Nicotinic cholinergic receptors as targets in pain control

Nicotinic Receptors in the Nervous System

Volumn , Issue , 2001, Pages 113-142

  Damaj, M Imad ^a   Flores, Christopher M ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 1542748317     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (158)

1. Davis, L., Pollock, L.J., and Stone, T.T., Visceral pain, Surg. Gynecol. Obstet., 55, 418-426, 1932.
2. Spande, T., Garraffo, H., Edwards, M., Yeh, H., Pannell, L., and Daly, J., Epibatidine: A novel (chloropyridyl) azabicycloheptane with potent analgesic activity from an Ecuadoran poison frog, J. Am. Chem. Soc., 114, 3475-3478, 1992.
3. Bannon, A.W., Decker, M.W., Holladay, M.W., Curzon, P., Donnelly-Roberts, D., Puttfarcken, P.S., Bitner, R.S., Diaz, A., Dickenson, A.H., Porsolt, R.D., Williams, M., and Arneric, S.P., Broad-spectrum, non-opioid analgesic activity by selective modulation of neuronal nicotinic acetylcholine receptors, Science, 279, 77-81, 1998.
4. Lipton, J.A., Ship, J.A., and Larach-Robinson, D., Estimated prevalence and distribution of reported orofacial pain in the U.S., J. Am. Dent. Assoc., 124, 115-121, 1993.
5. Gilbert, S.D., Clark, T.M., and Flores, C.M., Antihyperalgesic activity of Epibatidine in the formalin model of facial pain, Pain, in press, 2000.
6. Clavelou, P., Pajot, J., Dallel, R., and Raboisson, P., Application of the formalin test to the study of orofacial pain in the rat, Neurosci. Lett., 103, 349-353, 1989.
7. Lawand, N.B., Lu, Y., and Westlund, K.N., Nicotinic cholinergic receptors: potential targets for inflammatory pain relief, Pain, 80, 291-299, 1999.
8. Aceto, M.D., Bagley, R.S., Dewey, W.L., Fu, T.-C., and Martin, B.R., The spinal cord as a major site for the antinociceptive action of nicotine in the rat, Neuropharmacology, 25, 1031-1036, 1986.
9. Christensen, M.-K. and Smith, D.F., Antinociceptive effects of the stereoisomers of nicotine given intrathecally in spinal rats, J. Neural. Transm., 80, 189-194, 1990.
10. Chiari, A., Tobin, J.R., Pan, H.-L., Hood, D.D., and Eisenach, J.C., Sex differences in cholinergic analgesia I, Anesthesiology, 91, 447-454, 1999.
11. Lavand’homme, P.M. and Eisenach, J.C., Sex differences in cholinergic analgesia II, Anesthesiology, 91, 455-461, 1999.
12. Yaksh, T.L., Dirksen, R., and Harty, G.J., Antinociceptive effects of intrathecally injected cholinomimetric drugs in the rat and cat, Eur. J. Pharmacol., 117, 81-88, 1985.
13. Smith, M.D., Yang, X., Nha, J.-Y., and Buccafusco, J.J., Antinociceptive effect of spinal cholinergic stimulation: interaction with substance P, Life Sci., 45, 1255-1261, 1989.
14. Gillberg, P.G., Hartvig, P., Gordh, T., Sottile, A., Jansson, I., Archer, T., and Post, C., Behavioral effects after intrathecal administration of cholinergic receptor agonists in the rat, Psychopharmacology, 100, 464-469, 1990.
15. Khan, I.M., Taylor, P., and Yaksh, T.L., Cardiovascular and behavioral responses to nicotinic agents administered intrathecally, J. Pharmacol. Exp. Ther., 270, 150-158, 1994.
16. Damaj, M.I., Creasy, K.R., Grove, A.D., Rosecrans, J.A., and Martin, B.R., Pharmacological effects of epibatidine optical enantiomers, Brain Res., 664, 34-40, 1994.
17. Damaj, M.I., Creasy, K., Welch, S.P., Rosecrans, J., Aceto, M., and Martin, B.R., Comparative pharmacology of nicotine and ABT-418, a new nicotinic agonist, Psychopharmacology, 120, 483-490, 1995.
18. Damaj, M.I., Fei-Yin, M., Dukat, M., Glassco, W., Glennon, R.A., and Martin, B.R., Antinociceptive responses to nicotinic acetylcholine receptor ligands after systemic and intrathecal administration in mice, J. Pharmacol. Exp. Ther., 284, 1058-1065, 1998.
19. Suh, H.-W., Song, D.K., Lee, K.J., Choi, S.R., and Kim, Y.H., Intrathecally injected nicotine enhances the antinociception induced by morphine but not b-endorphin, DPen2,5-enkephalin and U50,488H administered intrathecally in the mouse, Neuropeptides, 30, 373-378, 1996.
