The spinal contribution of substance P to the generation and maintenance of inflammatory hyperalgesia in the rat

Pain

Volumn 67, Issue 1, 1996, Pages 151-161

  Traub, Richard J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Carrageenan; CP 96,345; Formalin; NK 1 receptor; Pain; Tachykinin

Indexed keywords

2 BENZHYDRYL 3 (2 METHOXYBENZYLAMINO) 1 AZABICYCLO[2.2.2]OCTANE; FORMALDEHYDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SUBSTANCE P; TACHYKININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ETIOLOGY; HYPERALGESIA; INFLAMMATION; INTRATHECAL DRUG ADMINISTRATION; MALE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT;

EID: 0030246892     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/0304-3959(96)03076-X     Document Type: Article

References (74)

1. Aloisi A.M., Pooro C.A., Cavazzuti M., Baraldi P., Carli G. Mirror pain in the formalin test: behavioral and 2-deoxyglucose studies. Pain. 55:1993;267-273.
2. Aloisi A.M., Albonetti M.E., Carli G. Behavioral effects of different intensities of formalin pain in rats. Physiol. Behav. 58:1995;603-610.
3. Berberich P., Hoheisel U., Mense S. Effects of a carrageenan-induced myositis on the discharge properties of group III and IV muscle receptors in the cat. J. Neurophysiol. 59:1988;1395-1409.
4. 1) receptors at sites of inflammation. Proc. Natl. Acad. Sci, USA. 91:1994;8964-8968.
5. Brown J.L., Liu H., Maggio J.E., Vigna S.R., Mantyh P.W., Basbaum A.I. Morphological characterization of substance P receptor-immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis. J. Comp. Neurol. 356:1995;327-344.
6. Chapman V., Dickenson A.H. The effect of intrathecal administration of RP67580, a potent neurokinin 1 antagonist on nociceptive transmission in the rat spinal cord. Neurosci. Lett. 157:1993;149-152.
7. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature. 356:1992;521-523.
8. 2 receptors in the rat spinal cord. Br. J. Pharmacol. 115:1995;1013-1019.
9. Coderre T.J., Melzack R. The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J. Neurosci. 12:1992;3665-3670.
10. Coderre T.J., Katz J., Vaccarino A.L., Melzack R. Contribution of central neuroplasticity to pathological pain: review of clinical experimental evidence. Pain. 52:1993;259-285.
11. Cumberbatch M.J., Chizh B.A., Headley P.M. Modulation of excitatory amino acid responses by tachykinins and selective tachykinin receptor agonists in the rat spinal cord. Br. J. Pharmacol. 115:1995;1005-1012.
12. De Koninck Y., Henry J.L. Substance P-mediated slow excitatory postsynaptic potential elicited in dorsal horn neurons in vivo by noxious stimulation. Proc. Natl. Acad. Sci. USA. 88:1991;11344-11348.
13. De Koninck Y., Ribeiro-Da-Silva A., Henry J.L., Cuello A.C. Spinal neurons exhibiting a specific nociceptive response receive abundant substance P-containing synaptic contacts. Proc. Natl. Acad. Sci. USA. 89:1992;5073-5077.
14. DeBiasi S., Rustioni A. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc. Natl. Acad. Sci. USA. 85:1988;7820-7824.
15. Dickenson A.H., Sullivan A.F. Subcutaneous formalin-induced activity of dorsal horn neurones in the rat: differential response to an intrathecal opiate administered pre or post formalin. Pain. 30:1987a;349-360.
16. Dickenson A.H., Sullivan A.F. Peripheral origins and central modulation of subcutaneous formalin-induced activity of rat dorsal horn neurones. Neurosci. Lett. 83:1987b;207-211.
