Opioidergic and adrenergic modulation of formalin-evoked spinal c-fos mRNA expression and nocifensive behavior in the rat

European Journal of Pharmacology

Volumn 379, Issue 2-3, 1999, Pages 141-149

  Sawamura, Shigehito ^a,b   Fujinaga, Masahiko ^a,b   Kingery, Wade S ^a,c   Belanger, Natasha ^a,b   Davies, M Frances ^a,b   Maze, Mervyn ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Anesthesiology   (United States)

^c Phys Med and Rehab Service   (United States)

Author keywords

2 Adrenoceptor; c fos; Formalin test; Opioid receptor; Spinal cord

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; ATIPAMEZOLE; DEXMEDETOMIDINE; FORMALDEHYDE; MORPHINE; NALOXONE; OPIATE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; GENETIC TRANSCRIPTION; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; NOCICEPTION; NONHUMAN; NORTHERN BLOTTING; ONCOGENE C FOS; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD;

ANALGESICS; ANIMALS; FORMALDEHYDE; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; PAIN; PAIN MEASUREMENT; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, OPIOID; RNA, MESSENGER; SPINAL CORD;

EID: 0032704741     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(99)00463-X     Document Type: Article

References (57)

1. Abbadie C., Besson J.-M. Effects of morphine and naloxone on basal and evoked Fos-like immunoreactivity in lumbar spinal cord neurons of arthritic rats. Pain. 52:1993;29-39.
2. Abbadie C., Honore P., Besson J.M. Intense cold noxious stimulation of the rat hindpaw induces c-fos expression in lumbar spinal cord neurons. Neuroscience. 59:1994;457-468.
3. Abbadie C., Taylor B.K., Peterson M.A., Basbaum A.I. Differential contribution of the two phases of the formalin test to the pattern of c-fos expression in the rat spinal cord: studies with remifentanil and lidocaine. Pain. 69:1997;101-110.
4. Calcagnetti D.J., Helmstetter F.J., Fanselow M.S. Analgesia produced by centrally administered DAGO, DPDPE and U50488H. Eur. J. Pharmacol. 153:1988;117-122.
5. Chapman V., Honore P., Buritova J., Besson J.M. The contribution of the NMDA receptor activation to spinal c-Fos expression in a model of inflammatory pain. Br. J. Pharmacol. 116:1995;1628-1634.
6. Chomcznyski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Ann. Biochem. 162:1987;156-159.
7. Coderre T.J., Abbott F.V., Melzack R. Effects of peripheral antisympathetic treatments in the tail-flick, formalin and autotomy tests. Pain. 18:1984;13-23.
8. Dennis S.G., Melzack R., Gutman S., Boucher F. Pain modulation by adrenergic agents and morphine as measured by three pain tests. Life Sci. 26:1980;1247-1259.
9. Dickenson A.H., Chapman V., Green G.M. The pharmacology of excitatory and inhibitory amino acid-mediated events in the transmission and modulation of pain in the spinal cord. Gen. Pharmacol. 28:1997;633-638.
10. Doyle, C.A., Palmer, J.A., Munglani, R., Hunt, S.P., 1997. Molecular consequences of noxious stimulation. In: Borsooks, D. (Ed.), Molecular Neurobiology of Pain, Vol. 9. IASP Press, Seattle, pp. 145-169.
11. Doze V.A., Chen B.X., Maze M. Dexmedetomidine produces a hypnotic-anesthetic action in rats via activation of central alpha-2 adrenoceptors. Anesthesiology. 71:1989;75-79.
12. Draisci G., Iadarola M.J. Temporal analysis of increases in c-fos, preprodynorphin and preproenkephalin mRNAs in rat spinal cord. Mol. Brain Res. 6:1989;31-37.
13. Drower E.J., Stapelfeld A., Mueller R.A., Hammond D.L. The antinociceptive effects of prostaglandin antagonists in the rat. Eur. J. Pharmacol. 133:1987;249-256.
14. Elliot K.J., Brodsky M., Hynansky A.D., Foley K.M., Inturrisi C.E. Dextromethorphan suppresses both formalin-induced nociceptive behavior and the formalin-induced increase in spinal cord c-fos mRNA. Pain. 61:1995;401-409.
