The activation of nicotinic acetylcholine receptors enhances the inhibitory synaptic transmission in the deep dorsal horn neurons of the adult rat spinal cord

Molecular Pain

Volumn 3, Issue , 2007, Pages

  Takeda, Daisuke ^a,b   Nakatsuka, Terumasa ^c   Gu, Jianguo G ^d   Yoshida, Munehito ^a  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b KANSAI UNIVERSITY OF HEALTH SCIENCES   (Japan)

^c SAGA UNIVERSITY   (Japan)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CHOLINE; GLUTAMIC ACID; MECAMYLAMINE; N METHYL 4 (3 PYRIDINYL) 3 BUTENAMINE; NICOTINE; NICOTINIC RECEPTOR; TETRODOTOXIN; BICUCULLINE; STRYCHNINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FACILITATION; MALE; NERVE ENDING; NOCICEPTION; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION; WHOLE CELL; ANIMAL; DRUG EFFECT; NERVE CELL; PHYSIOLOGY; POSTERIOR HORN CELL; SYNAPSE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; BICUCULLINE; NEURONS; NICOTINE; POSTERIOR HORN CELLS; RATS; RECEPTORS, NICOTINIC; STRYCHNINE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 35549004608     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-3-26     Document Type: Article

References (48)

1. Changeux JP, Edelstein SJ: Allosteric receptors after 30 years. Neuron 1998, 21:959-980. 10.1016/S0896-6273(00)80616-9 9856454
2. McGehee DS: Molecular diversity of neuronal nicotinic acetylcholine receptors. Ann N Y Acad Sci 1999, 868:565-577. 10.1111/ j.1749-6632.1999.tb11330.x 10414338
3. Dani JA, Ji D, Zhou FM: Synaptic plasticity and nicotine addiction. Neuron 2001, 31:349-352. 10.1016/S0896-6273(01)00379-8 11516393
4. Cordero-Erausquin M, Marubio LM, Klink R, Changeux JP: Nicotinic receptor function: New perspectives from knockout mice. Trends Pharmacol Sci 2000, 21:211-217. 10.1016/S0165-6147(00)01489-9 10838608
5. Davis L, Pollock LJ, Stone TT: Visceral pain Surg Gynecol Obstet 1932, 55:418-427
6. Sahley TL, Berntson GG: Antinociceptive effects of central and systemic administrations of nicotine in the rat. Psychopharmacology 1979, 65:279-283. 10.1007/BF00492216 117500
7. Tripathi HL, Martin BR, Aceto MD: Nicotine-induced antinociception in rats and mice: Correlation with nicotine brain levels. J Pharmacol Exp Ther 1982, 221:91-96. 7062295
8. Aceto MD, Awaya H, Martin BR, May EL: Antinociceptive action of nicotine and its methiodide derivatives in mice and rats. Br J Pharmacol 1983, 79:869-876. 6140048
9. Spande TF, Garraffo HM, Yeh HJ, QL, Pannell LK, Daly JW: A new class of alkaloids from a dendrobatid poison frog: A structure for alkaloid 251F. J Nat Prod 1992, 55:707-722. 10.1021/np50084a002 1522417
10. Qian C, Li T, Shen TY, Libertine-Garahan L, Eckman J, Biftu T, Ip S: Epibatidine is a nicotinic analgesic. Eur J Pharmacol 1993, 250:R13-14. 10.1016/0014-2999(93)90043-H 8112391
11. Badio B, Daly JW: Epibatidine, a potent analgetic and nicotinic agonist. Mol Pharmacol 1994, 45:563-569. 8183234
12. Sullivan JP, Decker MW, Brioni JD, Donnelly-Roberts D, Anderson DJ, Bannon AW, Kang CH, Adams P, Piattoni-Kaplan M, Buckley MJ: (+/ -)-Epibatidine elicits a diversity of in vitro and in vivo effects mediated by nicotinic acetylcholine receptors. J Pharmacol Exp Ther 1994, 271:624-631. 7965777
13. Genzen JR, McGehee DS: Short- and long-term enhancement of excitatory transmission in the spinal cord dorsal horn by nicotinic acetylcholine receptors. Proc Natl Acad Sci USA 2003, 100:6807-6812. 164528 12748382 10.1073/pnas.1131709100