17. Dougherty P.M., Palecek J., Paleckova V., Willis W.D. Infusion of substance P or neurokinin A by microdialysis alters responses of primate spinothalamic tract neurons to cutaneous stimuli and to iontophoretically released excitatory amino acids. Pain. 61:1995;411-425.
18. Dougherty P.M., Sluka K.A., Sorkin L.S., Westlund K.N., 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. 17:1992;1-13.
19. Dougherty P.M., Willis W.D. Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-D-aspartic acid and substance P. Pain. 47:1991;85-93.
20. Dubuisson D., Dennis S. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain. 4:1977;161-174.
21. Duggan A.W., MacMillan S.J.A., Mark M.A., Riley R.C., Schaible H.-G. Afferent volley patterns and the spinal release of immunoreactive substance P in the dorsal horn of the anaesthetized spinal cat. Neuroscience. 65:1995;849-858.
22. Eisenberg E., Vos B.P., Strassman A.M. The NMDA antagonist memantine blocks pain behavior in a rat model of formalin-induced facial pain. Pain. 54:1993;301-307.
23. Fisher N.D., Baranauskas G., Nistri A. Multiple types of tachykinin receptor medicate a slow excitation of rat spinal motorneurones in vitro. Neurosci. Lett. 165:1994;84-88.
24. Galeazza M.T., Garry M.G., Yost H.J., Strait K.A., Hargreaves K.M., Seybold V.S. Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neurosci. 66:1995;443-458.
25. Garces Y.I., Rabito S.F., Minshall R.D., Sagen J. Lack of potent antinociceptive activity by substance antagonist CP-96345 in the rat spinal cord. Life Sci. 52:1992;353-360.
26. Garrett N.E., Kidd B.L., Cruwys S.C., Tomlinson D.R. Changes in preprotachykinin mRNA expression and substance P levels in dorsal root ganglia of monoarthritic rats: comparison with changes in synovial substance P levels. Brain Res. 675:1995;203-207.
27. Garry M.G., Hargreaves K.M. Enhanced release of immunoreactive CGRP and substance P from spinal dorsal horn slices occurs during carrageenan inflammation. Brain Res. 582:1992;139-142.
28. Grady E.F., Garland A.M., Gamp P.D., Lovett M., Payan D.G., Bunnett N.W. Delineation of the endocytic pathway of substance P and its seven-transmembrane domain NK1 receptor. Mol. Biol. Cell. 6:1995;509-524.
29. Guard S., Boyle S.J., Tang K. -W., Watling K.J., McKnight A.T., Woodruff G.N. The interaction of the NK1 receptor antagonist CP-96345 with L-type calcium channels and its functional consequences. Br. J. Pharmacol. 110:1993;385-391.
30. Haley J.E., Sullivan A.F., Dickenson A.H. Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518:1990;218-226.
31. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 32:1988;77-88.
32. Holland L.N., Goldstein B.D. Examination of tonic nociceptive behavior using a method of substance P-receptor desensitization in the dorsal horn. Pain. 56:1994;339-346.
33. Holland L.N., Goldstein B.D., Aronstam R.S. Substance P receptor desensitization in the dorsal horn: possible involvement of receptor-G protein complexes. Brain Res. 600:1993;89-96.
34. Hunskaar S., Hole K. The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain. 30:1987;103-114.
35. Hylden J.L.K., Nahin R.L., Traub R.J., Dubner R. Expansion of receptive fields of spinal lamina I projection neurons in rats with unilateral adjuvant-induced inflammation: the contribution of dorsal horn mechanisms. Pain. 37:1989;229-243.
36. Liu H., Brown J.L., Jasmin L., Maggio J.E., Vigna S.R., Mantyh P.W., Basbaum A.I. Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc. Natl. Acad. Sci, USA. 91:1994;1009-1013.