15. Gogas K.R., Presley R.W., Levine J.D., Basbaum A.I. The antinociceptive action of supraspinal opioids results from an increase in descending inhibitory control: correlation of nociceptive behavior and c-fos expression. Neuroscience. 42:1991;617-628.
16. Gogas K.R., Cho H.J., Botchkina G.I., Levine J.D., Basbaum A.I. Inhibition of noxious stimulus-evoked pain behaviors and neuronal fos-like immunoreactivity in the spinal cord of the rat by supraspinal morphine. Pain. 65:1996;9-15.
17. Hammond D.L., Presley R., Gogas K.R., Basbaum A.I. Morphine or U-50,488 suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus solitarii evoked by a noxious visceral stimulus in the rat. J. Comp. Neurol. 315:1992;244-253.
18. Harris J.A. Using c-fos as a neural marker of pain. Brain Res. Bull. 45:1998;1-8.
19. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog. Neurobiol. 50:1996;83-107.
20. Hu S., Zhu J. Sympathetic facilitation of sustained discharges of polymodal nociceptors. Pain. 38:1989;85-90.
21. Hunt S.P., Pini W., Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 328:1987;632-634.
22. Hunter J.C., Woodburn V.L., Durieux C., Pettersson E.K.E., Poat J.A., Hughes J. C-fos antisense oligodeoxynucleotide increases formalin-induced nociception and regulates preprodynorphin expression. Neuroscience. 65:1995;485-492.
23. Hylden J.L.K., Noguchi K., Ruda M.A. Neonatal capsaicin treatment attenuates spinal Fos activation and dynorphin gene expression following peripheral tissue inflammation and hyperalgesia. J. Neurosci. 12:1992;1716-1725.
24. Johnson C.M., Hill C.S., Chawla S., Treisman R., Bading H. Calcium controls gene expression via three distinct pathways that can function independently of the Ras/mitogen-activated protein kinases (ERKs) signaling cascade. J. Neurosci. 17:1997;6189-6202.
25. Jones S.L., Light A.R. Termination patterns of serotoninergic medullary raphe spinal fibers in the rat lumbar spinal cord: an anterograde immunohistochemical study. J. Comp. Neurol. 297:1990;267-282.
26. Kanui T.I., Tjolsen A., Lund A., Mjellem-Joly N., Hole K. Antinociceptive effects of intrathecal administration of alpha-adrenoceptor antagonists and clonidine in the formalin test in the mouse. Neuropharmacology. 32:1993;367-371.
27. Kocher L. Systemic naloxone does not affect pain-related behavior in the formalin test in rat. Physiol. Behav. 43:1988;265-268.
28. Malmberg A.B., Yaksh T.L. Pharmacology of the spinal action of ketorolac, morphine, ST-91, U50488H, and L-PIA on the formalin test and an isobolographic analysis of the NSAID interaction. Anesthesiology. 79:1993;270-281.
29. Maze M. "Exciting" aspects of opiate receptor signal transduction. Anesthesiology. 87:1997;1032-1033.
30. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14:1991;421-451.
31. Munglani R., Hunt S.P. Molecular biology of pain. Br. J. Anaesth. 75:1995;186-192.
32. North M.A. Naloxone reversal of morphine analgesia but failure to alter reactivity to pain in the formalin test. Life Sci. 22:1978;295-302.
33. Pertovaara A. Antinociception induced by alpha-2-adrenoceptor agonists, with special emphasis on medetomidine studies. Prog. Neurobiol. 40:1993;691-709.
34. Pertovaara A., Kauppila T., Tukeva T. The effect of medetomidine, an alpha-2 adrenoceptor agonist, in various pain tests. Eur. J. Pharmacol. 179:1990;323-328.
35. Pertovaara A., Mecke E., Carlson S. Attempted reversal of cocaine-induced antinociceptive effects with naloxone, an opioid antagonist. Eur. J. Pharmacol. 192:1991;349-353.
36. Pertovaara A., Bravo R., Herdegen T. Induction and suppression of immediate-early genes in the rat brain by a selective alpha-2-adrenoceptor agonist and antagonist following noxious peripheral stimulation. Neuroscience. 54:1993;117-126.
37. Peterson M.A., Basbaum A.I., Abbadie C., Rhode D.S., McKay W.R., Taylor B.K. The differential contribution of capsaicin-sensitive afferents to behavioral and cardiovascular measures of brief and persistent nociception and to Fos expression in the formalin test. Brain Res. 755:1997;9-16.