20. Suh, H.W., Song, D.K., Choi, S.R., Chung, K.M., and Kim, Y.H., Nicotine enhances morphine- and b-endorphin-induced antinociception at the supraspinal level in the mouse, Neuropeptides, 30, 479-484, 1996.
21. Zarrindast, M., Nami, A.B., and Farzin, D., Nicotine potentiates morphine antinociception: a possible cholinergic mechanism, Eur. Neuropsychopharmacol, 6, 127-133, 1996.
22. Elgoyhen, A., Johnson, D.S., Boulter, J., Vetter, D., and Heinemann, S., α9: An acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells, Cell, 79, 705-715, 1994.
23. Lewis, P.R. and Shute, C.C.D., Cholinergic pathways in CNS, in Handbook of Psychopharmacology, Vol. 9, L.L. Iversen, S.D. Iversen and S.D. Synder, Eds., Plenum Press, New York, 1978, 315-355.
24. Woolf, N.J., Cholinergic systems in mammalian brain and spinal cord, Prog. Neurobiol., 37, 475-524, 1991.
25. Romano, C. and Goldstein, A., Stereospecific nicotine receptors on rat brain membranes, Science, 210, 647-650, 1980.
26. Marks, M.J. and Collins, A.C., Characterization of nicotine binding in mouse brain and comparison with the binding of α-bungarotoxin and quinuclidinyl benzilate, Mol. Pharmacol., 22, 554-564, 1982.
27. 3H] acetylcholine in rat brain, Mol. Pharmacol., 22, 56-62, 1981.
28. Abood, L.G. and Grassi, S., [3H]methylcarbamylcholine, a new radioligand for studying brain nicotinic receptors, Biochem. Pharmacol., 35, 4199-4202, 1986.
29. 3H]cytisine binding to nicotinic cholinergic receptors in brain, Mol. Pharmacol., 39, 9-12, 1990.
30. Flores, C.M., Rogers, S.W., Pabreza, L.A., Wolfe, B.B., and Kellar, K.J., A subtype of nicotinic cholinergic receptor in the rat brain is composed of α-4 and β-2 subunits and is up-regulated by chronic nicotine treatment, Mol. Pharmacol., 41, 31-37, 1992.
31. Clarke, P.B.S. and Pert, A., Autoradiographic evidence for nicotine receptors on nigrostriatal and mesolimbic dopaminergic neurons, Brain Res., 348, 355-358, 1985.
32. 3H]acetylcholine, [3H]nicotine, and [125I]-α-bungarotoxin, J. Neurosci., 5, 1307-1315, 1985.
33. London, E.D., Connolly, R.J., Szikszay, M., and Wamsley, J.K., Distribution of cerebral metabolic effects of nicotine in the rat, Eur. J. Pharmacol., 110, 391-392, 1985.
34. Boksa, P. and Quirion, R., [3H]N-methyl-carbamylcholine, a new radioligand specific for nicotinic acetylcholine receptors in brain, Eur. J. Pharmacol., 139, 323-333, 1987.
35. 3H]nicotine, Acta. Physiol. Scand., 132, 1-14, 1988.
36. 3H]Epibatidine binding to nicotinic cholinergic receptors in rat and human brain, Mol. Pharmacol., 48, 280-287, 1995.
37. 3-H]Epibatidine labels nicotinic receptors in rat brain: An autoradiographic study, J. Pharmacol. Exp. Ther., 275, 1030-1034, 1995.
38. Salvaterra, P.M. and Moore, W.J., Binding of (125I)-α bungarotoxin to particulate fractions of rat and guinea pig brain, Biochem. Biophys. Res. Commun., 55, 1311-1318, 1973.
39. Polz-Tejera, G. and Schmidt, J., Autoradiographic localisation of α-bungarotoxinbinding sites in the central nervous system, Nature, 258, 349-351, 1975.
40. Schulz, D.W., Loring, R.H., Aizenman, E., and Zigmond, R.E., Autoradiographic localization of putative nicotinic receptors in the rat brain using 125I-neuronal bungarotoxin, J. Neurosci., 11, 287-297, 1991.
41. Schulz, D.W. and Zigmon, R.E., Neuronal bungarotoxin blocks the nicotinic stimulation of endogenous dopamine release from rat striatum, Neurosci. Lett., 98, 310-316, 1989.
42. Llewelyn, M.B., Azami, J., Grant, C.M., and Roberts, M.H.T., Analgesia following microinjection of nicotine into the periaqueductal gray matter, Neurosci. Lett., Suppl. 7, S277, 1981.
