The massive expression of c-fos protein in spinal dorsal horn neurons is not followed by long-term changes in spinal nociception

Neuroscience

Volumn 73, Issue 3, 1996, Pages 657-666

  Sandkuhler J ^a   Treier, A C ^a   Liu, X G ^a   Ohnimus, M ^a  

^a NONE

Author keywords

immediate early gene; long term depression; mechanical hyperalgesia; pain; rat; spinal dorsal horn; thermal hyperalgesia

Indexed keywords

ETHER; MORPHINE; N METHYL DEXTRO ASPARTIC ACID; PROTEIN C FOS;

ANESTHESIA INDUCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; HOT PLATE TEST; IMMUNOREACTIVITY; LATENT PERIOD; LOCOMOTION; LUMBAR SPINAL CORD; MALE; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SACRAL SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; TAIL FLICK TEST; WITHDRAWAL REFLEX;

EID: 0030219391     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00073-5     Document Type: Article

References (50)

1. 1. Beck H. and Sandkühler J. (1993) Role of volume transmission for spinal nociception: extrasynaptic mediators of immediate early gene expression. IASP Publications, Abstr. - VIIth World Congr. Pain, 472.
2. 2. Beck H., Schröck H. and Sandkühler J. (1995) Controlled superfusion of the rat spinal cord for studying non-synaptic transmission: an autoradiographic analysis. J. Neurosci. Meth. 58, 193-202.
3. 3. Bennett G. J. and Xie Y.-K. (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107.
4. 4. Besson J. M. and Chaouch A. (1987) Peripheral and spinal mechanisms of nociception. Physiol. Rev. 67, 67-186.
5. 5. Bett K. and Sandkühler J. Map of brainstem and spinal dorsal horn neurons activated by chemical stimulation in the nucleus raphe magnus of the unanesthetized rat. Neuroscience 67, 497-504.
6. 6. Bliss T. V. P. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. 7. Caudle R. M. and Isaac L. (1987) Intrathecal dynorphin (1-13) results in an irreversible loss of the tail-flick reflex in rats. Brain Res. 435, 1-6.
8. 8. Deadwyler S. A., Dunwiddie T. and Lynch G. (1987) A critical level of protein synthesis is required for long-term potentiation. Synapse 1, 90-95.
9. 9. Dickenson A. H., Sullivan A. F., Fournie-Zaluski M. C. and Roques B. P. (1987) Prevention of degradation of endogenous enkephalins produces inhibition of nociceptive neurones in rat spinal cord. Brain Res. 408, 185-191.
10. 10. Dragunow M. and Faull R. (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Meth. 29, 261-265.
11. 11. Dragunow M., Faull R. L. M. and Jansen K. L. R. (1990) MK-801, an antagonist of NMDA receptors, inhibits injury-induced c-fos protein accumulation in rat brain. Neurosci. Lett. 109, 128-133.
12. 12. Draisci G. and Iadarola M. J. (1989) Temporal analysis of increases in c-fos, preprodynorphin and preproenkephalin mRNAs in rat spinal cord. Molec. Brain Res. 6, 31-37.
13. 13. Dubner R. (1991) Pain and hyperalgesia following tissue injury: new mechanisms and new treatments. Pain 44, 213-214.
14. 14. Duggan A. W., Hall J. G. and Headley P. M. (1976) Morphine, enkephalin and the substantia gelatinosa. Nature 264, 456-458.
15. 15. Duggan A. W., Hope P. J., Jarrott B., Schaible H.-G. and Fleetwood-Walker S. M. (1990) Release, spread and persistence of immunoreactive neurokinin A in the dorsal horn of the cat following noxious cutaneous stimulation. Studies with antibody microprobes. Neuroscience 35, 195-202.
16. 16. Duggan A. W., Morton C. R., Zhao Z. Q. and Hendry I. A. (1987) Noxious heating of the skin releases immunoreactive substance P in the substantia gelatinosa of the cat: a study with antibody microprobes. Brain Res. 403, 345-349.
17. 17. Frey U., Krug M., Brödemann R., Reymann K. and Matthies H. (1989) Long-term potentiation induced in dendrites separated from rat's CA1 pyramidal somata does not establish a late phase. Neurosci. Lett. 97, 135-139.
18. 18. Gillardon F., Beck H., Uhlmann E., Herdegen T., Sandkühler J., Peyman A. and Zimmermann M. (1994) Inhibition of c-Fos protein expression in rat spinal cord by antisense oligodeoxynucleotide superfusion. Eur. J. Neurosci. 6, 880-884.
19. 19. Go V. L. W. and Yaksh T. L. (1987) Release of substance P from the cat spinal cord. J. Physiol., Lond. 391, 141-167.
20. 20. Hengerer B., Lindholm D., Heumann R., Rüther U., Wagner E. F. and Thoenen H. (1990) Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc. natn. Acad. Sci. U.S.A. 87, 3899-3903.
21. 21. Herdegen T., Kovary K., Leah J. and Bravo R. (1991) Specific temporal and spatial distribution of JUN, FOS, and KROX-24 proteins in spinal neurons following noxious transsynaptic stimulation. J. comp. Neurol. 312, 1-14.
22. 22. Hori Y., Endo K. and Takahashi T. (1992) Presynaptic inhibitory action of enkephalin on excitatory transmission in superficial dorsal horn of rat spinal cord. J. Physiol., Lond. 450, 673-685.
23. 23. Hunt S. P., Pini A. and Evan G. (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328, 632-634.
24. 24. Hylden J. L. and Wilcox G. L. (1980) Intrathecal morphine in mice: a new technique. Eur. J. Pharmac. 67, 313-316.
