The role of trigeminal nasal TRPM8-expressing afferent neurons in the antitussive effects of menthol

Journal of Applied Physiology

Volumn 115, Issue 2, 2013, Pages 268-274

  Plevkova, J ^a   Kollarik, M ^b   Poliacek, I ^a   Brozmanova, M ^a   Surdenikova, L ^a   Tatar, M ^a   Mori, N ^b   Canning, B J ^b  

^a Faculty of Medicine of Comenius University and University Hospital Bratislava   (Slovakia)

^b JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

Cough; Turbinate; Vagal

Indexed keywords

ANTITUSSIVE AGENT; MENTHOL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M;

ANIMAL; ARTICLE; BREATHING; COLD; COUGHING; DRUG EFFECT; GENETICS; GUINEA PIG; INNERVATION; MALE; METABOLISM; NOSE; REFLEX; SENSORY NERVE CELL; TRACHEA; TRIGEMINAL NERVE; TURBINATE; VAGAL;

COUGH; TURBINATE; VAGAL;

ANIMALS; ANTITUSSIVE AGENTS; COLD TEMPERATURE; COUGH; GUINEA PIGS; MALE; MENTHOL; NEURONS, AFFERENT; NOSE; REFLEX; RESPIRATION; TRACHEA; TRIGEMINAL NERVE; TRPM CATION CHANNELS;

EID: 84880527311     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01144.2012     Document Type: Article

References (57)