43. Guimaraes, A. and Prado, W., Antinociceptive effects of carbachol microinjected into different portions of the mesencephalic periaqueductal gray matter of the rat, Brain Res., 647, 220-230, 1994.
44. Hamann, S.R. and Martin, W.R., Thermally evoked tail avoidance reflex - input-output relationships and their modulation, Brain Res. Bull., 29, 507-509, 1992.
45. Rogers, D. and Iwamoto, E., Multiple spinal mediators in parenteral nicotine-induced antinociception, J. Pharmacol. Exp. Ther., 267, 341-349, 1993.
46. Iwamoto, E.T. and Marion, L., Adrenergic, serotonergic and cholinergic components of nicotinic antinociception in rats, J. Pharmacol. Exp. Ther., 265, 777-789, 1993.
47. Curzon, P., Nikkel, A.L., Bannon, A.W., Arneric, S.P., and Decker, M.W., Differences between the antinociceptive effects of the cholinergic channel activators A-85380 and (+-)-epibatidine in rats, J. Pharmacol. Exp. Ther., 287, 847-853, 1998.
48. Bitner, R.S., Nikkel, A.L., Curzon, P., Arneric, S.P., Bannon, A.W., and Decker, M.W., Role of the nucleus raphe magnus in antinociception produced by ABT-594: Immediate early gene responses possibly linked to neuronal nicotinic acetylcholine receptors on serotonergic neurons, J. Neurosci., 18, 5426-5432, 1998.
49. Iwamoto, E.T., Antinociception after nicotine administration into the mesopontine tegmentum of rats: evidence for muscarinic actions, J. Pharmacol. Exp. Ther., 251, 412-421, 1989.
50. Parvini, S., Hamann, S.R., and Martin, W.R., Pharmacologic characteristics of a medullary hyperalgesic center, J. Pharmacol. Exp. Ther., 265, 286-293, 1993.
51. Flores, C.M. and Hargreaves, K.M., Neuronal nicotinic receptors: new targets in the treatment of pain, in Neuronal Nicotinic Receptors: Pharmacology and Therapeutic Opportunities, S.P. Arneric and J.D. Brioni, Eds., Wiley-Liss, New York, 1998, 359-378.
52. Marubio L. M, Arroyo-Jimenez M. M, Cordero-Erausquin M., Léna C., Le Novère N., de Kerchove d’Exaerde A., Huchet M., Damaj M. I., and Changeux J-P., Reduced antinociception in mice lacking neuronal nicotinic receptor subunits, Nature, 398, 805-810, 1999.
53. Bitner, R.S., Nikkel, A.L., Curzon, P., Donnelly-Roberts, D.L., Puttfarcken, P.S., Namovic, M., Jacobs, I.C., and Meyer, M.D., Reduced nicotinic receptor-mediated antinociception following in vivo antisense knock-down in rat, Brain Res., 871, 66-74, 2000.
54. Bitner, R.S., Nikkel, A.L., Curzon, P., Arneric, S.P., Bannon, A.W., and Decker, M.W., Role of the nucleus raphe magnus in antinociception produced by ABT-594: Immediate early gene responses possibly linked to neuronal nicotinic acetylcholine receptors on serotonergic neurons, J. Neurosci., 18, 5426-5432, 1998.
55. Bannon, A.W., Decker, M.W., Curzon, P., Buckley, M.J., Kim, D.J.B., Radek, R.J., Lynch, J.K., Wasicak, J.T., Lin, N.-H., Arnold, W.H., Holladay, M.W., Williams, M., and Arneric, S.P., ABT-594 [(R)-5-(2-azetidinylnethozy)-2-chloropyridine]: a novel, orally effective antinociceptive agent acting via neuronal nicotinic acetylcholine receptors: II. In vivo characterization, J. Pharmacol. Exp. Ther., 285, 787-794, 1998.
56. Rao, T.S., Correa, L.D., Reid, R.T., and Lloyd, G.K., Evaluation of anti-nociceptive effects of neuronal nicotinic acetylcholine receptor (NAChR) ligands in the rat tailflick assay, Neuropharmacology, 35, 393-405, 1996.
57. Damaj, M.I., Meyer, E.M., and Martin, B.R., The antinociceptive effects of α7 nicotinic agonists in an acute pain model, Neuropharmacology, 39, in press, 2000.
58. Hunt, S. and Schmidt, J., Some observations on the binding patterns of αbungarotoxin in the central nervous system of the rat, Brain Res., 157, 213-232, 1978.
59. Gillberg, P. and Aquilonius, S., Cholinergic, poioid and glycine receptor binding sites localized in human spinal cord by in vitro autoradiography, Acta Neurol. Scand., 72, 299-306, 1985.
