Secondary hyperalgesia in the monoarthritic rat is mediated by GABAB and NK1 receptors of spinal dorsal horn neurons: A behavior and c-fos study

Neuroscience

Volumn 141, Issue 4, 2006, Pages 2087-2095

  Castro, A R ^a,b,c   Pinto, M ^a,b   Lima, D ^a,b   Tavares, I ^a,b  

^a University of Porto   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

baclofen; Fos; substance P saporin; von Frey

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; FREUND ADJUVANT; NEUROKININ 1 RECEPTOR; PROTEIN C FOS; SAPORIN; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HINDLIMB; HYPERALGESIA; IMMUNOREACTIVITY; MALE; MECHANICAL STIMULATION; MONARTHRITIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SKIN STIMULATION; SPINAL CORD DORSAL HORN;

ANIMALS; ARTHRITIS; BACLOFEN; BEHAVIOR, ANIMAL; DRUG INTERACTIONS; FREUND'S ADJUVANT; GABA AGONISTS; GENE EXPRESSION; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; PAIN MEASUREMENT; PAIN THRESHOLD; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RECEPTORS, GABA-B; RECEPTORS, NEUROKININ-1; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SUBSTANCE P;

EID: 33747161263     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.048     Document Type: Article

References (64)

1. Abbadie C., Brown J.L., Mantyh P.W., and Basbaum A.I. Spinal cord substance P receptor immunoreactivity increases in both inflammatory and nerve injury models of persistent pain. Neuroscience 70 (1996) 201-209
2. Abbadie C., Trafton J., Liu H., Mantyh P.W., and Basbaum A.I. Inflammation increases the distribution of dorsal horn neurons that internalize the neurokinin-1 receptor in response to noxious and non-noxious stimulation. J Neurosci 17 (1997) 8049-8060
3. Almeida A., and Lima D. Activation by cutaneous or visceral noxious stimulation of spinal neurons projecting to the medullary dorsal reticular nucleus in the rat. a c-fos study. Eur J Neurosci 9 (1997) 686-695
4. Ataka T., Kumamoto E., Shimoji K., and Yoshimura M. Baclofen inhibits more effectively C-afferent than Aδ-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain 86 (2000) 273-282
5. Bertman L.J., and Advokat C. Comparison of the antinociceptive and antispastic action of (-)-baclofen after systemic and intrathecal administration in intact, acute and chronic spinal rats. Brain Res 684 (1995) 8-18
6. Butler S.H., Godefroy F., Besson J.M., and Weil-Fugazza J. A limited arthritic model for chronic pain studies in the rat. Pain 48 (1992) 73-81
7. B receptor-mediated events to inflammatory pain processing. carrageenan oedema and associated spinal c-fos expression in the rat. Neuroscience 73 (1996) 487-496
8. Castro A.R., Bowery N., and Castro-Lopes J.M. Baclofen and midazolam alter c-fos induction by peripheral noxious or innocuous stimulation in the rat spinal cord of normal and monoarthritic rats. Neuropharmacology 38 (1999) 1775-1788
9. B receptors in spinal neurons projecting to antinociceptive or pronociceptive medullary centres. Brain Res Bull 69 (2006) 266-275
10. B receptors are located in lamina I. Brain Res 1003 (2004) 77-85
11. Castro A.R., Pinto M., Lima D., and Tavares I. Imbalance between the expression of NK1 and GABAB receptors in nociceptive spinal neurons during secondary hyperalgesia. a c-fos study in the monoarthritic rat. Neuroscience 132 (2005) 905-916
12. Castro-Lopes J.M., Tavares I., Tölle T.R., Coito A., and Coimbra A. Increase in GABAergic cells and GABA levels in the spinal cord in unilateral inflammation of hindlimb in the rat. Eur J Neurosci 4 (1992) 296-301
13. Cervero F., Laird J.M.A., and García-Nicas E. Secondary hyperalgesia and presynaptic inhibition. an update. Eur J Pain 7 (2003) 345-351
14. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53 (1994) 55-63
15. Coggeshall R.E. Fos, nociception and the dorsal horn. Prog Neurobiol 77 (2005) 299-352
16. Cruz C.D., Avelino A., McMahon S.B., and Cruz F. Increased spinal cord phosphorylation of extracellular signal-regulated kinases mediates micturition overactivity in rats with chronic bladder inflammation. Eur J Neurosci 21 (2005) 773-781