1. Abe J, Hosokawa H, Okazawa M, Kandachi M, Sawada Y, Yamanaka K, Matsumura K, Kobayashi S. TRPM8 protein localization in trigeminal ganglion and taste papillae. Brain Res Mol Brain Res 136: 91-98, 2005.
2. Almeida MC, Hew-Butler T, Soriano RN, Rao S, Wang W, Wang J, Tamayo N, Oliveira DL, Nucci TB, Aryal P, Garami A, Bautista D, Gavva NR, Romanovsky AA. Pharmacological blockade of the cold receptor TRPM8 attenuates autonomic and behavioral cold defenses and decreases deep body temperature. J Neurosci 32: 2086-2099, 2012.
3. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208, 2007.
4. Brozmanova M, Plevkova J, Tatar M, Kollarik M. Cough reflex sensitivity is increased in the guinea pig model of allergic rhinitis. J Physiol Pharmacol 59, Suppl 6: 153-161, 2008.
5. Buday T, Brozmanova M, Biringerova Z, Gavliakova S, Poliacek I, Calkovsky V, Shetthalli MV, Plevkova J. Modulation of cough response by sensory inputs from the nose - role of trigeminal TRPA1 versus TRPM8 channels. Cough 8: 11, 2012.
6. Canning BJ, Mori N, Farmer DG. Mechanistic studies of acid-evoked coughing in anesthetized guinea pigs. Am J Physiol Regul Integr Comp Physiol 291: R454-R463, 2006.
7. Daoui S, Cognon C, Naline E, Emonds-Alt X, Advenier C. Involvement of tachykinin NK3 receptors in citric acid-induced cough and bronchial responses in guinea pigs. Am J Respir Crit Care Med 158: 42-48, 1998.
8. dos Santos MA, Santos Galvão CE, Morato Castro F. Menthol-induced asthma: a case report. J Investig Allergol Clin Immunol 11: 56-58, 2001.
9. Eccles R. Menthol: effects on nasal sensation of airflow and the drive to breathe. Curr Allergy Asthma Rep 3: 210-214, 2003.
10. Eccles R, Griffiths DH, Newton CG, Tolley NS. The effects of D and L isomers of menthol upon nasal sensation of airflow. J Laryngol Otol 102: 506-508, 1988.
11. Fisher JT. TRPM8 and dyspnea: from the frigid and fascinating past to the cool future? Curr Opin Pharmacol 11: 218-223, 2011.
12. Girard V, Naline E, Vilain P, Emonds-Alt X, Advenier C. Effect of the two tachykinin antagonists, SR 48968 and SR 140333, on cough induced by citric acid in the unanaesthetized guinea pig. Eur Respir J 8: 1110- 1114, 1995.
13. Haidl P, Kemper P, Butnarasu SJ, Klauke M, Wehde H, Köhler D. Does the inhalation of a 1% L-menthol solution in the premedication of fiberoptic bronchoscopy affect coughing and the sensation of dyspnea? Pneumologie 55: 115-119, 2001.
14. Hoffman AC. The health effects of menthol cigarettes as compared to non-menthol cigarettes. Tob Induc Dis 9, Suppl 1: S7, 2011.
15. Hondoh A, Ishida Y, Ugawa S, Ueda T, Shibata Y, Yamada T, Shikano M, Murakami S, Shimada S. Distinct expression of cold receptors (TRPM8 and TRPA1) in the rat nodose-petrosal ganglion complex. Brain Res 1319: 60-69, 2010.
16. Jovancevic L, Georgalas C, Savovic S, Janjevic D. Gustatory rhinitis. Rhinology 48: 7-10, 2010.
17. Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, Nilius B. Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27: 9874-9884, 2007.
18. Kenia P, Houghton T, Beardsmore C. Does inhaling menthol affect nasal patency or cough? Pediatr Pulmonol 43: 532-537, 2008.
19. Knowlton WM, Daniels RL, Palkar R, McCoy DD, McKemy DD. Pharmacological blockade of TRPM8 ion channels alters cold and cold pain responses in mice. PLoS One 6: e25894, 2011.
20. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493: 596-606, 2005.
21. Kwong K, Kollarik M, Nassenstein C, Ru F, Undem BJ. P2X2 receptors differentiate placodal vs. neural crest C-fiber phenotypes innervating guinea pig lungs and esophagus. Am J Physiol Lung Cell Mol Physiol 295: L858-L865, 2008.
22. Laude EA, Morice AH, Grattan TJ. The antitussive effects of menthol, camphor and cineole in conscious guinea-pigs. Pulm Pharmacol 7: 179- 184, 1994.
23. Lippmann M, Schlesinger RB. Toxicological bases for the setting of health-related air pollution standards. Annu Rev Public Health 21: 309- 333, 2000.
24. Marlowe KF. Urticaria and asthma exacerbation after ingestion of menthol- containing lozenges. Am J Health Syst Pharm 60: 1657-1659, 2003.
25. Matthews JM, Qin N, Colburn RW, Dax SL, Hawkins M, McNally JJ, Reany L, Youngman MA, Baker J, Hutchinson T, Liu Y, Lubin ML, Neeper M, Brandt MR, Stone DJ, Flores CM. The design and synthesis of novel, phosphonate-containing transient receptor potential melastatin 8 (TRPM8) antagonists. Bioorg Med Chem Lett 22: 2922-2926, 2012.
26. Mazzone SB, Mori N, Canning BJ. Synergistic interactions between airway afferent nerve subtypes regulating the cough reflex in guinea-pigs. J Physiol 569, Pt 2: 559-573, 2005.
27. Mazzone SB, Reynolds SM, Mori N, Kollarik M, Farmer DG, Myers AC, Canning BJ. Selective expression of a sodium pump isozyme by cough receptors and evidence for its essential role in regulating cough. J Neurosci 29: 13662-13671, 2009.
28. McCoy DD, Knowlton WM, McKemy DD. Scraping through the ice: uncovering the role of TRPM8 in cold transduction. Am J Physiol Regul Integr Comp Physiol 300: R1278-R1287, 2011.