60. Gillberg, P.G. and Wiksten, B., Effects of spinal cord lesions and rhizotomies on cholinergic and opiate receptor binding sites in rat spinal cord, Acta Physiol. Scand., 126q, 575-582, 1986.
61. Gillberg, P.G., d’Argy, R., and Aquilonius, S.M., Autoradiographic distribution of [3H]acetylcholine binding sites in the cervical spinal cord of man and some other species, Neurosci. Lett., 90, 197-202, 1988.
62. Bordey, A., Feltz, P., and Trouslard, J., Nicotinic actions on neurons of the central autonomic area in rat spinal cord slices, J. Physiol., 497, 175-187, 1996.
63. Naeff, B., Schlumpf, M., and Lichtensteiger, W., Prenatal and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: an autoradiographic study, Brain Res. Dev. Brain Res., 68, 163-174, 1992.
64. Flores, C.M., Davila-Garcia, M.I., Ulrich, Y.M., and Kellar, K.J., Differential regulation of neuronal nicotinic receptor binding sites following chronic nicotine administration, J. Neurochem., 69, 2216-2219, 1997.
65. Khan, I.M., Yaksh, T.L., and Taylor, P., Epibatidine binding sites and activity in the spinal cord, Brain Res., 753, 269-282, 1997.
66. Ulrich, Y.M., Hargreaves, K.M., and Flores, C.M., A comparison of multiple injections vs. continuous infusion of nicotine for producing up-regulation of neuronal [3H]-epobatidine binding sites, Neuropharmacology, 36, 1119-1125, 1997.
67. Wada, E., Wada, K., Boulter, J., Deneris, E., Heinemann, S., Patrick, J., and Swanson, L., 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., 284, 314-335, 1989.
68. Séguéla, P., Wadiche, J., Dineleymiller, K., Dani, J.A., and Patrick, J.W., Molecular cloning, functional properties, and distribution of rat brain-α7 - a nicotinic cation channel highly permeable to calcium., J. Neurosci., 13, 596-604, 1993.
69. Marks, M.J., Pauly, J.R., Gross, S.D., Deneris, E.S., Hermans-Borgmeyer, I., Heinemann, S.F., and Collins, A.C., Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment, J. Neurosci., 12, 2765-2784, 1992.
70. Dineley-Miller, K. and Patrick, J., Gene transcripts for the nicotinic acetylcholine receptor subunit, β4, are distributed in multiple areas of the rat central nervous system, Mol. Brain Res., 16, 339-344, 1992.
71. Eccles, J.C., Fatt, P., and Koketsu, K., Cholinergic and inhibitory synapses in a parthway from motor-axon collaterals to motoneurons, J. Physiol. (London), 126, 524-562, 1954.
72. Damaj, M.I., Welch, S.P., and Martin, B.R., Nicotine-induced antinociception in mice: role of G-proteins and adenylate cyclase, Pharmacol. Biochem. Behav., 48, 37-42, 1994.
73. Khan, M.M., Marsla, M., Printz, M.P., Taylor, P., and Yaksh, T.L., Intrathecal nicotinc agonist-elicited release of excitatory amino acids as measured by in vivo spinal microdialysis in rats, J. Pharmacol. Exp. Ther., 278, 97-106, 1996.
74. Reuter, L.E., Meyer, M.D., and Decker, M.W., Spinal mechanisms underlying A-85380-induced effects on acute thermal pain, Brain Res., 872, 93-101, 2000.
75. Khan, I.M., Yaksh, T.L., and Taylor, P., Epibatidine binding sites and activity in the spinal cord, Brain Res., 753, 269-282, 1997.
76. Khan, I.M., Buerkle, H., Yaksh, T.L., and Taylor, P., Nociceptive and antinociceptive responses to intrathecally administered nicotinic agonists, Neuropharmacology, 37, 1515-1525, 1998.
77. Donnelly-Roberts, D.L., Puttfarcken, P.S., Kuntzweiler, T.A., Briggs, C.A., Anderson, D.J., Campbell, J.E., Piattoni-Kaplan, M., McKenna, D.G., Wasicak, J.T., Holladay, M.W., Williams, M., and Arneric, S.P., ABT-594 [(R)-5-(2-azetidinylmethoxy)-2-chloropyridine]: a novel, orally effective analgesic acting via neuronal nicotinic acetylcholine receptors: I. In vitro characterization, J. Pharmacol. Exp. Ther., 285, 777-786, 1998.
