Clarithromycin inhibits interleukin-13-induced goblet cell hyperplasia in human airway cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 5, 2011, Pages 1075-1083

  Tanabe, Tsuyoshi ^a   Kanoh, Soichiro ^a   Tsushima, Kenji ^b   Yamazaki, Yoshitaka ^b   Kubo, Keishi ^b   Rubin, Bruce K ^a  

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

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Bronchial asthma; Clarithromycin; Goblet cell hyperplasia; IL 13; MUC5AC

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 6 CHLORO 8 NICOTINAMIDO BETA CARBOLINE; CLARITHROMYCIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13; LEFLUNOMIDE; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 5AC; STAT6 PROTEIN;

ARTICLE; BRONCHUS MUCOSA; CELL HYPERPLASIA; DRUG EFFECT; GOBLET CELL HYPERPLASIA; HISTOCHEMISTRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RESPIRATORY EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BRONCHI; CELL DIFFERENTIATION; CLARITHROMYCIN; ENZYME INHIBITORS; FLAVONOIDS; GOBLET CELLS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; HYPERPLASIA; INTERLEUKIN-13; ISOXAZOLES; JANUS KINASES; MAP KINASE SIGNALING SYSTEM; MUCIN 5AC; MUCUS; NF-KAPPA B; PROTEIN SYNTHESIS INHIBITORS; PYRIDINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR;

EID: 80555157601     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0327OC     Document Type: Article

References (60)