29. Millqvist E, Ternesten-Hasséus E, Bende M. Inhalation of menthol reduces capsaicin cough sensitivity and influences inspiratory flows in chronic cough. Respir Med 107: 433-438, 2013.
30. Morice AH, Marshall AE, Higgins KS, Grattan TJ. Effect of inhaled menthol on citric acid induced cough in normal subjects. Thorax 49: 1024-1026, 1994.
31. Muroi Y, Ru F, Chou YL, Carr MJ, Undem BJ, Canning BJ. Selective inhibition of vagal afferent nerve pathways regulating cough using NaV1.7 shRNA silencing in guinea pig nodose ganglia. Am J Physiol Regul Integr Comp Physiol. First published April 10, 2013; doi:10.1152/ajpregu.00028.2013.
32. Namer B, Seifert F, Handwerker HO, Maihöfner C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. Neuroreport 16: 955-959, 2005.
33. Nassenstein C, Kwong K, Taylor-Clark T, Kollarik M, Macglashan DM, Braun A, Undem BJ. Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J Physiol 586: 1595-1604, 2008.
34. Nassenstein C, Taylor-Clark TE, Myers AC, Ru F, Nandigama R, Bettner W, Undem BJ. Phenotypic distinctions between neural crest and placodal derived vagal C-fibres in mouse lungs. J Physiol 588, Pt 23: 4769-4783, 2010.
35. Nishino T, Tagaito Y, Sakurai Y. Nasal inhalation of l-menthol reduces respiratory discomfort associated with loaded breathing. Am J Respir Crit Care Med 156: 309-313, 1997.
36. Orani GP, Anderson JW, Sant'Ambrogio G, Sant'Ambrogio FB. Upper airway cooling and l-menthol reduce ventilation in the guinea pig. J Appl Physiol 70: 2080-2086, 1991.
37. Paul IM, Beiler JS, King TS, Clapp ER, Vallati J, Berlin CM Jr. Vapor rub, petrolatum, and no treatment for children with nocturnal cough and cold symptoms. Pediatrics 126: 1092-1099, 2010.
38. Plevkova J, Brozmanova M, Pecova R, Tatar M. Effects of intranasal capsaicin challenge on cough reflex in healthy human volunteers. J Physiol Pharmacol 55, Suppl 3: 101-106, 2004.
39. Plevkova J, Kollarik M, Brozmanova M, Revallo M, Varechova S, Tatar M. Modulation of experimentally-induced cough by stimulation of nasal mucosa in cats and guinea pigs. Respir Physiol Neurobiol 142: 225-235, 2004.
40. Plevkova J, Poliacek I, Antosiewicz J, Adamkov M, Jakus J, Svirlochova K, Tatar M. Intranasal TRPV1 agonist capsaicin challenge and its effect on c-fos expression in the guinea pig brainstem. Respir Physiol Neurobiol 173: 11-15, 2010.
41. Redolfi S, Raux M, Donzel-Raynaud C, Morelot-Panzini C, Zelter M, Derenne JP, Similowski T, Straus C. Effects of upper airway anaesthesia on respiratory-related evoked potentials in humans. Eur Respir J 26: 1097-1103, 2005.
42. Sekizawa S, Tsubone H, Kuwahara M, Sugano S. Nasal receptors responding to cold and l-menthol airflow in the guinea pig. Respir Physiol 103: 211-219, 1996.
43. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819-829, 2003.
44. Tatar M, Webber SE, Widdicombe JG. Lung C-fibre receptor activation and defensive reflexes in anaesthetized cats. J Physiol 402: 411-420, 1988.
45. Tatar M, Sant'Ambrogio G, Sant'Ambrogio FB. Laryngeal and tracheobronchial cough in anesthetized dogs. J Appl Physiol 76: 2672-2679, 1994.
46. Taylor-Clark TE, Kollarik M, MacGlashan DW Jr, Undem BJ. Nasal sensory nerve populations responding to histamine and capsaicin. J Allergy Clin Immunol 116: 1282-1288, 2005.
47. Trevisani M, Milan A, Gatti R, Zanasi A, Harrison S, Fontana G, Morice AH, Geppetti P. Antitussive activity of iodo-resiniferatoxin in guinea pigs. Thorax 59: 769-772, 2004.
48. Voets T, Owsianik G, Nilius B. TRPM8. Handb Exp Pharmacol 179: 329-344, 2007.
49. Willis DN, Liu B, Ha MA, Jordt SE, Morris JB. Menthol attenuates respiratory irritation responses to multiple cigarette smoke irritants. FASEB J 25: 4434-4444, 2011.
50. Winickoff JP, McMillen RC, Vallone DM, Pearson JL, Tanski SE, Dempsey JH, Healton C, Klein JD, Abrams D. US attitudes about banning menthol in cigarettes: results from a nationally representative survey. Am J Public Health 101: 1234-1236, 2011.
51. Wise PM, Breslin PA, Dalton P. Sweet taste and menthol increase cough reflex thresholds. Pulm Pharmacol Ther 25: 236-241, 2012.
52. Wise PM, Preti G, Eades J, Wysocki CJ. The effect of menthol vapor on nasal sensitivity to chemical irritation. Nicotine Tob Res 13: 989-997, 2011.
53. Xing H, Ling J, Chen M, Gu JG. Chemical and cold sensitivity of two distinct populations of TRPM8-expressing somatosensory neurons. J Neurophysiol 95: 1221-1230, 2006.
54. Xing H, Ling JX, Chen M, Johnson RD, Tominaga M, Wang CY, Gu J. TRPM8 mechanism of autonomic nerve response to cold in respiratory airway. Mol Pain 4: 22, 2008.
55. Zanotto KL, Merrill AW, Carstens MI, Carstens E. Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli. J Neurophysiol 97: 966-978, 2007.
56. Zhao H, Sprunger LK, Simasko SM. Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat. Am J Physiol Gastrointest Liver Physiol 298: G212-G221, 2010.
57. Zhou Y, Sun B, Li Q, Luo P, Dong L, Rong W. Sensitivity of bronchopulmonary receptors to cold and heat mediated by transient receptor potential cation channel subtypes in an ex vivo rat lung preparation. Respir Physiol Neurobiol 177: 327-332, 2011.