78. Miao, F.J.-P., Dallman, M.F., Benowitz, N.L., Basbaum, A.I., and Levine, J.D., Adrenal medullary modulation of the inhibition of Bradykinin- induced plasma extravasation by intrathecal nicotine, J. Pharmacol. Exp. Ther., 264, 839-844, 1993.
79. Naguib, M. and Yaksh, T.L., Antinociceptive effects of spinal cholinesterase inhibition and isobolographic analysis of the interaction with µ and α2 receptor systems, Anesthesiology, 80, 1338-1348, 1994.
80. Zhuo, M. and Gebhart, G.F., Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars α in the rat, Brain Res., 550, 35-48, 1991.
81. Langley, J.N. and Dickenson, W.L., On the local paralysis of peripheral ganglia and on the connection of different classes of nerve fibers with them, Proc. Roy Soc. Lond, 46, 423-431, 1889.
82. Langley, J.N., On the reaction of cells and of nerve-endings to certain poisons, chiefly as regards the reaction of striated muscle to nicotine and to curare., J. Physiol., 33, 374-413, 1905.
83. Conti-Tronconi, B.M. and Raftery, M.A., The nicotinic cholinergic receptor: correlation of molecular structure with functional properties, Ann. Rev. Biochem., 51, 491-530, 1982.
84. Popot, J.L. and Changeux, J.P., Nicotinic receptor of acetylcholine: structure of an oligomeric integral membrane protein, Physiol. Rev., 64, 1162-1239, 1982.
85. McCarthy, M.P., Earnest, J.P., Young, E.F., Choe, S., and Stroud, R.M., The molecular neurobiology of the acetylcholine receptor, Ann. Rev. Neurosci., 9, 383-413, 1986.
86. Schechter, N., Handy, I.C., Pezzementi, L., and Schmidt, J., Distribution of α-bungarotoxin binding sites in the central nervous system and peripheral organs of the rat, Toxicon, 16, 245-251, 1978.
87. Polz-Tejera, G., Hunt, S.P., and Schmidt, J., Nicotinic receptors in sensory ganglia, Brain Res., 195, 223-230, 1980.
88. Ninkovic, M. and Hunt, S.P., Alpha-bungarotoxin binding sites on sensory neurons and their axonal transport in sensory afferents, Brain Res., 272, 57-69, 1983.
89. Wada, K., Ballivet, M., Boulter, J., Connolly, J., Wada, E., Deneris, E.S., Swanson, L.W., Heinemann, S., and Patrick, J., Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor, Science, 240, 330-334, 1988.
90. Boyd, R.T., Jacob, M.H., McEachern, A.E., Caron, S., and Berg, D.K., Nicotinic acetylcholine receptor mRNA in dorsal root ganglion neurons, J. Neurobiol., 22, 1-14, 1991.
91. Flores, C.M., DeCamp, R.M., Kilo, S., Rogers, S.W., and Hargreaves, K.M., Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of α3β4, a novel subtyoe in the mammaliam nervous system, J. Neurosci., 16, 7892-7901, 1996.
92. Roberts, R.G.D., Stevenson, J.E., Westerman, R.A., and Pennefather, J., Nicotine acetylcholine receptors on capsaicin-sensitive nerves, NeuroReport, 6, 1578-1582, 1995.
93. Liu, L. and Simon, S.A., Responses of cultured rat trigeminal ganglion neurons to bitter tastants, Chem. Senses, 23, 125-130, 1998.
94. Keiger, C.J. and Walker, J.C., Individual variation in the expression profiles of nicotinic receptors in the olfactory bulb and trigeminal ganglion and identification of α2, α6, α9, and β3 transcripts, Biochem. Pharmacol., 59, 233-240, 2000.
95. Armstrong, D., Dry, R.M.L., Keele, C.A., and Markham, J.W., Observations on chemical excitants of cutaneous pain in man, J. Physiol., 120, 326-351, 1953.
96. Keele, C.A. and Armstrong, D., Substances Producing Pain and Itch, Edward Arnold, London, 1964, 107-123.
97. Jancsò, N., Jancsò-Gabor, S., and Takats, I., Pain and inflammation induced by nicotine, acetylcholine and structurally related compounds and their prevention by desensitizing agents, Acta Physiol., 19, 113-132, 1961.
98. Juan, H., Nicotinic nociceptors on perivascular sensory nerve endings, Pain, 12, 259-264, 1982.
99. Tanelian, D.L., Cholinergic activation of a population of corneal afferent nerves, Exp. Brain Res., 86, 414-420, 1991.
100. Steen, K.H. and Reeh, P.W., Actions of cholinergic agonists and antagonists on sensory nerve endings in rats, in vitro, J. Neurophysiol., 70, 397-405, 1993.