37. Ma Q-P., Woolf C.J. Involvement of neurokinin receptors in the induction but not the maintenance of mechanical allodynia in rat flexor motoneurons. J. Physiol. 486:1995;769-777.
38. Mantyh P.W., DeMaster E., Malhotra A., Ghilardi J.R., Rogers S.D., Mantyh C.R., Liu H., Basbaum A.I., Vigna S.R., Maggio J.E., Simone D.A. Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science. 268:1995;1629-1632.
39. 2+ of NMDA responses spinal cord neurones. Nature. 309:1984;261-263.
40. McCarson K.E., Krause J.E. NK-1 and NK-3 type tachykinin receptor mRNA expression in the rat spinal cord dorsal horn is increased during adjuvant of formalin-induced nociception. J. Neurosci. 14:1994;712-720.
41. Murase K., Nedeljkov V., Randic M. The actions of neuropeptides on dorsal horn neurons in the rat spinal cord slice preparation: an intracellular study. Brain Res. 234:1982;170-176.
42. Murase K., Ryu P.D., Randic M. Tachykinins modulate multiple ionic conductances in voltage-clamped rat spinal dorsal horn neurons. J. Neurophysiol. 61:1989;854-865.
43. Neugebauer V., Weiretter F., Schaible H.-G. 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. 73:1995;1574-1583.
44. Nowak L.M., MacDonald R.L. Substance P: ionic basis for depolarizing responses of mouse spinal cord neurons in cell culture. J. Neurosci. 2:1982;1119-1128.
45. Nowak L., Bregestovski P., Asher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 307:1984;462-465.
46. Ohkubo T., Shibata M., Takahashi H., Inoki R. Roles of substance P and somatostatin on transmission of nociceptive information induced by formalin in spinal cord. J. Pharm. Exp. Ther. 252:1990;1261-1268.
47. Porro C, Cavazzuti M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog. Neurobiol. 41:1993;565-607.
48. Radhakrishnan V., Henry J.L. Antagonism of nociceptive responses of cat spinal dorsal horn neurons in vivo by the nk-1 receptor antagonists CP-96345 and CP-99994, but not by CP-96344. Neurosci. 64:1995;943-958.
49. Radhakrishnan V., Henry J.L. Novel substance P antagonist, CP-96, 345 blocks responses of cat spinal dorsal horn neurons to noxious cutaneous stimulation and to substance P. Neurosci. Lett. 132:1991;39-43.
50. Randic M., Hecimovic H., Ryu P.D. Substance P modulates glutamate-induced currents in acutely isolated rat spinal dorsal horn neurones. Neurosci. Lett. 117:1990;74-80.
51. Ren K., Dubner R. NMDA receptor antagonists attenuate mechanical hyperalgesia in rats with unilateral inflammation of the hindpaw. Neurosci. Lett. 163:1993;22-26.
52. Ren K., Hylden J.L.K., Williams G.M., Ruda M.A., Dubner R. The effects of a non-competitive NMDA receptor antagonist, MK-801, on behavioral hyperalgesia and dorsal horn neuronal activity in rats with unilateral inflammation. Pain. 50:1992a;331-344.
53. Ren, K., Iadarola, M.J. and Dubner, R., An isobolographic analysis of the effects of N-methyl-D-aspartate and NK-1 tachykinin receptor antagoninsts on inflammatory hyperalgesia in the rat, Br. J. Pharmacol., (1996) in press.
54. Ren K., Williams G.M., Hylden J.L.K., Ruda M.A., Dubner R. The intrathecal administration of excitatory amino acid receptor antagonists selectively attenuated carrageenan-induced behavioral hyperalgesia in rats. Eur. J. Pharm. 219:1992b;235-243.
55. Rosland J.H., Tjolsen, Maehle B.A., Hole K. The formalin test in mice: effect of formalin concentration. Pain. 42:1990;235-242.
56. Ruda M.A., Bennett G.J., Dubner R. Neurochemistry and neural circuitry in the dorsal horn. Prog. Brain Res. 66:1986;219-268.
