Differential roles of neurokinin 1 and neurokinin 2 receptors in the development and maintenance of heat hyperalgesia induced by acute inflammation

British Journal of Pharmacology

Volumn 120, Issue 7, 1997, Pages 1263-1273

  Sluka, K A ^a   Milton, M A ^a   Willis, W D ^a   Westlund, K N ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Arthritis; Dorsal horn; Inflammation; Joint; Microdialysis; Neurokinin A; Neurokinin receptors; Pain; Spinal cord; Substance P

Indexed keywords

3 (2 METHOXYBENZYLAMINO) 2 PHENYLPIPERIDINE; CARRAGEENAN; KAOLIN; NEUROKININ 1 RECEPTOR; NEUROKININ 2 RECEPTOR; SAREDUTANT; TACHYKININ RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DOSE RESPONSE; ETIOLOGY; HEAT; HYPERALGESIA; INFLAMMATION; KNEE; LATENT PERIOD; MALE; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; STEREOISOMERISM; TEMPERATURE; WEIGHT BEARING;

ANIMALS; ARTHRITIS; HEAT; HYPERALGESIA; MALE; MICRODIALYSIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; RECEPTORS, NEUROKININ-2;

EID: 0030890339     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0701044     Document Type: Article

References (75)

1. 2) receptor revisited with SR48968, a potent non-peptide antagonist. Biochem. Biophys. Res. Commun., 184, 1418-1424.
2. ATTAL, N., JAZAT, F., KAYSER, V. & GUILBAULD, G. (1990). Further evidence for 'pain-related' behaviors in a model of unilateral peripheral mononeuropathy. Pain, 41, 235-251.
3. BALUK, P., BERTRAND, C., GEPPETTI, P., MCDONALD, D.M. & NADEL, J.A. (1995). NK1 receptors mediate leukocyte adhesion in neurogenic inflammation in the rat trachea. Am. J. Physiol., 268, 263-269.
4. BARNES, P.J. (1992). Neurogenic inflammation and asthma. J. Asthma, 29, 165-180.
5. BETHEL, R.A., BROKAW, J.J., EVANS, T.W., NADEL, J.A. & MCDONALD, D.M. (1988). Substance P-induced increase in vascular permeability in the rat trachea does not depend on neutrophils or other components of circulating blood. Exp. Lung Res., 14, 769-779.
6. BOWKER, R.M., WESTLUND, K.N., SULLIVAN, M.C., WILBLR, J.F. & COULTER, J.D. (1983). Descending serotonergic, peptidergic and cholinergic pathways from the raphe nuclei: a multiple transmitter complex. Brain Res., 288, 33-48.
7. 3-tachykinin and μ-opioid receptors. Br. J. Pharmacol., 108, 24P.
8. BRAIN, S.D. & WILLIAMS, T.J. (1985). Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol., 86, 855-861.
9. COHEN, R.H. & PERL, L.R. (1990). Contributions of arachidonic acid derivatives and substance P to the sensitization of cutaneous nociceptors. J. Neurophysiol., 64, 457-464.
10. DOCHERTY, R.J. & SHAH, K. (1995). Non-specific block of voltage-dependent sodium and calcium channels in guinea-pig sensory neurones by (±) CP 96,345 and (±) CP99,994. Br. J. Pharmacol., 115, 118P.
11. DONALDSON, L.F., HARMAR, A.J., MCQUEEN, D.S. & SECKL, J.R. (1992). Increased expression of preprotachykinin, calcitonin gene-related peptide, but not vasoactive intestinal peptide messenger RNA in dorsal root ganglia during the development of adjuvant monoarthritis in the rat. Mol. Brain Res., 16, 143-149.
12. DOUGHERTY, P.M., PALECEK, J., PALECKOVA, V. & WILLIS, W.D. (1994). Neurokinin 1 and 2 antagonists attenuate the response and NK1 antagonists prevent the sensitization of primate spinothalamic tract neurons after intradermal capsaicin. J. Neurophysiol., 72, 1464-1475.
13. EMSON, P.C. (1979). Peptides as neurotransmitter candidates in the mammalian CNS. Prog. Neurobiol., 13, 61-116.
14. FLEETWOOD-WALKER, S.M., MITCHELL, R., HOPE, P.J., ELYASSIR, N., MOLONY, V. & BLADON, C.M. (1990). The involvement of neurokinin receptor subtypes in somatosensory processing in the superficial dorsal horn of the cat. Brain Res., 519, 169-182.
15. 2 receptors in mediating brief nociceptive inputs to rat dorsal horn (laminae II-V) neurons. Eur. J. Pharmacol., 242, 173-181.