101. Baccaglini, P.I. and Cooper, E., Influences on the expression of acetylcholine receptors on rat nodose neurones in cell culture, J. Physiol., 324, 441-451, 1982.
102. Mandelzys, A., Cooper, E., Verge, V.M., and Richardson, P.M., Nerve growth factor induces functional nicotinic acetylcholine receptors on rat sensory neurons in culture, Neuroscience, 37, 523-50, 1990.
103. Sucher, N.J., Cheng, T.P., and Lipton, S.A., Neural nicotinic acetylcholine responses in sensory neurons from postnatal rat, Brain Res., 533, 248-254, 1990.
104. Liu, L., Identification of acetylcholine receptors in adult rats trigeminal ganglion neurons, Brain Res, 617, 37-42, 1993.
105. Liu, L. and Simon, S.A., Similarities and differences in the currents activated by capsaicin, piperine, and zingerone in rat trigeminal ganglion cells, J. Neurophysiol., 76, 1858-1869, 1996.
106. Puttfarcken, P.S., Manelli, A.M., Arneric, S.P., and Donnelly-Roberts, D.L., Evidence for nicotinic receptors potentially modulating nociceptive transmission at the level of the primary sensory neuron: studies with F11 cells, J. Neurochem., 69, 930-938, 1997.
107. Francel, P.C., Harris, K., Smith, M., Fishman, M.C., Dawson, G., and Miller, R.J., Neurochemical characteristics of a novel dorsal root ganglion X neuroblastoma hybrid cell line, F-11, J. Neurochem., 48, 1624-1641, 1987.
108. Aceto, M.D., Awaya, H., Martin, B.R., and May, E.L., Antinociceptive action of nicotine and its methiodide derivatives in mice and rats, Br. J. Pharmacol., 79, 869-876, 1983.
109. Caggiula, A.R., Epstien, L.H., Perkins, K.A., and Saylor, S., Different methods of assessing nicotine-induced antinociception may engage different neural mechanisms, Psychopharmaacology, 122, 301-306, 1995.
110. Tripathi, H.L., Martin, B.R., and Aceto, M.D., Nicotine-induced antinociception in rats and mice: correlation with nicotine brain levels, J. Pharmacol. Exp. Ther., 221, 91-96, 1982.
111. Bannon, A.W., Decker, M.W., Curzon, P., Buckley, M.J., Kim, D.J.B., Radek, R.J., Lynch, J.K., Wasicak, J.T., Lin, N.-H., Arnold, W.H., Holladay, M.W., Williams, M., and Arneric, S.P., ABT-594 [(R)-5-(2-azetidinylmethoxy)-2-chloropyridine]: a novel, orally effective antinoceiceptive agent acting via neuronal nicotinic acetylcholine receptors: II. In vivo characterization, J. Pharmacol. Exp. Ther., 285, 787-794, 1998.
112. Dussor, G.O., Leong, A.S., Gracia, N.B., Hargreaves, K.M., Arneric, S.P., and Flores, C.M., Differential effects of neuronal nicotinic receptor agonists on capsaicin-evoked CGRP release from peripheral terminals of primary sensory neurons., Soc. Neurosci. Abst., 24, 1625, 1998.
113. Donnelly-Roberts, D.L., Puttfarcken, P.S., Kuntzweiler, T.A., Briggs, C.A., Anderson, D.J., Campbell, J.E., Piattoni-Kaplan, M., McKenna, D.G., Wasicak, J.T., Holladay, M.W., Williams, M., and Arneric, S.P., ABT-594 [(R)-5-(2-azetidinylmethoxy)-2-chloropyridine]: a novel, orally effective analgesic acting via neuronal nicotinic acetylcholine receptors: I. In vitro characterization, J. Pharmacol. Exp. Ther., 285, 777-786, 1998.
114. de la Garza, R., Bickford-Wimer, P.C., Hoffer, B.J., and Freedman, R., Heterogeneity of nicotine actions in the rat cerebellum: an in vivo electrophysiologic study, J. Pharmacol. Exp. Ther., 240, 689-695, 1987.
115. Wong, L.A. and Gallagher, J.P., A direct nicotinic receptor-mediated inhibition recorded intracellularly in vitro, Nature, 341, 439-442, 1989.
116. Wong, L.A. and Gallagher, J.P., Pharmacology of nicotinic receptor-mediated inhibition in rat dorsolateral septal neurones, J. Physiol., 436, 325-346, 1991.
117. Sorenson, E.M. and Gallagher, J.P., The reducing agent dithiothreitol (DTT) does not abolish the inhibitory nicotinic response recorded from rat dorsolateral septal neurons, Neurosci. Lett., 152, 137-140, 1993.