1. Fahy JV. Goblet cell and mucin gene abnormalities in asthma. Chest 2002;122:320S-326S. (Pubitemid 36043022)
2. Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 2006;86:245-278.
3. Voynow JA, Rubin BK. Mucins, mucus and sputum. Chest 2009;135:505-512.
4. Rubin BK, Tomkiewicz R, Fahy JV, Green FH. Histopathology of fatal asthma: drowning in mucus. Pediatr Pulmonol 2001;S23:88-89. (Pubitemid 33021812)
5. Aikawa T, Shimura S, Sasaki H, Ebina M, Takishima T. Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack. Chest 1992;101:916-921.
6. Ordonez CL, Khashayar R, Wong HH, Ferrando R, Wu R, Hyde DM, Hotchkiss JA, Zhang Y, Novikov A, Dolganov G, et al. Mild and moderate asthma is associated with goblet cell hyperplasia and abnormalities in mucin gene expression. Am J Respir Crit Care Med 2001;163:517-523. (Pubitemid 32158539)
7. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. Interleukin-13: central mediator of allergic asthma. Science 1998;282:2258-2261. (Pubitemid 29004074)
8. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, Elias JA. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 1999;103:779-788. (Pubitemid 29152623)
9. Atherton HC, Jones G, Danahay H. IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am J Physiol Lung Cell Mol Physiol 2003;285:L730-L739. (Pubitemid 37022875)
10. Zhen G, Park SW, Nguyenvu LT, Rodriguez MW, Barbeau R, Paquet AC, Erle DJ. IL-13 and epidermal growth factor receptor have critical but distinct roles in epithelial cell mucin production. Am J Respir Cell Mol Biol 2007;36:244-253. (Pubitemid 46233478)
11. Culic O, Erakovic V, Parnham MJ. Anti-inflammatory effects of macrolide antibiotics. Eur J Pharmacol 2001;429:209-229. (Pubitemid 33043997)
12. Lopez-Boado YS, Rubin BK. Macrolides as immunomodulatory medications for the therapy of chronic lung diseases. Curr Opin Pharmacol 2008;8:286-291.
13. Shinkai M, Henke MO, Rubin BK. Macrolide antibiotics as immunomodulatory medications: proposed mechanisms of action. Pharmacol Ther 2008;117:393-405.
14. Gotfried MH, Jung R, Messick CR, Rubinstein I, Garey KW, Rodvold KA, Danziger LH. Effects of six week clarithromycin therapy in corticosteroid- dependent asthma: a randomized double-blind, placebocontrolled pilot study. Curr Ther Res 2004;65:1-12. (Pubitemid 38953428)
15. Amayasu H, Yoshida S, Ebana S, Yamamoto Y, Nishikawa T, Shoji T, Nakagawa H, Hasegawa H, Nakabayashi M, Ishizaki Y. Clarithromycin suppresses bronchial hyperresponsiveness associated with eosinophilic inflammation in patients with asthma. Ann Allergy Asthma Immunol 2000;84:594-598. (Pubitemid 30418859)
16. Kostadima E, Tsiodras S, Alexopoulos EI, Kaditis AG, Mavrou I, Georgatou N, Papamichalopoulos A. Clarithromycin reduces the severity of bronchial hyperresponsiveness in patients with asthma. Eur Respir J 2004;23:714-717. (Pubitemid 38618141)
17. Kraft M, Cassell GH, Pak J, Martin RJ. Mycoplasma pneumoniae and Chlamydia pneumoniae in asthma: effect of clarithromycin. Chest 2002;121:1782-1788. (Pubitemid 34634396)
18. Strunk RC, Bacharier LB, Phillips BR, Szefler SJ, Zeiger RS, Chinchilli VM, Martinez FD, Lemanske RF Jr, Taussig LM, Mauger DT, et al. Azithromycin or montelukast as inhaled corticosteroid-sparing agents in moderate-to-severe childhood asthma study. J Allergy Clin Immunol 2008;122:1138-1144.
19. Piacentini GL, Peroni DG, Bodini A, Pigozzi R, Costella S, Loiacono A, Boner AL. Azithromycin reduces bronchial hyperresponsiveness and neutrophilic airway inflammation in asthmatic children: a preliminary report. Allergy Asthma Proc 2007;28:194-198.
20. Simpson JL, Powell H, Boyle MJ, Scott RJ, Gibson PG. Clarithromycin targets neutrophilic airway inflammation in refractory asthma. Am J Respir Crit Care Med 2008;177:148-155.
21. Rubin BK, Druce H, Ramirez OE, Palmer R. Effect of clarithromycin on nasal mucus properties in healthy subjects and in patients with purulent rhinitis. Am J Respir Crit Care Med 1997;155:2018-2023. (Pubitemid 27256133)
22. Goswami SK, Kivity S, Marom Z. Erythromycin inhibits respiratory glycoconjugate secretion from human airways in vitro. Am Rev Respir Dis 1990;141:72-78. (Pubitemid 20023385)
23. Ou XM, Feng YL, Wen FQ, Wang K, Yang J, Deng ZP, Liu DS, Li YP. Macrolides attenuate mucus hypersecretion in rat airways through inactivation of NF-κB. Respirology 2008;13:63-72.
24. Kaneko Y, Yanagihara K, Seki M, Kuroki M, Miyazaki Y, Hirakata Y, Mukae H, Tomono K, Kadota J, Kohno S. Clarithromycin inhibits overproduction of muc5ac core protein in murine model of diffuse panbronchiolitis. Am J Physiol Lung Cell Mol Physiol 2003;285:L847-L853. (Pubitemid 37158831)
25. Imamura Y, Yanagihara K, Mizuta Y, Seki M, Ohno H, Higashiyama Y, Miyazaki Y, Tsukamoto K, Hirakata Y, Tomono K, et al. Azithromycin inhibits MUC5AC production induced by the Pseudomonas aeruginosa autoinducer N-(3-Oxododecanoyl) homoserine lactone in NCI-H292 Cells. Antimicrob Agents Chemother 2004;48:3457-3461. (Pubitemid 39129345)
26. Tamaoki J. The effects of macrolides on inflammatory cells. Chest 2004;125:41S-51S. (Pubitemid 38200960)
27. Beigelman A, Gunsten S, Mikols CL, Vidavsky I, Cannon CL, Brody SL, Walter MJ. Azithromycin attenuates airway inflammation in a noninfectious mouse model of allergic asthma. Chest 2009;136:498-506.
