by the antinociceptive drug 7-nitro-indazole. Neuropharmacology 33: 1253-1259, 1994.
49. MCNEILL, D. L., WESTLUND, K. N., AND COGGESHALL, R. E. Peptide immunoreactivity of unmyelinated primary afferent axons in rat lumbar dorsal roots. J. Histochem. Cytochem. 37: 1047-1052, 1989.
50. MELLER, S. T., CUMMINGS, C. P., TRAUB, R. J., AND GEBHART, G. F. The role of nitric oxide in the development and maintenance of the hyperalgesia produced by intraplantar injection of carrageenan in the rat. Neumscience 60: 367-374, 1994.
51. 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 re-flex. Eur. J. Pharmacol. 214: 93-96, 1992a.
52. MELLER, S. T. AND GEBHART, G. F. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136, 1993.
53. 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: 7-10, 1992b.
54. MOORE, P. K., BABBEDGE, R. C., WALLACE, P., GAFFEN, Z. A., AND HART, S. L. 7-Nitro indazole, an inhibitor of nitric oxide synthase, inhibits anti-nociceptive activity in the mouse without increasing blood pressure. Br. J. Pharmacol. 108: 296-297, 1993a.
55. G-nitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br. J. Pharmacol. 102: 198-202, 1991.
56. MOORE, P. K., WALLACE, P., GAFFES, Z. A., HART, S. L., AND BABBEDGE, R. C. Characterization of the novel nitric oxide synthase inhibitor 7-nitric indazole and related indazoles-antinociceptive and cardiovascular effects. Br. J. Pharmacol. 110: 219-224, 1993b.
57. NESTLER, E. J. AND GREENGARD, P. Protein phosphorylation in the brain. Nature 305: 583-588, 1983.
58. OHTA, K., ARAKI, N., SHIBATA, M., HAMADA. J., KOMATSUMOTO, S., SHIMAZU, K., AND FUKUUCHI. Y. A novel in vivo assay system for consecutive measurement of brain nitric oxide production combined with the microdi-alysis technique. Neurosci. Lett. 176: 165-168, 1994.
59. OWENS, C. M. Plastic Changes in the Responses of Primate Spinothalamic Neurons (PhD thesis). Galveston, TX: Univ. of Texas Medical Branch, 1991.
60. PALEČEK, J., PALEČKOVÁ, V., DOUGHERTY, P. M., AND WILLIS, W. D. The effect of phorbol esters on the responses of primate spinothalamic neurons to mechanical and thermal stimuli. J. Neurophysiol. 71: 529-537, 1994.
61. PALEČEK, J., PALEČKOVÁ, V., AND WILLIS, W. D. The role of nitric oxide in hyperalgesia induced by capsaicin injection in primates (Abstract). 7th World Congress on Pain, IASP, Paris, 1993, p. 226-227.
62. PEHL, U. AND SCHMID, H. A. Electrophysiological responses of neurons in the rat spinal cord to nitric oxide. Neuroscience 77: 563-573, 1997.
63. RADHAKRISHNAN, V. AND HENRY, J. L. L-NAME blocks responses to NMDA, substance P and noxious cutaneous stimuli in cat dorsal horn. Neuroreport 4: 323-326, 1993.
64. RADHAKRISHNAN, V., YASHPAL, K., HUI-CHAN, C. W., AND HENRY, J. L. Implication of a nitric oxide synthase mechanism in the action of substance P: L-NAME blocks thermal hyperalgesia induced by endogenous and exogenous substance P in the rat. Eur. J. Pharmacol. 7: 1920-1925, 1995.
65. REDEN, J. Molsidomine. Blood Vessels 27: 282-294, 1990.
66. REES, D. D., PALMER, R.M.J., SCHULZ, R., HODSON. H. F., AND MONCADA, S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br. J. Pharmacol. 101: 746-752, 1990.
67. 2+-independent nitric oxide synthases. FEBS Lett. 291: 145-149, 1991.
68. SEMOS, M. L. AND HEADLEY, P. M. The role of nitric oxide in spinal nociceptive reflexes in rats with neurogenic and non-neurogenic peripheral inflammation. Neuropharmacology 33: 1487-1497, 1994.
69. SHIBUKI, K. AND OKADA, D. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349: 326-328, 1991.
70. SILVA, M. T., ROSE, S., HINDMARSH, J. G., AISLAITNER, G., GORROD, J. W., MOORE, P. K., JENNER, P., AND MARSDEN, C. D. Increased striatal dopamine efflux in vivo following inhibition of cerebral nitric oxide synthase by the novel monosodium salt of 7-nitric indazole. Br. J. Pharmacol. 114: 257-258, 1995.
71. SIMONE, D. A., SORKIN, L. S., OH, U., CHUNG, J. M. OWENS, C., LAMOTTE, R. H., AND WILLIS, W. D. Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J. Neurophysiol. 66: 228-246, 1991.
