Nicotine Inhibits Voltage-Dependent Sodium Channels and Sensitizes Vanilloid Receptors

Journal of Neurophysiology

Volumn 91, Issue 4, 2004, Pages 1482-1491

  Liu, L ^a   Zhu, W ^b   Zhang, Z S ^a   Yang, T ^a   Grant, A ^a   Oxford, G ^b   Simon, S A ^a,c  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CAPSAICIN; NICOTINE; NICOTINIC RECEPTOR; SODIUM ION; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; GUSTATORY SYSTEM; HUMAN; HUMAN CELL; INFLAMMATION; NOCICEPTION; NONHUMAN; PAIN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SODIUM CURRENT; SODIUM TRANSPORT; TEMPERATURE DEPENDENCE; TRIGEMINUS GANGLION;

ANIMALS; CAPSAICIN; CELLS, CULTURED; CRICETINAE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC CONDUCTIVITY; EMBRYO; HUMANS; ION CHANNEL GATING; KIDNEY; MECAMYLAMINE; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONS; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DRUG; SODIUM CHANNELS; TRIGEMINAL GANGLION;

EID: 1542615229     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00922.2003     Document Type: Article

References (70)

1. Alimohammadi H and Silver WL. Evidence for nicotinic acetylcholine receptors on nasal trigeminal nerve endings of the rat. Chem Senses 25: 61-66, 1999.
2. Armett CJ and Ritchie JM. The action of acetylcholine and some related substances on conduction in mammalian non-myelinated nerve-fibers. J Physiol 155: 372-384, 1961.
3. Baccaglini PI and Hogan PG. Some rat sensory neurons in culture express characterictics of differentiated pain cells. Proc Natl Acad Sci USA 80: 594-598, 1983.
4. + channels in pain pathways. Trends Pharmacol Sci 22: 27-31, 2001.
5. Bannon AW, Decker MW, and Arneric SP. Broad spectrum, non-opioid analgesic activity by selective modulation of neuronal nicotinic receptors. Science 279: 77-81, 1998.
6. Bergren DR. Chronic tobacco smoke exposure increases airway sensitivity to capsaicin in awake guinea pigs. J Appl Physiol 90: 695-704, 2001.
7. Carstens E, Andersen KA, Simons CT, Carstens MI, and Jinks SL. Analgesia induced by chronic nicotine infusion in rats: differences by gender and pain. Psychopharmacology 157: 40-45, 2001.
8. Carstens E, Andersen KA, Simons CT, Carstens MI, and Jinks SL. Analgesia induced by chronic nicotine infusion in rats: differences by gender and pain. Psychopharmacology 157:40-45, 2001.
9. Carstens E, Kuenzler N, and Handwerker KO. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to the oral or ocular mucosa. J Neurophysiol 80: 465-492, 1998.
10. Caterina MJ, Schunmacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
11. + channels expressed in mammalian cells. Am J Physiol Heart Circ Physiol 274: H1643-H1654, 1998.
12. Damaj MI and Flores CF. Nicotinic cholinergic receptors as targets in pain control. In: Nicotinic Receptors in the Nervous System, edited by Levin ED. Boca Raton, FL CRC, 2002, p. 113-142.
13. Docherty RJ, Robertson B, and Bevan S. Capsaicin causes prolonged inhibition of voltage-activated calcium currents in adult dorsal root ganglion neurons in culture. Neuroscience 40: 513-521, 1991.
14. Dressier JM, Nguyn N, Sieffermann JM, Carstens E, and O'Mahoney M. Oral irritant properties of piperine and nicotine: psychophysical evidence for asymmetrical desensitization effects. Chem Senses 24: 405-413, 1999.
15. Dressirier J-M, O'Mahoney M, and Carstens E. Oral irritant effects of nicotine: psychophysical evidence for decreased sensation following repeated application and lack of cross-desensitization to capsaicin. Ann NY Acad Sci 855: 828-830, 1998a.
16. Dressier JM, O'Mahoney M, Sieffermann JM, and Carstens E. Mecamylamine inhibits nicotine but not capsaicin irritation on the tongue: psychophysical evidence that nicotine and capsaicin activate separate receptors. Neurosci Lett 240: 65-68, 1998b.
17. Duner-Engstrom M, Fredholm BB, Larsson O, Lundberg JM, and Saria A. Autonomic mechanisms underlying capsaicin induced oral sensations and salivation in man. J Physiol 373: 87-95, 1986.
18. Dussor GO, Leong AS, Gracia NB, Hargreaves KM, Arneric SP, and Flores CM. Differential effects of neuronal nicotinic receptor agonists on capcaicin-evoked CGRP release from peripheral terminals of primary sensory neurons. Soc Neurosci Abstr 24: 1625, 1998.