14. Cordero-Erausquin M, Changeux JP: Tonic nicotinic modulation of serotoninergic transmission in the spinal cord. Proc Natl Acad Sci USA 2001, 27:2803-2807. 10.1073/pnas.041600698
15. Cordero-Erausquin M, Pons S, Faure P, Changeux JP: Nicotine differentially activates inhibitory and excitatory neurons in the dorsal spinal cord. Pain 2004, 109:308-318. 10.1016/j.pain.2004.01.034 15157692
16. Kiyosawa A, Katsurabayashi S, Akaike N, Pang ZP: Nicotine facilitates glycine release in the rat spinal dorsal horn. J Physiol 2001, 536:101-110. 10.1111/j.1469-7793.2001.t01-1-00101.x 11579160
17. Fucile S, Lax P, Eusebi F: Nicotine modulates the spontaneous synaptic activity in cultured embryonic rat spinal cord interneurons. J Neurosci Res 2002, 67:329-336. 10.1002/jnr.10124 11813237
18. Takeda D, Nakatsuka T, Papke R, Gu JG: Modulation of inhibitory synaptic activity by a non-α4β2, non-α7 subtype of nicotinic receptors in the substantia gelatinosa of adult rat spinal cord. Pain 2003, 101:13-23. 10.1016/S0304-3959(02)00074-X 12507696
19. Genzen JR, McGehee DS: Nicotinic modulation of GABAergic synaptic transmission in the spinal cord dorsal horn. Brain Res 2005, 1031:229-237. 10.1016/j.brainres.2004.10.042 15649448
20. Willis WD, Coggeshall RE: Sensory Mechanisms of the Spinal Cord New York: Plenum; 2nd 1991
21. Woolf CJ, King AE: Physiology and morphology of multireceptive neurons with C-afferent fiber inputs in the deep dorsal horn of the rat lumbar spinal cord. J Neurophysiol 1987, 58:460-479. 3655877
22. Singer S, Rossi S, Verzosa S, Hashim A, Lonow R, Cooper T, Sershen H, Lajtha A: Nicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function. Neurochem Res 2004, 29(9):1779-92. 10.1023/B:NERE.0000035814.45494.15 15453274
23. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW: Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 1995, 269:1692-1696. 10.1126/science.7569895 7569895
24. Wang J, Wang X, Irnaten M, Venkatesan P, Evans C, Baxi S, Mendelowitz D: Endogenous acetylcholine and nicotine activation enhances GABAergic and glycinergic inputs to cardiac vagal neurons. J Neurophysiol 2003, 89(5):2473-81. 10.1152/jn.00934.2002 12611951
25. Keiger CJ, Prevette D, Conroy WG, Oppenheim RW: Developmental expression of nicotinic receptors in the chick and human spinal cord. J Comp Neurol 2003, 455:86-99. 10.1002/cne.10468 12454998
26. Lena C, Changeux JP, Mulle C: Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J Neurosci 1993, 13:2680-2688. 8501532
27. Vincler M, Eisenach JC: Plasticity of spinal nicotinic acetylcholine receptors following spinal nerve ligation. Neurosci Res 2004, 48(2):139-45. 10.1016/j.neures.2003.10.007 14741388
28. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lena C, Le Novere N, de Kerchove d'Exaerde A, Huchet M, Damaj MI, Changeux JP: Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 1999, 398:805-810. 10.1038/19756 10235262
29. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, Swanson LW: Distribution of α2, α3, α4, and β2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat. J Comp Neurol 1989, 284:314-335. 10.1002/cne.902840212 2754038
30. Matsubayashi H, Alkondon M, Pereira EF, Swanson KL, Albuquerque EX: Strychnine: A potent competitive antagonist of α-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal neurons. J Pharmacol Exp Ther 1998, 284:904-913. 9495848
31. Garcia-Colunga J, Miledi R: Modulation of nicotinic acetylcholine receptors by strychnine. Proc Natl Acad Sci USA 1999, 30:4113-4118. 10.1073/pnas.96.7.4113