17. Dickenson A.H., Brewer C.M., and Hayes N.A. Effects of topical baclofen on C fibre-evoked neuronal activity in the rat dorsal horn. Neuroscience 14 (1985) 557-562
18. Ding Y.-Q., Takada M., Shigemoto R., and Mizuno N. Spinoparabrachial tract neurons showing substance P receptor-like immunoreactivity in the lumbar spinal cord of the rat. Brain Res 674 (1995) 336-340
19. Dirig D.M., and Yaksh T.L. Intrathecal baclofen and muscimol, but not midazolam, are antinociceptive using the rat-formalin model. J Pharmacol Exp Ther 275 (1995) 219-175
20. Dubner R., and Ruda M.A. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15 (1992) 96-103
21. Fields H.L., Basbaum A.I., and Heinricher M.M. Central nervous system mechanisms of pain modulation. In: McMahon S.B., and Koltzenburg M. (Eds). Wall and Melzak's textbook of pain. 5th ed (2006), Elsevier Churchill Livingstone, Philadelphia 125-142
22. Grant G., and Robertson B. Primary afferent projections to the spinal cord. In: Paxinos G. (Ed). The rat nervous system (2004), Elsevier, Sydney 111-119
23. Hammond D.L., and Drower E.J. Effects of intrathecally administered THIP, baclofen, and muscimol on nociceptive threshold. Eur J Pharmacol 103 (1984) 121-125
24. Hammond D.L., Nelson V., and Thomas D.A. Intrathecal methysergide antagonizes the antinociception, but not the hyperalgesia produced by microinjection of baclofen in the ventromedial medulla of the rat. Neurosci Lett 244 (1998) 93-96
25. Hammond D.L., and Washington J.D. Antagonism of L-baclofen-induced antinociception by CGP 35348 in the spinal cord of the rat. Eur J Pharmacol 234 (1993) 255-262
26. Honoré P., Menning P.M., Rogers S.D., Nichols M.L., Basbaum A.I., Besson J.-M., and Mantyh P.W. Spinal substance P receptor expression and internalization in acute, short-term, and long-term inflammatory pain states. J Neurosci 19 (1999) 7670-7678
27. Huang J.H., Ali Z., Travison T.G., Campbell J.N., and Meyer R.A. Spatial mapping of the zone of secondary hyperalgesia reveals a gradual decline of pain with distance but sharp borders. Pain 86 (2000) 33-42
28. Iyadomi M., Iyadomi I., Kumamoto E., Tomokuni K., and Yoshimura M. Presynaptic inhibition by baclofen of miniature EPSCs and IPSCs in substantia gelatinosa neurons of the adult rat spinal dorsal horn. Pain 85 (2000) 385-393
29. Kangrga I., Jiang M., and Randic M. Actions of (-)-baclofen on rat dorsal horn. Brain Res 562 (1991) 265-275
30. Khasabov S.G., Ghilard J.R., Mantyh P.W., and Simone D.A. Spinal neurons that express NK1 receptors modulate descending controls that project through the dorsolateral funiculus. J Neurophysiol 93 (2005) 998-1006
31. Khasabov S.G., Rogers S.D., Ghilard J.R., Peters C.M., Mantyh P.W., and Simone D.A. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22 (2002) 9086-9098
32. Krause J.E., DiMaggio D.A., and McCarson K.E. Alterations in neurokinin 1 receptor gene expression in models of pain and inflammation. Can J Physiol Pharmacol 73 (1995) 854-859
33. Leah J.D., Porter J., de-Pommery J., Menétry D., and Weil-Fuguzza J. Effect of acute stimulation on Fos expression in spinal neurons in the presence of persisting C-fiber activity. Brain Res 719 (1996) 104-111
34. Lima D., Avelino A., and Coimbra A. Differentail activation of c-fos in spinal neurones by distinct classes of noxious stimuli. Neuroreport 4 (1992) 747-750
35. Magerl W., Fuchs P.N., Meyer R.A., and Treede R.-D. Roles of capsaicin-insensitive nociceptors in cutaneous pain and secondary hyperalgesia. Brain 124 (2001) 1754-1764
36. Magerl W., and Treede R.-D. Secondary tactile hyperalgesia. a novel type of pain induced somatosensory plasticity in human subjects. Neurosci Lett 361 (2003) 136-139
37. A receptor activation, inhibits electrically evoked substance P-like immunoreactivity release from the rat spinal cord in vitro. J Pharmacol Exp Ther 255 (1993) 1490-1496
38. B antagonist, prevents antinociception and muscle-relaxant effect induced by baclofen. Br J Pharmacol 103 (1991) 1303-1308
39. 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., and Simone D.A. Receptor endocytoses and dendrite reshaping in spinal neurons after somatosensory stimulation. Science 268 (1995) 1629-1632