19. Dussor GO, Leong AS, Gracia NB, Price TJ, Hargreaves KM, and Flores CM. Potentiation of evoked CGRP release from oral mucosa: a potential basis for the pro-inflammatory effects of nicotine. Eur J Neurosci 18: 2515-2526, 2003.
20. Frazier DT, Sevick C, and Narahashi T. Nicotine: effect on nerve membrane conductance. Eur J Pharmacol 22: 217-220, 1973.
21. Geppetti P, Bertrand C, Baker J, Yamawaki I, Piedimonte G, and Nadel JA. Ruthenium red but not capsazepine reduces plasma extravasation by cigarette smoke in rat airways. Br J Pharmacol 108: 646-650, 2003.
22. Gold MS, Dastmalchi S, and Levine JD. Co-expression of nociceptor properties in the dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71: 265-275, 1996.
23. Green BG. Capsaicin sensitization and desensitization on the tongue produced by brief exposures to a low concentration. Neurosci Lett 107: 173-178, 1989.
24. + channels, Types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45: 1227-1234, 1994.
25. Gunthorpe MJ, Benham CD, Randall A, and Davis JB. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci 23: 183-191, 2002.
26. Henkel G. Effects of oleamide on tetrodotoxin-sensitive sodium channels investigated. Anesthesiology 94: A5-A6, 2003.
27. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer. 1993.
28. Hui K, Liu B, and Qin F. Capsaicin activation of the pain receptor. VR1: multiple open states from both partial and full binding. J Gen Physiol 84: 2957-2968, 2003.
29. Jansco N, Jansco-Gabor A, and Takats I. Pain and inflammation induced by nicotine. Acta Physiol 19: 113-132, 1961.
30. Jarvik ME and Assil KM. Mecamylamine blocks the burning sensation of nicotine on the tounge. Chem Senses 13: 213-218, 1988.
31. Jinks SL and Carstens E. Activation of spinal wide dynamic range neurons by intracutaneous microinjection of nicotine. J Neurophysiol 82: 3046-3055, 1999.
32. Jung J, Lee S-Y, Hwang PW, Cho H, Shin J, Kang Y-S, Kim S, and Oh U. Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. J Biol Chem 277: 4448-4454, 2003.
33. Kim H-C, Chung M-K, Kim J-S, and Lee J-H. Voltage-dependent sodium and calcium currents in acutely isolated adult rat trigeminal root ganglion neurons. J Neurophysiol 81: 1123-1134, 1999.
34. Kiyosawa A, Katsurabayashi S, Akaike N, Pang ZP, and Akaike N. Nicotine facilitates glycine release in the rat spinal dorsal horn. Physiol 536: 101-110, 2001.
35. Kuzhikandathil EV, Wang H, Szabo T, Morozova N, Blumberg PM, and Oxford GS. Functional analysis of capsaicin receptor (vanilloid receptor subtype 1) multimerization and agonist responsiveness using a dominant negative mutation. J Neurosci 15: 8697-8706, 2001.
36. Kwak J, Wang MH, Hwang SW, Kim T-Y, Lee S-Y, and Oh U. Intracellular ATP increases capsaicin-activated channel activity by interacting with nucleotide-binding domains. J Neurosci 20: 8298-8304, 2000.
37. Lindstrom J. Nicotinic receptors in health and disease. Mol Neurobiol 15: 193-222, 1997.
38. Liu L, Oortgiesen M, Li L, and Simon SA. Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive neurons. J Neurophysiol 85: 745-758, 2001.
39. Liu L and Simon SA. Capsaicin and nicotine both activate a subset of rat trigeminal ganglion neurons. Am J Physiol Cell Physiol 270: C1807-C1814, 1996.
40. Liu L and Simon SA. Capsazepine, a vanilloid receptor antagonist, inhibits nicotinic acetylcholine receptors in rat trigeminal ganglia. Neurosci Lett 228: 29-32, 1997.
41. Liu L, and Simon SA. Capsaicin, acid and heat evoked currents in rat trigeminal ganglion neurons: evidence for functional VR1 receptors. Physiol Behav 69: 363-378, 2000.
42. Liu L and Simon SA. Modulation of 1A currents by capsaicin in rat trigeminal ganglion neurons. J Neurophysiol 89: 1347-1401, 2003.
43. Liu L, Szallasi A, and Simon SA. A non-pungent resiniferatoxin analogue, phorbol 12 phenylacetate 13 20-homovanillate reveals receptor subtypes on rat triegminal ganglion neurons. Neuroscience 84: 569-581, 1998.