118. Sorenson, E.M. and Gallagher, J.P., The membrane hyperpolarization of rat dorsolateral septal nucleus neurons is mediated by a novel nicotinic receptor, J. Pharmacol. Exp. Ther., 277, 1733-1743, 1996.
119. Fillingim, R.B. and Maixner, W., The influence of resting blood pressure and gender on pain responses, Psychosom. Med., 58, 326-332, 1996.
120. Berkley, K.J., On the dorsal columns: translating basic research hypotheses to the clinic, Pain, 70, 103-107, 1997.
121. Gear, R.W., Gordon, N.C., Heller, P.H., Paul, S., Miaskowski, C., and Levine, J.D., Gender difference in analgesic response to the kappa-opioid pentazocine, Neurosci. Lett., 205, 207-209, 1996.
122. Gear, R.W., Miaskowski, C., Gordon, N.C., Heller, P.H., Paul, S., and Levine, J.D., The kappa opioid nalbuphine produces gender- and dose-dependent analgesia and antianalgesia in patients with postoperative pain, Pain, 83, 339-345, 1999.
123. Craft, R. and Milholland, R., Sex Differences in cocaine- and nicotine-induced antinociception in the rat, Brain Res., 809, 137-140, 1998.
124. Damaj, M.I., Influence of gender and sex hormones on nicotine acute pharmacological effects in mice, J. Pharmacol. Exp. Ther., in press, 2000.
125. Valera, S., Ballivet, M., and Bertrand, D., Progesterone modulates a neuronal nicotinic acetylcholine receptor, Proc. Natl. Acad. Sci. USA, 89, 9949-9953, 1992.
126. Buisson, B. and Bertrand, D., Allosteric modulation of neuronal nicotinic acetylcholine receptors, J. Physiol. (Paris), 92, 89-100, 1998.
127. Bullock, A., Clark, A., Grady, S., Robinson, S., Slobe, B., Marks, M., and Collins, A., Neurosteriods modulate nicotinic receptor function in mouse striatal and thalamic synaptosomes, J. Neurochem., 68, 2412-2423, 1997.
128. Ke, L. and Lukas, R.J., Effects of steroid exposure on ligand binding and functional activities of diverse nicotinic acetylcholine receptor subtypes, J. Neurochem., 67, 1100-1111, 1996.
129. Flores, C.M., Wilson, S.G., and Mogil, J.S., Pharmacogenetic variability in neuronal nicotinic receptor-mediated antinociception, Pharmacogenetics, 9, 619-625, 1999.
130. Poulsen, L., Brosen, K., Arendt-Nielsen, L., Gram, L.F., Elbaek, K., and Sindrup, S.H., Codeine and morphine in extensive and poor metabolizers of sparteine: pharmacokinetics, analgesic effect and side effects., Eur. J. Clin. Pharmacol., 51, 289-295, 1996.
131. Benowitz, N.L. and Jacob, P.I., Individual differences in nicotine kinetics and metabolism in humans, NIDA Res. Monogr., 173, 48-64, 1997.
132. Nakajima, M., Yamagishi, S., Yamamoto, H., Yamamoto, T., Kuroiwa, Y., and Yokoi, T., Deficient cotinine formation from nicotine is attributed to the whole deletion of the CYP2A6 gene in humans, Clin. Pharmacol. Ther., 67, 57-69, 2000.
133. Yamazaki, H., Inoue, K., Hashimoto, M., and Shimada, T., Roles of CYP2A6 and CYP2B6 in nicotine C-oxidation by human liver microsomes, Arch. Toxicol., 73, 65-70, 1999.
134. Collins, A.C. and Marks, M.J., Genetic studies of nicotinic and muscarinic agents. in The Genetic Basis of Alcohol and Drug Actions, J.C. Crabbe Jr., and R.A. Harris, Eds., Plenum Press, New York, 1991, 323-352.
135. Seale, T.W., Nael, R., and Basmadjian, G., Inherited, selective hyporesponsiveness to the analgesic action of nicotine in mice, NeuroReport, 8, 191-195, 1996.
136. Seale, T.W., Nael, R., Singh, S., and Basmadjian, G., Inherited, selective hypoanalgesic response to cytisine in the tail-flick test in CF-1 mice, NeuroReport, 9, 201-205, 1998.
137. Schachter, S., Pharmacological and psychological determinants of smoking, Ann. Int. Med., 88, 104-114, 1978.
138. Silverstein, B., Cigarette smoking, nicotine addiction, and relaxation, J. Pers. Soc. Psychol., 42, 946-950, 1982.
139. Pomerleau, C.S., Nicotine as a psychoactive drug: anxiety and pain reduction, Psychopharmacol. Bull., 22, 865-869, 1986.