25. 25. Iadarola M. J., Douglass J., Civelli O. and Naranjo J. R. (1988) Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: evidence using cDNA hybridization. Brain Res. 455, 205-212.
26. 26. Kobierski L. A., Chu H.-M., Tan Y. and Comb M. J. (1991) cAMP-dependent regulation of proenkephalin by JunD and JunB: positive and negative effects of AP-1 proteins. Proc. natn. Acad. Sci. U.S.A. 88, 10,222-10,226.
27. 27. Kolhekar R., Meller S. T. and Gebhart G. F. (1993) Characterization of the role of spinal N-methyl-D-aspartate receptors in thermal nociception in the rat. Neuroscience 57, 385-395.
28. 28. Lanteri-Minet M., Isnardon R., De Pommery J. and Menetrey D. (1993) Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 55, 737-753.
29. 29. Levine J. D., Fields H. L. and Basbaum A. I. (1993) Peptides and the primary afferent nociceptor. J. Neurosci. 13, 2273-2286.
30. 30. Liu X.-G. and Sandkühler J. (1995) Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is blocked by D-CPP, a NMDA receptor antagonist. Neurosci. Lett. 191, 43-46.
31. 31. Liu X.-G. and Sandkühler J. (1995) The effects of extrasynaptic substance P on nociceptive neurons in laminae I and II in rat lumbar spinal dorsal horn. Neuroscience 68, 1207-1218.
32. 32. Lucas J. J., Mellström B., Colado M. I. and Naranjo J. R. (1993) Molecular mechanisms of pain: serotonin 1A receptor agonists trigger transactivation by c-fos of the prodynorphin gene in spinal cord neurons. Neuron 10, 599-611.
33. 33. Marti A., Jehn B., Costello E., Keon N., Ke G., Martin F. and Jaggi R. (1994) Protein kinase A and AP-1 (c-Fos/JunD) are induced during apoptosis of mouse mammary epithelial cells. Oncogene 9, 1213-1223.
34. 34. Meller S. T. and Gebhart G. F. (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52, 127-136.
35. 35. Nachemson A. K. and Bennett G. J. (1993) Does pain damage spinal cord neurons? Transsynaptic degeneration in rat following a surgical incision. Neurosci. Lett. 162, 78-80.
36. 36. Neugebauer V., Lücke T. and Schaible H. G. (1993) N-Methyl-D-aspartate (NMDA) and non-NMDA receptor antagonists block the hyperexcitability of dorsal horn neurons during development of acute arthritis in rat's knee joint. J. Neurophysiol. 70, 1365.
37. 37. Noguchi K., Dubner R. and Ruda M. A. (1992) Preproenkephalin mRNA in spinal dorsal horn neurons is induced by peripheral inflammation and is co-localized with fos-related proteins. Neuroscience 46, 561-570.
38. 38. Noguchi K., Morita Y., Kiyama H., Sato M., Ono K. and Tohyama M. (1989) Preproenkephalin gene expression in the rat spinal cord after noxious stimuli. Molec. Brain Res. 5, 227-234.
39. 39. Polak J. M., Bloom S. R., Sabate J. M., Mulderry P. M., Ghatei M. A., McGregor G. P., Morrison J. F. B., Kelly S. J., Evans R. M. and Rosenfeld M. S. (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and eight other species. J. Neurosci. 4, 3101-3111.
40. 40. Randić M., Jiang M. C. and Cerne R. (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J. Neurosci. 13, 5228-5241.
41. 41. Sandkühler J. (1991) Induction of the proto-oncogene c-fos as a cellular marker of brainstem neurons activated from the PAG. In The Midbrain Periaqueductal Gray Matter (eds Depaulis A. and Bandler R.), pp. 267-286. Plenum Press, New York.
42. 42. Sandkühler J., Eblen-Zajjur A. A. and Liu X.-G. (1994) Differential effects of skin inflammation, extrasynaptic substance P and noxious skin heating on rhythmicity, synchrony and nonlinear dynamics in rat spinal dorsal horn. In Progress in Pain Research and Management, Vol. 2, Proceedings of the 7th World Congress on Pain (eds Gebhart G. F., Hammond D. L. and Jensen T. S.), pp. 347-358. IASP Publications., Washington.
43. 43. Sandkühler J. and Herdegen T. (1995) Distinct pattern of activated neurons throughout the rat midbrain periaqueductal gray induced by chemical stimulation. J. comp. Neurol. 357, 546-553.
44. 44. Schreiber S. S., Maren S., Tocco G., Shors T. J. and Thompson R. F. (1991) A negative correlation between the induction of long-term potentiation and activation of immediate early genes. Molec. Brain Res. 11, 89-91.
45. 45. Sluka K. A. and Westlund K. N. (1993) 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.
46. 46. Smith F. L. and Dewey W. L. (1993) Endogenous dynorphin modulates calcium-mediated antinociception in mice. Pharmac. Biochem. Behav. 45, 383-391.
47. 47. Tölle T. R., Castro-Lopes J. M., Evan G. and Zieglgänsberger W. (1991) c-fos Induction in the spinal cord following noxious stimulation: prevention by opiates but not by NMDA antagonists. In: Proceedings of the VIth World Congress on Pain (eds Bond M. R., Charlton J. E. and Woolf C. J.), pp. 299-305. Elsevier, Amsterdam.
48. 48. Woolf C. J. (1984) Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain 18, 325-343.
49. 49. Worley P. F., Bhat R. V., Baraban J. M., Erickson C. A., McNaughton B. L. and Barnes C. A. (1993) Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J. Neurosci. 13, 4776-4786.
50. 50. Yaksh T. L. and Rudy T. A. (1976) Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 17, 1031-1036.