16. FREEMAN, D.H.J. (1987). Applied Categorical Data Analysis, pp. 179-207. New York: Marcel Dekker.
17. GAMSE, R. & SARIA, A. (1986). Nociceptive behaviour after intrathecal injections of substance P, neurokinin A and calcitonin gene-related peptide in mice. Neurosci. Lett., 70, 143-147.
18. GARCES, Y.I., RABITO, S.F., MINSHALL, R.D. & SAGEN, J. (1994). Lack of potent antinociceptive activity by substance P antagonist CP-96,345 in the rat spinal cord. Life Sci., 52, 353-360.
19. GARRETT, C., CARRUETTE, A., FARDIN, V., MOUSSAOUI, S., MONTIER, F., PEYRONEL, J.-F. & LADURON, P.M. (1993). Antinociceptive properties and inhibition of neurogenic inflammation with potent SP antagonists belonging to perhydroisoindolones. Regul. Peptides, 46, 24-30.
20. G0IBSON, S.J., POLAK, J.M., BLOOM, S.R. & WALL, P.D. (1981). The distribution of nine peptides in rat spinal cord with special emphasis on the substantia gelatinosa and the area around the central canal. J. Comp. Neurol., 201, 65-79.
21. 7 11 in the pathogenesis of arthritis. Regul. Peptides, 46, 195-197.
22. 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.
23. HOPE, P.J., JARROTT, B., SCHAIBLE, H.-G., CLARKE, R.W. & DUGGAN, A.W. (1990). Release and spread of immunoreactive neurokinin A in the cat spinal cord in a model of acute arthritis. Brain, Res., 533, 292-299.
24. KENSHALO, D.R., J.R., LEONARD, R.B., CHUNG, J.M. & WILLIS, W.D. (1982). Facilitation of the responses of primate spinothalamic cells to cold and to tactile stimuli by noxious heating of the skin. Pain, 12, 141-152.
25. KHALIL, Z. & HELME, R.D. (1989). Sequence of events in substance P-mediated plasma extravasation in rat skin. Brain Res., 500, 256-262.
26. LAM, F.Y. & FERRELL, W.R. (1989a). Inhibition of carrageenan induced inflammation in the rat knee joint by substance P antagonists. An. Rheum. Dis., 48, 928-932.
27. LAM, F.Y. & FERRELL, W.R. (1989b). Capsaicin suppresses substance P-induced joint inflammation in the rat. Neurosci. Lett., 105, 155-158.
28. LAM, F.Y. & FERRELL, W.R. (1991). Specific neurokinin receptors mediate plasma extravasation in the rat knee joint. Br. J. Pharmacol., 103, 1263-1267.
29. LEVINE, J.D., CLARK, R., DEVOR, M., HELMS, C. MOSKOWITZ, M.A. & BASBAUM, A.I. (1984). Intraneuronal substance P contributes to the severity of experimental arthritis. Science, 226, 547-549.
30. 2+ channels. Eur. J. Pharmacol., 264, 113-115.
31. MA, Q.-P. & WOOLFE, C.J. (1995). Involvement of neurokinin receptors in the induction but not the maintenance of mechanical allodynia in rat flexor motoneurones. J. Physiol., 486, 769-777.
32. MARCOS, P., COVENAS, R., DELEON, M., NARVAEZ, J.A., TRAMU, G., AGUIRRE, J.A. & GONZALEZ-BARON, S. (1993). Neurokinin A-like immunoreactivity in the cat brainstem. Neuropeptides, 25, 105-114.
33. MCCARTHY, P.W. & LAWSON, S.N. (1989). Cell type and conductive velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience, 28, 745-753.
34. MCGILLIS, J.P., MITSUHASHI M. & PAYAN, D.G. (1990). Immunomodulation by tachykinin neuropeptides. Ann. New York Acad. Sci., 594, 85-94.
35. MCLEAN, S., GANONG, A., SEYMOUR, P.A., SNIDER, R.M., DESAI, M.C., ROSEN, I., BRYCE, D.K., LONGO, K.P., REYNOLDS, L.S., ROBINSON, C., SCHMIDT, A.W., SIOK, C. & HEYM, J. (1993). Pharmacology of CP-99,994; a nonpeptide antagonist of the tachykinin 1 neurokinin-1 receptor. J. Pharmacol. Exp. Ther., 267, 472-479.
36. MINAMI, M., KURAISHI, Y., KAWAMURA, M., YAMAGUICHI, T., MASU, Y., NAKANISHI, S. & SATOH, M. (1989). Enhancement of preprotachykinin A gene expression by adjuvant-induced inflammation of substance P-containing spinal neurons in nociception. Neurosci. Lett., 98, 105-110.
37. MUNRO, F.E., FLEETWOOD-WALKFR, S.M., PARKER, R.M. & MITCHELL. R. (1993). The effects of neurokinin receptor antagonists on mustard oil-evoked activation of rat dorsal horn neurons. Neuropeptides, 25, 299-305.