40. Mantyh P.W., and Hunt S.P. Setting the tone. superficial dorsal horn projection neurons regulate pain sensitivity. Trends Neurosci 27 (2004) 582-584
41. Mantyh P.W., Rogers S.D., Honoré P., Allen B.J., Ghilardi J.R., Li J., Daughters R.S., Lappi D.A., Wiley R.G., and Simone D.A. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278 (1997) 275-279
42. McCarson K.E., and Krause J.E. The neurokinin-1 receptor antagonist LY306,740 blocks nociception-induced increases in dorsal horn neurokinin-1 receptor gene expression. Mol Pharmacol 50 (1996) 1189-1199
43. Merskey H., and Bogduk N. Classification of chronic pain. 2nd ed (1994), IASP Press, Seattle
44. Neugebauer V., Weiretter H.G., and Schaible H.G. Involvement of substance 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
45. Nichols M.L., Allen B.J., Rogers S.D., Ghilardi J.R., Honoré P., Luger N.M., Finke M.P., Li J., Lappi D.A., Simone D.A., and Mantyh P.W. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286 (1999) 1558-1561
46. Noguchi K., and Ruda M.A. Gene regulation in an ascending nociceptive pathway. inflammation-induced increase in preprotachykinin mRNA in rat lamina I spinal projection neurons. J Neurosci 12 (1992) 2563-2472
47. Oku R., Satoh M., and Takagi H. Release of substance P from the spinal dorsal horn is enhanced in polyarthritic rats. Neurosci Lett 74 (1987) 315-319
48. Schaible H.-G., Jarrott B., Hope P.J., and Duggan A.W. 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 (1990) 214-223
49. Schafer M.K., Nohr D., Krause J.E., and Weihe E. Inflammation-induced upregulation of NK1 receptor mRNA in dorsal horn neurones. Neuroreport 4 (1993) 1007-1010
50. A and glycine receptors to central sensitization. disinhibition and touch-evoked allodynia in the spinal cord. J Neurophysiol 72 (1994) 169-179
51. Sluka K.A., and Westlund K.N. 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 (1993) 89-103
52. Sumikura H., Andersen O.K., Drewes A.M., and Arendt-Nielsen L. Spatial and temporal profiles of flare and hyperalgesia after intradermal capsaicin. Pain 105 (2003) 285-291
53. Suzuki R., Morcuende S., Webber M., Hunt S.P., and Dickenson A.H. Superficial NK1-expression neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5 (2002) 1319-1326
54. Tavares I., Albino-Teixeira A., and Lima D. Hypertension inhibits noxious-evoked c-fos expression in the rat spinal cord. Neuroreport 6 (1995) 1664-1668
55. Tavares I., Lima D., and Coimbra A. Neurons in the superficial dorsal horn of the rat spinal cord projecting to the medullary ventrolateral reticular formation express c-fos after noxious stimulation of the skin. Brain Res 623 (1993) 278-286
56. Thomas D.A., McGowan M.K., and Hammond D.L. Microinjection of baclofen in the ventromedial medulla of rats. antinociception at low doses and hyperalgesia at high doses. J Pharmacol Exp Ther 275 (1995) 274-284
57. Todd A.J., McGill M.M., and Shehab S.A.S. Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem. Eur J Neurosci 12 (2000) 689-700
58. Traub R.J. The spinal contribution of substance P to the generation and maintenance of inflammatory in the rat. Pain 67 (1996) 151-161
59. Urban L., Thompson S.W.N., and Dray A. Modulation of spinal excitability. co-operation between neurokinin and excitatory amino acid neurotransmitters. Trends Neurosci 17 (1994) 432-438
60. Vanegas H. To the descending pain-control system in rats, inflammation-induced primary and secondary hyperalgesia are two different things. Neurosci Lett 361 (2004) 225-228
61. Vierck C.J., Kline R.H., and Wiley R.G. Intrathecal substance P-saporin attenuates operant escape from nociceptive thermal stimuli. Neuroscience 119 (2003) 223-232
62. Wiley R.G., and Lappi D.A. Destruction of neurokinin-1 receptor expressing cells in vitro and in vivo using substance P-saporin in rats. Neurosci Lett 230 (1997) 97-100
63. Yang K., Wang D., and Li Y.-Q. Distribution and depression of the GABAB receptor in the spinal dorsal horn of adult rat. Brain Res Bull 55 (2001) 470-485
64. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110