Cigarette smoke has sensory effects through nicotinic and TRPA1 but not TRPV1 receptors on the isolated mouse trachea and larynx

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 8, 2015, Pages L812-L820

  Kichko, Tatjana I ^a   Kobal, Gerd ^b   Reeh, Peter W ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b Altria Client Services Inc   (United States)

Author keywords

Camphor; Gas phase; Mecamylamine; Particulate matter

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CIGARETTE SMOKE; MECAMYLAMINE; N (4 TERT BUTYLPHENYL) 4 (3 CHLORO 2 PYRIDINYL) 1 PIPERAZINECARBOXAMIDE; NICOTINE; NICOTINIC RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1; SMOKE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPA1 PROTEIN, MOUSE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DESENSITIZATION; FEMALE; GAS; ISOLATED ORGAN; LARYNX; LIMIT OF DETECTION; MALE; MOUSE; MOUSE LARYNX; MOUSE TRACHEA; NONHUMAN; PARTICULATE MATTER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; SENSORY NERVE CELL; SMOKING; TRACHEA; WILD TYPE; ADVERSE EFFECTS; ANALYSIS; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; HUMAN; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; SMOKE;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; FEMALE; HUMANS; IN VITRO TECHNIQUES; LARYNX; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, NICOTINIC; SENSORY RECEPTOR CELLS; SMOKE; SMOKING; TRACHEA; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS;

EID: 84944455948     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00164.2015     Document Type: Article

References (43)