32. Saitoh T, Ishida M, Maruyama M, Shinozaki H: A novel antagonist, phenylbenzene omega-phosphono-alpha-amino acid, for strychnine-sensitive glycine receptors in the rat spinal cord. Br J Pharmacol 1994, 113:165-170. 7812607
33. Bradaïa A Trouslard J Fast synaptic transmission mediated by α-bungarotoxin-sensitive nicotinic acetylcholine receptors in lamina X neurones of neonatal rat spinal cord. J Physiol 2002, 544:727-739. 10.1113/jphysiol.2002.028894 12411519
34. Urban L, Willetts J, Murase K, Randic M: Cholinergic effects on spinal dorsal horn neurons in vitro: An intracellular study. Brain Res 1989, 500:12-20. 10.1016/0006-8993(89)90294-1 2605485
35. Séguéla P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW: Molecular cloning, functional properties, and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. J Neurosci 1993, 13:596-604. 7678857
36. Rashid MH, Ueda H: Neuropathy-specific analgesic action of intrathecal nicotinic agonists and its spinal GABA-mediated mechanism. Brain Res 2002, 953:53-62. 10.1016/S0006-8993(02)03270-5 12384238
37. Damaj MI Meyer EM Martin BR The antinociceptive effects of α7 nicotinic agonists in an acute pain model. Neuropharmacol 2000, 39:2785-2791. 10.1016/S0028-3908(00)00139-8
38. Li X, Eisenach JC: Nicotinic acetylcholine receptor regulation of spinal norepinephrine release. Anesthesiology 2002, 96:1450-1456. 10.1097/ 00000542-200206000-00026 12170059
39. Todd AJ, Spike RC: The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog Neurobiol 1993, 41:609-645. 10.1016/ 0301-0082(93)90045-T 7904359
40. Rashid MH, Furue H, Yoshimura M, Ueda H: Tonic inhibitory role of alpha4beta2 subtype of nicotinic acetylcholine receptors on nociceptive transmission in the spinal cord in mice. Pain 2006, 125(1-2):125-35. 10.1016/j.pain.2006.05.011 16781069
41. Olave MJ, Puri N, Kerr R, Maxwell DJ: Myelinated and unmyelinated primary afferent axons form contacts with cholinergic interneurons in the spinal dorsal horn. Exp Brain Res 2002, 145(4):448-56. 10.1007/ s00221-002-1142-5 12172656
42. Bowker RM, Westlund KN, Sullivan MC, Wilber JF, Coulter JD: Descending serotonergic, peptidergic and cholinergic pathways from the raphe nuclei: A multiple transmitter complex Brain Res 1983, 288:33-48. 10.1016/0006-8993(83)90079-3 6198030
43. Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE: The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: An immunocytochemical study. J Comp Neurol 1984, 229:329-346. 10.1002/cne.902290305 6389613
44. Todd AJ: Immunohistochemical evidence that acetylcholine and glycine exist in different populations of GABAergic neurons in lamina III of rat spinal dorsal horn. Neuroscience 1991, 44:741-746. 10.1016/ 0306-4522(91)90093-4 1754057
45. Baccei ML, Fitzgerald M: Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci 2004, 24(20):4749-57. 10.1523/JNEUROSCI.5211-03.2004 15152035
46. Allain AE, Baïri A, Meyrand P, Branchereau P: Expression of the glycinergic system during the course of embryonic development in the mouse spinal cord and its co-localization with GABA immunoreactivity. J Comp Neurol 2006, 496(6):832-46. 10.1002/cne.20967 16628621
47. Ataka T, Gu JG: Relationship between tonic inhibitory currents and phasic inhibitory activity in the spinal cord lamina II region of adult mice. Mol Pain 2006, 2;2:36. 10.1186/1744-8069-2-36
48. Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M: Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 2000, 99:549-556. 10.1016/S0306-4522(00)00224-4 11029546