38. NAGAHISA, A., KANAI, Y., SUGA, O., TANIGUCHI, K., TSUCHIYA, M., LOWE III, J.A. & HESS, H.-J. (1992). Antiinflammatory and analgesic activity of a non-peptide substance P receptor antagonist. Eur. J. Pharmacol., 217, 191-195.
39. 3H]MK-801. after intrathecai injection in mice. Pharmacol. Biochem. Behav., 44, 9-15.
40. NEUGEBAUER, V., WEIRETTER, K. & SCHAIBLE, H.-G. (1995). Involvement of substance P and neurokinin-1 receptors in the hyperexcitability of dorsal horn neurons during development of acute arthritis in rat's knee joint. J. Neurophysiol., 73, 1574-1583.
41. NOGUCTHI, K. & RUDA, M.A. (1992). Gene regulation in an ascending nociceptive pathway: inflammation-induced increase in preprotachykinin messenger RNA in rat lamina I spinal projection neurons. J. Neurosci., 12, 2563-2572.
42. OGAWA, T., KANAZAWA, I. & KIMURA, S. (1985). Regional distribution of substance P, neurokinin A, neurokinin B in rat spinal cord, nerve roots and dorsal root ganglia, and the effects of dorsal root or spinal transection. Brain Res., 359, 152-157.
43. 2 receptors in spinal nociceptive reflex in the rat. Eur. J. Pharmacol., 232, 255-261.
44. PONCELET, M., GUEDET, C., EMONDS-ALT, X., BRELIERE, J.C., LEFUR, G. & SOUBRIE, P. (1993). Turning behaviour induced in mice by a neurokinin A receptor agonist: stereoselective blockade of SR 48968, a non-peptide receptor antagonist. Neurosci. Lett., 149, 40-42.
45. RADHAKRISHNAN, V. & HENRY, J.L. (1991). Novel substance P antagonist, CP-96345, blocks responses of cat spinal dorsal horn neurons to noxious cutaneous stimulation and substance P. Neurosci. Lett., 132, 39-43.
46. RADHAKRISHNAN, V. & HENRY, J.L. (1995). Antagonism of nociceptive responses of cat spinal dorsal horn neurons in vivo by the NK-1 receptor antagonists CP-96,345 and CP-99,994, but not by CP-96,344. Neuroscience, 64, 943-958.
47. REES, H., SLUKA, K.A., TSURUOKA, M., CHEN, P.S. & WILLIS, W.D. (1995). The effects of NK1 and NK2 receptor antagonists on the sensitization of STT cells following acute inflammation in the anaesthetized primate. J. Physiol., 483P, 152P.
48. SAKURADA, T., KATSUMATA, K., YOGO, H., TAN-NO, K., SAKURADA, S. & KISARA, K. (1993). Antinociceplion induced by CP 96,345, a non-peptide NK-1 receptor antagonist, in the mouse formalin and capsaicin tests. Neurosci. Lett.,151,142-145.
49. SCHAFER, M.K.-H., NOHR, D., KRAUSE, J.E. & WEIHE, E. (1993). Inflammation-induced upregulation of NK1 receptor mRNA in dorsal horn neurons. NeuroReport, 4, 1007-1010.
50. SCHAIBLE, H.-G. & GRUBB, B.D. (1993). Afferent and spinal mechanisms of joint pain. Pain, 55, 5-54.
51. SCHAIBLE, H.-G., JARROTT, B., HOPE, P.J. & DUGGAN, A.W. (1990). Release of immunoreactive substance P in the spinal cord during development of acute arthritis in the knee joint of the cat: a study with antibody microprobes. Brain Res., 529, 214-223.
52. SCOTT, D.T., LAM, F.Y. & FERRELL., W.R. (1992). Acute-inflammation enhances substance P-induced plasma-protein extravasation in the rat knee-joint. Regul. Peptides. 39, 227-235.
53. 2 receptor antagonists: a comparison to other classes of antinociceptive agent. Pain, 61, 325-343.
54. SIMONE, D.A., SORKIN, L.S., OH, U.T., CHUNG, J.M., OWENS, C., LAMOTTE, R.H. & WILLIS, W.D. (1991). Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J. Neurophysiol., 66, 228-246.
55. SKILLING, S.R., SMULLIN, D.H., BEITZ, A.J. & LARSON, A.A. (1988). Extracellular amino acid concentration in dorsal spinal cord of freely moving rats following veratradine and nociceptive stimulation. J. Neurochem., 51, 127-132.
56. SLUKA, K.A., DOUGHERTY, P.M., SORKIN, L.S., WILLIS, W.D. & WESTLUND, K.N. (1992). Neural changes in acute arthritis in monkeys. III. Changes in substance-P,calcitonin gene-related peptide and glutamate in the dorsal horn of the spinal-cord. Brain Res., 17, 29-38.
