TRPV1 and TRPA1 stimulation induces MUC5B secretion in the human nasal airway in vivo

Clinical Physiology and Functional Imaging

Volumn 31, Issue 6, 2011, Pages 435-444

  Alenmyr, Lisa ^a   Herrmann, Annkatrin ^b   Högestätt, Edward D ^a   Greiff, Lennart ^c   Zygmunt, Peter M ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

MUC5AC; Nasal epithelium; Sensory nerves; Transient receptor potential; TRPM8

Indexed keywords

ALLYL ISOTHIOCYANATE; ANANDAMIDE; CALCIUM; CAPSAICIN; CINNAMALDEHYDE; MENTHOL; MUCIN 5AC; MUCIN 5B; OLVANIL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR AGONIST;

ADULT; ARTICLE; CILIARY MOTILITY; CILIATED EPITHELIUM; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; LACRIMATION DISORDER; NASAL BIOPSY; NASAL LAVAGE; NORMAL HUMAN; NOSE DISEASE; NOSE MUCUS; PAIN; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; QUANTITATIVE ASSAY; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; RHINORRHEA; SIDE EFFECT; SUBMUCOSA;

ACROLEIN; ADMINISTRATION, INTRANASAL; ADULT; AGED; ARACHIDONIC ACIDS; BIOPSY; CALCIUM; CALCIUM CHANNELS; CAPSAICIN; CILIA; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; HUMANS; IMMUNOHISTOCHEMISTRY; METHANOL; MIDDLE AGED; MOVEMENT; MUCIN 5AC; MUCIN-5B; MUSTARD PLANT; NASAL LAVAGE; NASAL MUCOSA; NERVE TISSUE PROTEINS; PAIN; PAIN MEASUREMENT; PLANT OILS; POLYUNSATURATED ALKAMIDES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SENSORY SYSTEM AGENTS; SWEDEN; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPM CATION CHANNELS; TRPV CATION CHANNELS; YOUNG ADULT;

EID: 80053894623     PISSN: 14750961     EISSN: 1475097X     Source Type: Journal    
DOI: 10.1111/j.1475-097X.2011.01039.x     Document Type: Article

References (55)