140. Nesbitt, P.D., Smoking, physiological arousal, and emotional response, J. Pers. Soc. Psychol., 25, 137-144, 1973.
141. Milgrom-Friedman, J., Penman, R., and Meares, R., A preliminary study on pain perception and tobacco smoking, Clin. Exp. Pharmacol. Physiol., 10, 161-169, 1983.
142. Lane, J., Rose, J., Lefebvre, J., and Keefe, F., Effects of cigarette smoking on perception of thermal pain, Exp. Clin. Psychopharmacol., 3, 140-147, 1995.
143. Pauli, P., Rau, H., Zhuang, P., Brody, S., and Birbaumer, N., Effects of smoking on thermal pain thresholds in deprived and minimally-deprived habitual smokers, Psychopharmacology., 111, 472-476, 1993.
144. Perkins, K., Epstein, L., Grobe, J., and Fonte, C., Tobacco abstinence, smoking cues, and the reinforcing value of smoking, Pharmacol. Biochem. Behav., 47, 107-112, 1994.
145. Fertig, J.B. and Pomerleau, O.F., Nicotine-produced antinociception in minimally deprived smokers and exsmokers, Addic. Behav., 11, 239-248, 1986.
146. Sult, S.C. and Moss, R.A., The effects of cigarette smoking on the perception of electrical stimulation and cold pressor pain, Addic. Behav., 11, 447-451, 1986.
147. Waller, D., Schalling, D., Levander, S., and Edman, G., Smoking, pain tolerance, and physiological activation, Psychopharmacology, 79, 193-198, 1983.
148. Shiffman, S. and Jarvik, M.E., Cigarette smoking, physiological arousal, and emotional response: Nesbitt’s paradox re-examined, Addic. Behav., 9, 95-98, 1984.
149. Knott, V.J. and De Lugt, D., Subjective and brain-evoked responses to electrical pain stimulation: effects of cigarette smoking and warning condition, Pharmacol. Biochem. Behav., 39, 889-893, 1991.
150. Perkins, K.A., Grobe, J.E., Stiller, R.L., Scierka, A., Goettler, J., Reynolds, W.A., and Jennings, J.R., Effects of nicotine on thermal pain detection in humans, Exp. Clin. Psychopharmacol., 2, 95-106, 1994.
151. Jamner, L., Girdler, S., Shapiro, D., and Jarvik, M., Pain Inhibition, Nicotine, and Gender, Exp. Clin. Psychopharmacol., 6, 96-106, 1998.
152. Kesingland, A.C., Gentry, C.T., Panesar, M.S., Bowes, M.A., Vernier, J.-M., Cube, R., Walker, K., and Urban, L., Analgesic profile of the nicotinic acetylcholine receptor agonists, (+)-epibatidine and ABT-594 in models of persistent inflammatory and neuropathic pain, Pain, 86, 113-118, 2000.
153. Boyce, S., Webb, J.K., Shepheard, M.G.N., Russell, R.G., Hill, R.G., and Rupniak, N.M.J., Analgesic and toxic effects of ABT-594 resemble epibatidine and nicotine in rats, Pain, 85, 443-450, 2000.
154. Bencherif, M., Lovette, M.E., Fowler, K.W., Arrington, S., Reeves, L., Caldwell, W.S., and Lippiello, P.M., RJR-2403: a nicotinic agonist with CNS selectivity I. In vitro characterization, J. Pharmacol Exp. Ther., 279, 1413-1421, 1996.
155. Lippiello, P.M., Bencherif, M., Gray, J.A., Peters, S., Grigoryan, G., Hodges, H., and Collins, A.C., RJR-2403: a nicotinic agonist with CNS selectivity II. In vivo characterization, J. Pharmacol. Exp. Ther., 279, 1422-1429, 1996.
156. Damaj, M.I., Glassco, W., Aceto, M.D., and Martin, B.R., Antinociceptive and pharmacological effects of metanicotine, a selective nicotinic agonist, J. Pharmacol. Exp. Ther., 291, 390-398, 1999.
157. Decker, M.W., Bannon, A.W., Buckley, M.J., Kim, D.J.B., Holladay, M.W., Ryther, K.B., Lin, N.-H., Wasicak, J.T., Williams, M., and Arneric, S.P., Antinociceptive effects of the novel neuronal nicotinic acetylcholine receptor agonist, ABT-594, in mice, Eur. J. Pharmacol., 346, 23-33, 1998.
158. Inoue, K., Yamazaki, H., Shimada, T., CYP2A6 genetic polymorphisms and liver microsomal coumarin and nicotine oxidation activities in Japanese and Caucasians, Arch. Toxicol., 73, 532-539, 2000.