44. Lundbaek JA and Andersen OS. Lysophospholipids modulate channel function by altering the mechanics properties of lipid bilayers. J Gen Physiol 104: 645-673, 1994.
45. Lundback JA and Andersen OS. Spring constants for channel-induced lipid bilayer deformations estimates using gramicidin channels. Biophys J 76: 889-895, 1999.
46. Lundherg JM. Tachykinins, sensory nerves, and asthma. Can J Physiol Pharmacol 73: 908-914, 1995.
47. Nakazawa K, Inoue K, Koizumi K, and Ikeda M. Inhibitory effects of capsaicin on acetylcholine-evoked responses in rat phacochromocytoma cells. Br J Pharmacol 113: 296-302, 1994.
48. Papke RL, Sanberg PR, and Shytle RD. Analysis of mecamylamine stereo-isomers on human nicotinic receptor subtypes. J Pharmacol Exp Ther 297: 646-656, 2001.
49. Petersen M and LaMotte RH. Relationships between capsaicin sensitivity of mammalian sensory neurons. Brain Res 561: 20-26, 1991.
50. Petersen M, Pierau Fr-K, and Weyrich M. The influence of capsaicin on membrane currents in dorsal root neurons of the guinea pig and chicken. Pfluegers 409: 403-410, 1987.
51. Petersen M, Wagner G, and Pierau F-K. Modulation of calcium currents by capsaicin in a Subppopulation of sensory neurons in guinea pig. Naunyn-Schimiederg's Arch Pharmacol 339: 184-191, 1989.
52. Petruska JC, Napaporn J, Johnson RD, Gu JG, and Cooper BY. Subclassified acutely dissociated cells of rat DRG: Histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84: 2365-2379, 2000.
53. Phan DV, Doda M, Bite A, and Gyorgy L. Antinociceptive activity of nicotine. Acta Physiol Acad Sci Hung 44: 85-93, 1973.
54. 2 binding site as a determinant of capsaicin receptor sensitivity. Science 300: 1284-1288, 2003.
55. Puttfarcken PS, Manelli AM, Arneric SP, and Donnelly-Roberts DL. 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.
56. Role LW and Berg DK. Nicotinic receptors, in the development and modulation of CNS synapses. Neuron 16: 1077-1085, 1996.
57. Sekizawa SI and Tsubone H. Nasal receptors, responding to noxious chemical irritants. Respir Physiol 96: 37-48, 1994.
58. Sigworth FJ. Life's transistors. Nature 423: 21-22, 2003.
59. Silver WL and Finger TE. The trigeminal system. In: Smell and Taste in Health and Disease, edited by Getchell TV. New York: Raven. 1991. p. 97-108.
60. Stadnicka A, Kwok W-M, and Bosnjak ZJ. Effects of Halothane and Isoflurane on fast and slow inactivation of human heart hHla sodium channels. Anesthesiology 90: 1671-1683, 1999.
61. Steen K and Reeh PW. Actions of cholinergic cholinergic agonists on sensory nerve endings in rat skin vivo. J Neurophysiol 70: 397-405, 1993.
62. Sterner O and Szallasi A. Novel natural vanilloid receptor agonists: new therapeutic target's for drug development. Trends Pharmacol Sci 20: 459-465, 1999.
63. Stucky CL, and Lewin GR. Isolectin B-4-positive and -negative nociceptors are functionally distinct. J Neurosci 19: 6497-6505, 1999.
64. Su X, Wachtel RE, and Gebhart GF. Capsaicin sensitivity and voltage-gated sodium currents in colon sensory neurons from rat dorsal root ganglia. Am J Physiol Gastrointest Liver Physiol 277: G1180-G1188, 1999.
65. Szallasi A and Blumberg PM. Mechanisms and therapeutic potential of vanilloids (capsaicin-like molecules). Adv Pharmacol 24: 123-155, 1993.
66. Tanelian DL. Cholinergic activation of a population of corneal afferent nerves. Exp Brain Res 86: 414-420, 1991.
67. Trevisani M, Smart D, Gunthorpe MJ, Tognetto M, Barbry P, Campi B, Amadesi S, Grey J, Jerman JC, Brough SJ, Owen D, Smith GD, Randall AD, Harrison S, Bianchi A, Davis JB, and Geppetti P. Ethanol elicits and potentates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5: 546-551, 2002.
68. Tripathi HL, Martin BR, and Aceto MD. Nicotine induced antinociception in rats and mice: correlation with brain nicotine levels. J Pharmacol Exp Ther 221: 91-96, 1982.
69. Walker JC, Kendal-Reed M, Keiger CJ, Bencherif M, and Silver WL. Olfactory and trigeminal responses to nicotine. Drug Dev Res 38: 160-168, 1996.
70. Yang C-Y, Wu WH, and Zbuzek VK. Antinociceptive effect of chronic nicotine and nociceptive effect of its withdrawl measured by hot-plate and tail-flick in rats. Psychopharmacology 106: 417-420, 1992.