72. SLUKA, K. A., WILLIS, W. D., AND WESTLUND, K. N. Joint inflammation and hyperalgesia are reduced by spinal bicuculline. Neuroreport 5: 109-112, 1993.
73. SORKIN, L. S. AND MCADOO, D. J. Amino acids and serotonin are released into the lumbar spinal cord of the anesthetized cat following intradermal capsaicin injection. Brain Res. 607: 89-98, 1993.
74. SORKIN, L. S., STEINMAN, J. L., HUGHES, M. G., WILLIS, W. D., AND MCADOO, D. J. Microdialysis recovery of serotonin released in spinal cord dorsal horn. J. Neurosci. Methods 23: 131-138, 1988.
75. SORKIN L. S., WESTLUND, K. N., SLUKA, K. A., DOUGHERTY, P. M., AND WILLIS, W. D. Neural changes in acute arthritis in monkeys. IV. Time course of amino acid release into the lumbar dorsal horn. Brain Res. Rev. 17: 39-50, 1992.
76. SOUTHAM, E., EAST, S. J., AND GARTHWAITE, J. Excitatory amino acid receptors coupled to the nitric oxide/cyclic GMP pathway in rat cerebellum during development. J. Neurochem. 56: 2072-2081, 1991.
77. SOUTHAM, E. AND GARTHWAITE, J. Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci. Lett. 130: 107-111, 1991.
78. SOYGUDER, Z., SCHMIDT, H.H.H.W., AND MORRIS, R. Postnatal development of nitric oxide synthase type 1 expression in the lumbar spinal cord of the rat: a comparison with the induction of c-fos in response to peripheral application of mustard oil. Neurosci. Lett. 180: 188-192, 1994.
79. STANFA, L. C., MISRA, C., AND DICKENSON, A. H. Amplification of spinal nociceptive transmission depends on the generation of nitric oxide in normal and carrageenan rats. Brain Res. 737: 92-98, 1996.
80. STEEL, J. H., TERENGHI, G., CHUNG, J. M., NA, H. S., AND POLAK, J. M. Increased nitric oxide synthase immunoreactivity in rat dorsal root ganglia in a neuropathic pain model. Neurosci. Lett. 169: 81-84, 1994.
81. TERENGHI, G., RIVEROS-MORENO, V., HUDSON, L. D., IBRAHIM, N. B., AND POLAK, J. M. Immunohistochemistry of nitric oxide synthase demonstrates immunoreactive neurons in spinal cord and dorsal root ganglia of human and rat. J. Neurol. Sci. 118: 34-37, 1993.
82. TREVINO, D. L., COULTER, J. D., AND WILLIS, W. D. Location of cells of origin of spinothalamic tract in lumbar enlargement of the monkey. J. Neurophysiol. 36: 750-761, 1973.
83. VALTSCHANOFF, J. G., WEINBERG, R. J., AND RUSTIONI, A. NADPH diaphorase in the spinal cord of rats. J. Comp. Neurol. 321: 209-222, 1992a.
84. VALTSCHANOFF, J. G., WEINBERG, R. J., RUSTIONI, A., AND SCHMIDT, H.H.H.W. Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord. Neurosci. Lett. 148: 6-10, 1992b.
85. VERGE, V. M., XU, Z., XU, X.-J., WIESENFELD-HALLIN, Z., AND HOKFELT, T. Marked increase in nitric oxide synthase mRNA in dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc. Natl. Acad. Sci. USA 89: 11617-11621, 1992.
86. VIZZARD, M. A., ERDMAN, S. L., AND DE GROAT, W. C. Increased expression of neuronal nitric oxide synthase in dorsal root ganglion neurons after systemic capsaicin administration. Neuroscience 67: 1-5, 1995.
87. WALL, P. D. Mechanisms of acute and chronic pain. In: Advances in Pain Research and Therapy, edited by L. Kruger and J. C. Liebeskind. New York: Raven, 1984, p. 95-104.
88. WILLIS, W. D. Electophysiological evidence for a role of altered discharges of spinothalamic tract neurons in hyperalgesia. In: Recent Advances in Neurology. Altered Sensation and Pain, edited by M. R. Dimitrijevic. Basel: Karger, 1990, p. 153-164.
89. WOOLF, C. J. Evidence for a central component of post-injury pain hypersensitivity. Nature 306: 686-688, 1983.
90. WU, J., LIN, Q., LU, Y., WILLIS, W. D., AND WESTLUND, K. N. Changes in nitric oxide synthase isoforms in the spinal cord of rat following induction of chronic arthritis. Exp. Brain Res. 118: 457-465, 1998a.
91. WU, J., LIN, Q., MCADOO, D. J., AND WILLIS, W. D. Nitric oxide contributes to central sensitization following intradermal injection of capsaicin. Neuroreport 9: 589-592, 1998b.
92. WU, W., LIUZZI, F. J., SCHINCO, F. P., DEPTO, A. S., LI, Y., MONG, J. A., DAWSON, T. M., AND SNYDER, S. H. Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 61: 719-726, 1994.