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 (2005); 136: 91-98.
2. Alenmyr L, Högestätt ED, Zygmunt PM, Greiff L. TRPV1-mediated itch in seasonal allergic rhinitis. Allergy (2009); 64: 807-810.
3. Ali MS, Hutton DA, Wilson JA, Pearson JP. Major secretory mucin expression in chronic sinusitis. Otolaryngol Head Neck Surg (2005); 133: 423-428.
4. Aust MR, Madsen CS, Jennings A, Kasperbauer JL, Gendler SJ. Mucin mRNA expression in normal and vasomotor inferior turbinates. Am J Rhinol (1997); 11: 293-302.
5. Axelsson HE, Minde JK, Sonesson A, Toolanen G, Högestätt ED, Zygmunt PM. Transient receptor potential vanilloid 1, vanilloid 2 and melastatin 8 immunoreactive nerve fibers in human skin from individuals with and without Norrbottnian congenital insensitivity to pain. Neuroscience (2009); 162: 1322-1332.
6. Baraniuk JN, Ali M, Yuta A, Fang SY, Naranch K. Hypertonic saline nasal provocation stimulates nociceptive nerves, substance P release, and glandular mucous exocytosis in normal humans. Am J Respir Crit Care Med (1999); 160: 655-662.
7. Braiman A, Priel Z. Efficient mucociliary transport relies on efficient regulation of ciliary beating. Respir Physiol Neurobiol (2008); 30: 202-207.
8. Brandelius A, Yudina Y, Calvén J, Bjermer L, Andersson M, Persson C, Uller L. dsRNA-induced expression of thymic stromal lymphopoietin (TSLP) in asthmaticepithelial cells is inhibited by a small airway relaxant. Pulm Pharmacol Ther (2011); 24: 59-66.
9. Chen H, Kuo HP. Effects of sensory neuropeptides on mucus secretion from cultured goblet cells. Changgeng Yi Xue Za Zhi (1998); 21: 283-290.
10. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem (2003); 278: 17036-17043.
11. Connell JT. Quantitative intranasal pollen challenges. 3. The priming effects in allergic rhinitis. J Allergy (1969); 43: 33-44.
12. Ding GQ, Zheng CQ. The expression of MUC5AC and MUC5B mucin genes in the mucosa of chronic rhinosinusitis and nasal polyposis. Am J Rhinol (2007); 21: 359-366.
13. Druce HM, Wright RH, Kossoff D, Kaliner MA. Cholinergic nasal hyperreactivity in atopic subjects. J Allergy Clin Immunol (1985); 76: 445-452.
14. Erjefält I, Persson CG. Anti-asthma drugs and capsaicin-induced microvascular effects in lower airways. Agents Actions (1985); 16: 9-10.
15. Fahy JV, Dickey BF. Airway mucus function and dysfunction. N Engl J Med (2010); 363: 2233-2247.
16. Fischer BM, Rochelle LG, Voynow JA, Akley NJ, Adler KB. Tumor necrosis factor-alpha stimulates mucin secretion and cyclic GMP production by guinea pig tracheal epithelial cells in vitro. Am J Respir Cell Mol Biol (1999); 20: 413-422.
17. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. Regulation of MUC5AC expression by IL-beta and IL17A: the NF-kappaB paradigm. J Immunol (2009); 183: 6236-6243.
18. Geppetti P, Fusco BM, Marabini S, Maggi CA, Fanciullacci M, Sicuteri F. Secretion, pain and sneezing induced by the application of capsaicin to the nasal mucosa in man. Br J Pharmacol (1988); 93: 509-514.
19. Greiff L, Pipkorn U, Alkner U, Persson CGA. The 'Nasal Pool-device' applies controlled concentrations of solutes on human nasal airway mucosa and samples its surface exudations/secretions. Clin Exp Allergy (1990); 20: 253-259.
20. Greiff L, Svensson C, Andersson M, Persson CGA. Effects of topical capsaicin in seasonal allergic rhinitis. Thorax (1995); 50: 225-229.
21. Greiff L, Andersson M, Coman WB, Korsgren M, Lindberg H, Marko-Varga G, Wallwork B, Persson CGA. Challenge-induced plasma exudation and mucinous secretion in human airways. Clin Physiol Funct Imaging (2005); 25: 241-245.
22. Groneberg DA, Peiser C, Dinh QT, Matthias J, Eynott PR, Heppt W, Carlstedt I, Witt C, Fischer A, Chung KF. Distribution of respiratory mucin proteins in human nasal mucosa. Laryngoscope (2003); 113: 520-524.
23. Herrmann A, Davies JR, Lindell G, Måretnsson S, Packer NH, Swallow DM, Carlstedt I. Studies of the 'insoluble' glycoprotein complex from human colon. Identification of reduction-insensitive MUC2 oligomers and C-terminal cleavage. J Biol Chem (1999); 274: 15828-15836.
24. Hovenberg HW, Davies JR, Carlstedt I. Different mucins are produced by the surface epithelium and the submucosa in human trachea: identification of MUC5AC as a major mucin from the goblet cells. Biochem J (1996); 318: 319-324.
25. Ji C, Guo Y. The expression of mucin genes in the human nasal polyps and allergic rhinitis. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi (2009); 23: 923-925.
26. 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 (2007); 27: 9874-9884.
27. Karmouty-Quintana H, Cannet C, Sugar R, Fozard JR, Page CP, Beckmann N. Capsaicin-induced mucus secretion in rat airways assessed in vivo and non-invasively by magnetic resonance imaging. Br J Pharmacol (2007); 150: 1022-1030.
28. Kim S, Nadel JA. Fibrinogen binding to ICAM-1 promotes EGFR-dependent mucin production in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol (2009); 297: L174-L183.