57. SLUKA, K.A., MILTON, M.A., WESTLUND, K.N. & WILLIS, W.D. (1995). Involvement of neurokinin receptors in the joint inflammation and heat hyperalgesia following acute inflammation in unanaesthetized rats. J. Physiol., 483P, 152P-153P.
58. SLUKA, K.A. & WESTLUND, K.N. (1992). An experimental arthritis in rats: dorsal horn aspartate and glutamate increases. Neurosci. Lett., 145, 141-144.
59. SLUKA, K.A. & WESTLUND, K.N. (1993a). Behavioral and immunohistochemical changes in an experimental arthritis model in rats. Pain, 55, 367-377.
60. SLUKA, K.A. & WESTLUND, K.N. (1993b). Spinal cord amino acid release and content in an arthritis model - the effects of pretreatment with non-NMDA. NMDA, and NK1 receptor antagonists, Brain Res., 627, 89-103.
61. SLUKA, K.A. & WESTLUND, K.N. (1993c). Centrally administered non-NMDA but not NMDA receptor antagonists block peripheral knee joint inflammation. Pain, 55, 217-255.
62. SLUKA, K.A., WILLIS, W.O. & WESTLUND, K.S. (1993). Joint inflammation and hyperalgesia are reduced by spinal bicuculline. NeuroReport, 5, 109-112.
63. SMITH, G.D., HARMAR, A.J., MCQUEEN, D.S. & SECKL, J.R. (1992). Increase in substance-P and CGRP, but not somatostatin content of innervating dorsal-root ganglia in adjuvant monoarthritis in the rat. Neurosci. Lett., 137, 257-260.
64. STEINBERG, R., RODIER, D., SOURDHAC, J., BOUGAULT, L, EMONDS-ALT, X., SOUBRIE, P. & LEFUR, G. (1995) Pharmacological characterization of tachykinin receptors containing acetylcholine release from rat striatum: an in vivo microdialysis study. J. Neurochem., 65, 2543-2548.
65. TOREBJÖRK, H.E., LUNDBERG, L.E.R. & LAMOTTE, R.H. (1992). Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J. Physiol., 448, 765-780.
66. VASKO, M.R., CAMPBELL, W.B. & WAITE, K.J. (1994). Prostaglandin E2 enhances bradykinin stimulated release of neuropeptides from rat sensory neurons in culture. J. Neurosci., 14, 4987-4997.
67. WEIHE, E., NOHR, O., MILLAN, M.J., STEIN, C., MULLER, S., GRAMSCH, C. & HERZ. A. (1988). Peptide neuroanatomy of adjuvant-induced arthritis inflammation in rat. Agents Actions, 25, 255-259.
68. WOOLF, C.J. (1983). Evidence for a central component of post-injury pain hypersensitivity. Nature, 306, 686-688.
69. YAMAMOTO, T., SHIMOYAMA, N. & MIZUGUCHI, T. (1993a). Effects of FKK224, a novel cyclopeptide NK1 and NK2 antagonist, and CP-96,345, a nonpeptide NK1 antagonist, on development and maintenance of thermal hyperesthesia evoked by carrageenan injection in the rat paw. Anethesiology, 79, 1042-1050.
70. YAMAMOTO, T., SHIMOYAMA, N. & MIZUGUCHI, T. (1993b). Effects of intrathecal FK888, a novel dipeptide NK1 receptor antagonist, on the formalin test in the rat. Neurosci. Lett., 161, 57-39.
71. YAMAMOTO, T. & YAKSH, T.L. (1991). Stereospecific effects of a nonpeptidergic NK1 selective antagonist. CP-96,345: antinociception in the absence of motor dysfunction. Life Sci., 49, 1955-1963.
72. YASHPAL, K. & HENRY, J.L. (1984). Substance P analogue blocks SP-induced facilitation of a spinal nociceptive reflex. Brain Res. Bull., 13, 597-600.
73. YASHPAL, K., PITCHER, G.M. & HENRY, J.L. (1995). Noxious peripheral stimulation produces antinociception mediated via substance P and opioid mechanisms in the rat tail-flick test. Brain Res., 674, 97-103.
74. YASHPAL, K., RADHAKRISHNAN, V., CODERRE, T.J. & HENRY, J.L. (1993). CP-96,345, but not its stereoisomer, CP,96,344, blocks the nociceptive responses to intrathecally administered substance P and to noxious thermal and chemical stimuli in the rat. Neurosci., 52, 1039-1047.
75. YASHPAL, K., WRIGHT, D.M. & HENRY, J.L. (1982). Substance P reduces tail-flick latency: implications for chronic pain syndromes. Pain, 14, 155-167.