38. Presley R.W., Menetrey D., Levine J.D., Basbaum A.I. Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord. J. Neurosci. 10:1990;323-335.
39. Puig S., Sorkin L.S. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain. 64:1995;345-355.
40. Rohde D.S., Detweiler D.J., Basbaum A.I. Formalin-evoked Fos expression in spinal cord is enhanced in morphine-tolerant rats. Brain Res. 766:1997;93-100.
41. Sato J., Suzudi S., Iseki T., Kumazawa T. Adrenergic excitation of cutaneous nociceptors in chronically inflamed rats. Neurosci. Lett. 164:1993;225-228.
42. Sato J., Suzuki S., Tamura R., Kumazawa T. Norepinephrine excitation of cutaneous nociceptors in adjuvant-induced inflamed rats does not depend on sympathetic neurons. Neurosci. Lett. 177:1994;135-138.
43. Skingle M., Hayes A., Tyers M.B. Antinociception activity of clonidine in the mouse, rat, and dog. Life Sci. 31:1982;1123-1132.
44. Sun W.Z., Shyu B.C., Shieh J.Y. Nitrous oxide or halothane, or both, fail to suppress c-fos expression in rat spinal cord dorsal horn neurones after subcutaneous formalin. Br. J. Anaesth. 76:1996;99-105.
45. Szekely A.M., Barbaccia M.L., Alho H., Costa E. In primary cultures of cerebellar granule cells the activation of N-methyl-D-aspartate-sensitive glutamate receptors induces c-fos mRNA expression. Mol. Pharmacol. 35:1989;401-408.
46. Tao Y.-X., Zhao Z.-Q. Ultrastructure of Fos-labeled neurons relating to nociceptive primary afferent and substance P terminals in rat spinal superficial laminae. Neuropeptides. 31:1997;327-332.
47. Tao Y.-X., Wei F., Zhao Z.-Q. A contribution of neurokinin-1 receptor to formalin-induced c-fos expression in the rat spinal dorsal horn. Neurosci. Lett. 221:1996;105-108.
48. Tasker R.A.R., Melzack R. Different alpha-receptor subtypes are involved in clonidine produced analgesia in different pain tests. Life Sci. 44:1989;9-17.
49. Tasker R.A.R., Connell B.J., Yole M.J. Systemic injections of alpha-1 adrenergic agonists produce antinociception in the formalin test. Pain. 49:1992;383-391.
50. Taylor B.K., Peterson M.A., Basbaum A.I. Continuous intravenous infusion of naloxone does not change behavioral, cardiovascular, or inflammatory responses to subcutaneous formalin in the rat. Pain. 69:1997;171-177.
51. Todd A.J., Spike R.C., Brodbelt A.R., Price R.F., Shehab S.A.S. Some inhibitory neurons in the spinal cord develop c-fos-immunoreactivity after noxious stimulation. Neuroscience. 63:1994;805-816.
52. Tokunaga A., Doi M., Senba E. Effects of local anaesthesia on formalin-induced Fos expression in the rat dorsal horn. NeuroReport. 6:1995;2301-2304.
53. Tolle T.R., Schadrack J., Castro-Lopes J.M., Evan G., Roques B.P., Zieglgansberger W. Effects of kelatorphan and morphine before and after noxious stimulation on immediate-early gene expression in rat spinal cord neurons. Pain. 56:1994;103-112.
54. Wheeler-Aceto H., Cowan A. Naloxone causes apparent antinociception and pronociception simultaneously in the rat paw formalin test. Eur. J. Pharmacol. 236:1993;193-199.
55. Wilson D.G., Rees H., Roberts M.H.T. The antinociceptive effects of anterior pretectal stimulation in tests using thermal, mechanical and chemical noxious stimuli. Pain. 44:1991;195-200.
56. Yashpal K., Mason P., McKenna J.E., Sharma S.K., Henry J.L., Coderre T.J. Comparison of the effects of treatment with intrathecal lidocaine given before and after formalin on both nociception and Fos expression in the spinal cord dorsal horn. Anesthesiology. 88:1998;157-164.
57. Zhang R.-X., Wang R., Chen J.-Y., Qiao J.-T. Effects of descending inhibitory systems on the c-Fos expression in the rat spinal cord during formalin-induced noxious stimulation. Neuroscience. 58:1994;299-304.