29. Kim DH, Chu HS, Lee JY, Hwang SJ, Lee SH, Lee HM. Up-regulation of MUC5AC and MUC5B mucin genes in chronic rhinosinusitis. Arch Otolaryngol Head Neck Surg (2004); 130: 747-752.
30. Kim SW, Hong JS, Ryu SH, Chung WC, Yoon JH, Koo JS. Regulation of mucin gene expression by CREB via a non-classical retinoic acid signalling pathway. Mol Cell Biol (2007); 27: 6933-6947.
31. Kowalski ML, Dietrich-Milobedzki A, Majkowska-Wojciechowska B, Jarzebska M. Nasal reactivity to capsaicin in patients with seasonal allergic rhinitis during and after the pollen season. Allergy (1999); 54: 804-810.
32. Kuwahara I, Lillehoj EP, Koga T, Isohama Y, Miyata T, Kim KC. The signalling pathway involved in neutrophil elastase stimulated MUC1 transcription. Am J Respir Cell Mol Biol (2007); 37: 691-698.
33. Lindberg S, Mercke U. Capsaicin stimulates mucociliary activity by releasing substance P and acetylcholine. Eur J Respir Dis (1986); 68: 96-106.
34. Lumpkin EA, Caterina MJ. Mechanisms of sensory transduction in the skin. Nature (2007); 445: 858-865.
35. Meezaman D, Charles P, Daskal E, Polymeropoulos MH, Martin BM, Rose MC. Cloning and analysis of cDNA encoding a major airway glucoprotein, human tracheobronchial mucin (MUC5). J Biol Chem (1994); 269: 12932-12939.
36. Mullol J, Rieves RD, Baraniuk JN, Lundgren JD, Mérida M, Hausfeld JH, Shelhamer JH, Kaliner MA. The effects of neuropeptides on mucous glycoprotein secretion from human nasal mucosa in vitro. Neuropeptides (1992); 21: 231-238.
37. Nassini R, Materazzi S, De Siena G, De Cesaris F, Geppetti P. Transient receptor potential channels as novel drug targets in respiratory diseases. Curr Opin Investig Drugs (2010); 11: 535-542.
38. O'Hanlon S, Facer P, Simpson KD, Sandhu G, Saleh HA, Anand P. Neuronal markers in allergic rhinitis: expression and correlation with sensory testing. Laryngoscope (2007); 117: 1519-1527.
39. Philip G, Baroody FM, Proud D, Naclerio RM, Togias AG. The human nasal response to capsaicin. J Allergy Clin Immunol (1994); 94: 1035-1045.
40. Raphael GD, Igarashi Y, White MV, Kaliner MA. The pathophysiology of rhinitis. V. Sources of protein in allergen-induced nasal secretions. J Allergy Clin Immunol (1991); 88: 33-42.
41. Sanico AM, Philip G, Proud D, Naclerio RM, Togias A. Comparison of nasal mucosal responsiveness to neuronal stimulation in non-allergic and allergic rhinitis: effects of capsaicin nasal challenge. Clin Exp Allergy (1998); 28: 92-100.
42. Seki N, Shirasaki H, Kikuchi M, Sakamoto T, Watanabe N, Himi T. Expression and localization of TRPV1 in human nasal mucosa. Rhinology (2006); 44: 128-134.
43. Seki N, Shirasaki H, Kikuchi M, Himi T. Capsaicin induces the production of IL-6 in human upper respiratory epithelial cells. Life Sci (2007); 80: 1592-1597.
44. Shirasaki H, Asakura K, Narita SI, Kataura A. Expression of substance P (NK1) receptor mRNA in human nose. Acta Otolaryngol (1998); 118: 717-722.
45. Smirnova MG, Guo L, Birchall JP, Pearson JP. LPS up-regulate mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol (2003); 221: 42-49.
46. Svensson C, Andersson M, Greiff L, Alkner U, Persson CGA. Exudative hyperresponsiveness of the airway microcirculation in seasonal allergic rhinitis. Clin Exp Allergy (1995); 25: 942-950.
47. Takashima Y, Ma L, McKemy DD. The development of peripheral cold neural circuits based on TRPM8 expression. Neuroscience (2010); 169: 828-842.
48. Turner J, Jones CE. Regulation of mucin expression in respiratory diseases. Biochem Soc Trans (2009); 37: 877-881.
49. Veronesi B, Carter JD, Devlin RB, Simon SA, Oortgiesen M. Neuropeptides and capsaicin stimulate the release of inflammatory cytokines in a human bronchial epithelial cell line. Neuropeptides (1999); 33: 447-456.
50. Viswanathan H, Brownlee IA, Pearson JP, Carrie S. MUC5B secretion is up-regulated in sinusitis compared with controls. Am J Rhinol (2006); 20: 554-557.
51. Vos MH, Neelands TR, McDonald HA, Choi W, Kroeger PE, Puttfarcken PS, Faltynek CR, Moreland RB, Han P. TRPV1b overexpression negatively regulates TRPV1 responsiveness to capsaicin, heat and low pH in HEK293 cells. J Neurochem (2006); 99: 1088-1102.
52. Wickström C, Davies JR, Eriksen GV, Veerman EC, Carlstedt I. MUC5B is a major gel-forming, oligomericmucin from human salivary gland, respiratory tract and endocervix: identification of glycoforms and C-terminal cleavage. Biochem J (1998); 334: 685-693.
53. Woo HJ, Yoo WJ, Bae CH, Song SY, Kim YW, Park SY, Kim YD. Leptin up-regulates MUC5B expression in human airway epithelial cells via mitogen-activated protein kinase pathway. Exp Lung Res (2010); 36: 262-269.
54. Yu H, Li Q, Kolosov VP, Perelman JM, Zhou X. Interleukin-13 induces mucin 5AC production involving STAT6/SPDEF in human airway epithelial cells. Cell Commun Adhes (2011); 17: 83-92.
55. Yuan-Chen Wu D, Wu R, Reddy SP, Lee YC, Chang MM. Distinct epidermal growth factor receptor/extracellular regulated kinase-independent and -dependent signalling pathways in the induction of airway mucin 5B and mucin 5AC expression by phorbol 12-myristate 13-acetate. Am J Pathol (2007); 170: 20-32.