1. Agopyan N, Head J, Yu S, Simon SA. TRPV1 receptors mediate particulate matter-induced apoptosis. Am J Physiol Lung Cell Mol Physiol 286: L563-L572, 2004.
2. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM. Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol 583: 175-193, 2007.
3. Andrè E, Campi B, Materazzi S, Trevisani M, Amadesi S, Massi D, Creminon C, Vaksman N, Nassini R, Civelli M, Baraldi PG, Poole DP, Bunnett NW, Geppetti P, Patacchini R. Cigarette smoke-induced neurogenic inflammation is mediated by alpha,beta-unsaturated aldehydes and the TRPA1 receptor in rodents. J Clin Invest 118: 2574-2582, 2008.
4. Asgharian B, Price OT, Schroeter JD, Kimbell JS, Singal M. A lung dosimetry model of vapor uptake and tissue disposition. Inhal Toxicol 24: 182-193, 2012.
5. Averbeck B, Reeh PW. Interactions of inflammatory mediators stimulating release of calcitonin gene-related peptide, substance P and prostaglandin E(2) from isolated rat skin. Neuropharmacology 40: 416-423, 2001.
6. Bang S, Kim KY, Yoo S, Kim YG, Hwang SW. Transient receptor potential A1 mediates acetaldehyde-evoked pain sensation. Eur J Neurosci 26: 2516-2523, 2007.
7. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282, 2006.
8. Bernardini N, Roza C, Sauer SK, Gomeza J, Wess J, Reeh PW. Muscarinic M2 receptors on peripheral nerve endings: a molecular target of antinociception. J Neurosci 22: RC229, 2002.
9. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405: 183-187, 2000.
10. Djordjevic MV, Bush LP, Gay SL, Burton HR. Accumulation and distribution of acylated nornicotine derivatives in flue-cured tobacco alkaloid isolines. J Agric Food Chem 38: 347-350, 1990.
11. Feng Y, Kleinstreuer C, Rostami A. Evaporation and condensation of multicomponent electronic cigarette droplets and conventional cigarette smoke particles in an idealized G3-G6 triple bifurcating unit. J Aerosol Sci 80: 58-74, 2015.
12. Fischer M, Carli G, Raboisson P, Reeh P. The interphase of the formalin test. Pain 155: 511-521, 2014.
13. Hoffmann D, Hoffmann I, El-Bayoumy K. The less harmful cigarette: a controversial issue. A tribute to Ernst L Wynder. Chem Res Toxicol 14: 767-790, 2001.
14. Hummel T, Livermore A, Hummel C, Kobal G. Chemosensory eventrelated potentials in man: relation to olfactory and painful sensations elicited by nicotine. Electroencephalogr Clin Neurophysiol 84: 192-195, 1992.
15. Kichko TI, Lennerz J, Eberhardt M, Babes RM, Neuhuber W, Kobal G, Reeh PW. Bimodal concentration-response of nicotine involves the nicotinic acetylcholine receptor, transient receptor potential vanilloid type 1, and transient receptor potential ankyrin 1 channels in mouse trachea and sensory neurons. J Pharmacol Exp Ther 347: 529-539, 2013.
16. Krasteva G, Canning BJ, Hartmann P, Veres TZ, Papadakis T, Mühlfeld C, Schliecker K, Tallini YN, Braun A, Hackstein H, Baal N, Weihe E, Schütz B, Kotlikoff M, Ibanez-Tallon I, Kummer W. Cholinergic chemosensory cells in the trachea regulate breathing. Proc Natl Acad Sci USA 108: 9478-9483, 2011.
17. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50: 277-289, 2006.
18. Lee LY, Burki NK, Gerhardstein DC, Gu Q, Kou YR, Xu J. Airway irritation and cough evoked by inhaled cigarette smoke: role of neuronal nicotinic acetylcholine receptors. Pulm Pharmacol Ther 20: 355-364, 2007.
19. Liu BY, Tsai TL, Ho CY, Lu SH, Lai CJ, Kou YR. Role of TRPA1 and TRPV1 in the ROS-dependent sensory irritation of superior laryngeal capsaicin-sensitive afferents by cigarette smoke in anesthetized rats. Pulm Pharmacol Ther 26: 364-372, 2013.
20. Liu L, Simon SA. Capsazepine, a vanilloid receptor antagonist, inhibits nicotinic acetylcholine receptors in rat trigeminal ganglia. Neurosci Lett 228: 29-32, 1997.
21. Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA. Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 91: 1482-1491, 2004.
22. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, Fanger CM. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA 104: 13525-13530, 2007.
23. Osawa Y, Tochigi B, Tochigi M, Ohnishi S, Watanabe Y, Bullion K, Osawa G, Nakabayashi Y, Yarborough C. Aromatase inhibitors in cigarette smoke, tobacco leaves and other plants. J Enzym Inhib 4: 187-200, 1990.
24. Pang X, Lewis AC. Carbonyl compounds in gas and particle phases of mainstream cigarette smoke. Sci Total Environ 409: 5000-5009, 2011.
25. Pankow JF. A consideration of the role of gas/particle partitioning in the deposition of nicotine and other tobacco smoke compounds in the respiratory tract. Chem Res Toxicol 14: 1465-1481, 2001.
26. Papke RL. Tricks of perspective: insights and limitations to the study of macroscopic currents for the analysis of nAChR activation and desensitization. J Mol Neurosci 40: 77-86, 2010.
27. Picciotto MR, Addy NA, Mineur YS, Brunzell DH. It is not “either/or”: activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog Neurobiol 84: 329-342, 2008.
28. Pouli AE, Hatzinikolaou DG, Piperi C, Stavridou A, Psallidopoulos MC, Stavrides JC. The cytotoxic effect of volatile organic compounds of the gas phase of cigarette smoke on lung epithelial cells. Free Radic Biol Med 34: 345-355, 2003.
29. Rickert WS, Wright WG, Trivedi AH, Momin RA, Lauterbach JH. A comparative study of the mutagenicity of various types of tobacco products. Regul Toxicol Pharmacol 48: 320-330, 2007.
30. Roemer E, Schorp MK, Piadé JJ, Seeman JI, Leyden DE, Haussmann HJ. Scientific assessment of the use of sugars as cigarette tobacco ingredients: a review of published and other publicly available studies. Crit Rev Toxicol 42: 244-278, 2012.
31. Ruparel NB, Patwardhan AM, Akopian AN, Hargreaves KM. Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain 135: 271-279, 2008.
32. Selescu T, Ciobanu AC, Dobre C, Reid G, Babes A. Camphor activates and sensitizes transient receptor potential melastatin 8 (TRPM8) to cooling and icilin. Chem Senses 38: 563-575, 2013.
33. Steen KH, Reeh PW. Actions of cholinergic agonists and antagonists on sensory nerve endings in rat skin, in vitro. J Neurophysiol 70: 397-405, 1993.
34. Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, Viana F, Nemery B, Nilius B, Voets T. Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci 12: 1293-1299, 2009.
35. Tanelian DL. Cholinergic activation of a population of corneal afferent nerves. Exp Brain Res 86: 414-420, 1991.
36. Thuerauf N, Kaegler M, Dietz R, Barocka A, Kobal G. Dose-dependent stereoselective activation of the trigeminal sensory system by nicotine in man. Psychopharmacology (Berl) 142: 236-243, 1999.
37. Thuerauf N, Markovic K, Braun G, Bleich S, Reulbach U, Kornhuber J, Lunkenheimer J. The influence of mecamylamine on trigeminal and olfactory chemoreception of nicotine. Neuropsychopharmacology 31: 450-461, 2006.
38. Uchiyama S, Tomizawa T, Inaba Y, Kunugita N. Simultaneous determination of volatile organic compounds and carbonyls in mainstream cigarette smoke using a sorbent cartridge followed by two-step elution. J Chromatogr A 1314: 31-37, 2013.
39. Valenzano KJ, Grant ER, Wu G, Hachicha M, Schmid L, Tafesse L, Sun Q, Rotshteyn Y, Francis J, Limberis J, Malik S, Whittemore ER, Hodges D. N-(4-tertiarybutylphenyl)-4-(3-chloropyridin-2-yl)tetrahydropyrazine- 1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: I. In vitro characterization and pharmacokinetic properties. J Pharmacol Exp Ther 306: 377-386, 2003.
40. Vetter I, Hein A, Sattler S, Hessler S, Touska F, Bressan E, Parra A, Hager U, Leffler A, Boukalova S, Nissen M, Lewis RJ, Belmonte C, Alzheimer C, Huth T, Vlachova V, Reeh PW, Zimmermann K. Amplified cold transduction in native nociceptors by M-channel inhibition. J Neurosci 33: 16627-16641, 2013.
41. Weng WH, Hsu CC, Chiang LL, Lin YJ, Lin YS, Su CL. Role of TRPV1 and P2X receptors in the activation of lung vagal C-fiber afferents by inhaled cigarette smoke in rats. Mol Med Rep 7: 1300-1304, 2013.
42. Xu H, Blair NT, Clapham DE. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid independent mechanism. J Neurosci 25: 8924-8937, 2005.
43. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110, 1983.