57. Sakurada S., Katsumata K., Yogo H., Tan-No K., Sakurada T., Kisara K. Antinociception induced by CP 96345, a nonpeptide NK-1 receptor antagonist, in the mouse formalin and capsaicin tests. Neurosci. Lett. 151:1993a;142-145.
58. Sakurada T., Katsumata K., Manome Y., Tan-No K., Sakurada S., Kisara K., Ohba M. Antinociceptive effects in the formalin and capsaicin tests after intrathecal administration of substance P analogues in mice. Eur. J. Pharm. 242:1993b;47-52.
59. Satoh M., Kuraishi Y., Kawamura M. Effects of intrathecal antibodies to substance P, calcitonin gene-related peptide and galanin on repeated cold stress-induced hyperalgesia: comparison with carrageenan-induced hyperalgesia. Pain. 49:1992;273-378.
60. Schaible H.-G., Schmidt R.F. Time course of mechanosensitivity changes in articular afferents during a developing experimental arthritis. J. Neurophysiol. 60:1988;2180-2195.
61. 2+ channels. Eur. J. Pharm. 219:1992;491-492.
62. Sher G.D., Mitchell D. Intrathecal N-methyl-D-aspartate induces hyperexcitability in rat dorsal horn convergent neurones. Neurosci. Lett. 119:1990;199-202.
63. Sluka K.A., Dougherty P.M., Sorkin L.S., Willis W.D., Westlund K.N. 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. Rev. 17:1992;29-38.
64. Tjolsen A., Berge O.-G., Hunskaar S., Rosland J.H., Hole K. The formalin test: an evaluation of the method. Pain. 51:1992;5-17.
65. Toda T., Haruhide H. The inhibitory effect of substance P antagonist, CP-96345, on the late discharges of nociceptive neurones in the rat superficial spinal dorsal horn. Neurosci. Lett. 158:1993;36-38.
66. Traub R.J., Brozoski D. Pre-treatment but not post-treatment with an NK-1 receptor antagonist attenuates hindpaw inflammation-induced hyperalgesia in the rat. Soc. Neurosci. Abs. 21:1995;898.
67. Urban L., Thompson S.W.N., Dray A. Modulation of spinal excitability: co-operation between neurokinin and excitatory amino acid neurotransmitters. Trends Neurolog. Sci. 17:1994;432-438.
68. Woolf C.J., Thompson S.W.N. The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain. 44:1991;293-299.
69. Xu X.-J., Dalsgaard C.-J., Wiesenfeld-Hallin Z. Intrathecal CP-96345 blocks reflex facilitation induced in rats by substance P and C-fiber-conditioning stimulation. Eur. J. Pharm. 216:1992;337-344.
70. Yamamoto T., Yaksh T.L. Stereospecific effects of a nonpeptidic NK1 selective antagonist, CP-96345: antinociception in the absence of motor dysfunction. Life Sci. 49:1991;1955-1963.
71. Yamamoto T., Shimoyama N., Mizuguchi T. Effects of FK224, a novel cyclopeptide NK1 and NK2 antagonist and CP-96345, a nonpeptide NK1 antagonist, on development and maintenance of thermal hyperesthesia evoked by carrageenan injection in the rat paw. Anesthesiology. 79:1993a;1042-1050.
72. Yamamoto T., Shimoyama N., Mizuguchi T. The effects of morphine, MK-801, an NMDA antagonist, and CP-96345, an NK1 antagonist, on the hyperesthesia evoked by carrageenan injection in the rat paw. Anesthesiology. 78:1993b;124-133.
73. Yamamoto T., Shimoyama N., Mizuguchi T. Effects of intrathecal FK888, a novel dipeptide NK1 receptor antagonist, on the formalin test in the rat. Neurosci. Lett. 161:1993c;57-59.
74. Yashpal K., Radahakrishnan V., Coderre T.J., Henry J.L. CPû345, but not its stereoisomer, CP-96344, blocks the nociceptive responses to intrathecally administered substance P and to noxious thermal and chemical stimuli in the rat. Neuroscience. 52:1993;1039-1047.