28. Hrvacić B, Bosnjak B, Bosnar M, Ferencić Z, Glojnarić I, Haber VE. Clarithromycin suppresses airway hyperresponsiveness and inflammation in mouse models of asthma. Eur J Pharmacol 2009;616:236-243.
29. Shimizu T, Shimizu S, Hattori R, Gabazza EC, Majima Y. In vivo and in vitro effects of macrolide antibiotics on mucus secretion in airway epithelial cells. Am J Respir Crit Care Med 2003;168:581-587. (Pubitemid 37088602)
30. Tanabe T, Fujimoto K, Yasuo M, Tsushima K, Yoshida K, Ise H, Yamaya M. Modulation of mucus production by interleukin-13 receptor alpha 2 in the human airway epithelium. Clin Exp Allergy 2008;38:122-134. (Pubitemid 350233391)
31. Shinkai M, Shinkai M, Foster GH, Rubin BK. Macrolide antibiotics modulate ERK phosphorylation and IL-8 and GM-CSF production by human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006;290:L75-L85.
32. Caramori G, Di Gregorio C, Carlstedt I, Casolari P, Guzzinati I, Adcock IM, Barnes PJ, Ciaccia A, Cavallesco G, Chung KF, et al. Mucin expression in peripheral airways of patients with chronic obstructive pulmonary disease. Histopathology 2004;45:477-484. (Pubitemid 39524322)
33. Mata M, Sarria B, Buenestado A, Cortijo J, Cerda M, Morcillo EJ. Phosphodiesterase 4 inhibition decreases MUC5AC expression induced by epidermal growth factor in human airway epithelial cells. Thorax 2005;60:144-152. (Pubitemid 40222898)
34. Honeybourne D, Baldwin DR. The site concentrations of antimicrobial agents in the lung. J Antimicrob Chemother 1992;30:249-260.
35. Rodvold KA, Gotfried MH, Danziger LH, Servi RJ. Intrapulmonary steadystate concentrations of clarithromycin and azithromycin in healthy adult volunteers. Antimicrob Agents Chemother 1997;41:1399-1402. (Pubitemid 27231452)
36. Shim JJ, Dabbagh K, Ueki IF, Dao-Pick T, Burgel PR, Takeyama K, Tam DC, Nadel JA. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils. Am J Physiol Lung Cell Mol Physiol 2001;280:L134-L140.
37. Tyner JW, Kim EY, Ide K, Pelletier MR, Roswit WT, Morton JD, Battaile JT, Patel AC, Patterson GA, Castro M, et al. Blocking airway mucous cell metaplasia by inhibiting EGFR antiapoptosis and IL-13 transdifferentiation signals. J Clin Invest 2006;116:309-321. (Pubitemid 43228348)
38. Takeyama K, Dabbagh K, Lee HM, Agustí C, Lausier JA, Ueki IF, Grattan KM, Nadel JA. Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 1999;96:3081-3086. (Pubitemid 29148847)
39. Takeyama K, Dabbagh K, Jeong Shim J, Dao-Pick T, Ueki IF, Nadel JA. Oxidative stress causes mucin synthesis via transactivation of epidermal growth factor receptor: role of neutrophils. J Immunol 2000;164:1546-1552. (Pubitemid 30067272)
40. Levine SJ, Larivée P, Logun C, Angus CW, Ognibene FP, Shelhamer JH. Tumor necrosis factor-alpha induces mucin hypersecretion and MUC-2 gene expression by human airway epithelial cells. Am J Respir Cell Mol Biol 1995;12:196-204.
41. Yasunaga S, Yuyama N, Arima K, Tanaka H, Toda S, Maeda M, Matsui K, Goda C, Yang Q, Sugita Y, et al. The negative feedback regulation of the IL-13 signal by the IL-13 receptor alpha2 chain in bronchial epithelial cells. Cytokine 2003;24:293-303. (Pubitemid 37373665)
42. Li JD, Feng W, Gallup M, Kim JH, Gum J, Kim Y, Basbaum C. Activation of NF-kB via a Src-dependent Ras-MAPK-pp 90 rsk pathway is required for Pseudomonas aeruginosa-induced mucin overproduction in epithelial cells. Proc Natl Acad Sci USA 1998;95:5718-5723. (Pubitemid 28224162)
43. Chen LF, Greene WC. Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 2004;5:392-401.
44. Desaki M, Takizawa H, Ohtoshi T, Kasama T, Kobayashi K, Sunazuka T, Omura S, Yamamoto K, Ito K. Erythromycin suppresses nuclear factor-kappa B and activator protein-1 activation in human bronchial epithelial cells. Biochem Biophys Res Commun 2000;267:124-128. (Pubitemid 30072518)
45. Newton R, Holden NS, Catley MC, Oyelusi W, Leigh R, Proud D, Barnes PJ. Repression of inflammatory gene expression in human pulmonary epithelial cells by small-molecule IkappaB kinase inhibitors. J Pharmacol Exp Ther 2007;321:734-742. (Pubitemid 46624511)
46. Kanoh S, Rubin BK. Macrolides as immunomodulatory medications mechanisms of action and clinical application. Clin Microbiol Rev 2010;23:590-615.
47. Goto K, Chiba Y, Misawa M. IL-13 induces traslocation of NF-kappaB in cultured human bronchial smooth muscle cells. Cytokine 2009;46:96-99.
48. Goto K, Chiba Y, Matsusue K, Hattori Y, Maitani Y, Sakai H, Kimura S, Misawa M. The proximal STAT6 and NF-kappaB sites are responsible for IL-13- and TNF-alpha-induced RhoA transcriptions in human bronchial smooth muscle cells. Pharmacol Res 2010;61:466-472.
49. Mullings RE, Wilson SJ, Puddicombe SM, Lordan JL, Bucchieri F, Djukanovic R, Howarth PH, Harper S, Holgate ST, Davies DE. Signal transducer and activator of transcription 6 (STAT-6) expression and function in asthmatic bronchial epithelium. J Allergy Clin Immunol 2001;108:832-838. (Pubitemid 33096218)
50. Tekkanat KK, Maassab HF, Cho DS, Lai JJ, John A, Berlin A, Kaplan MH, Lukacs NW. IL-13-induced airwayhyperreactivity during respiratory syncytial virus infection is STAT6 dependent. J Immunol 2001;166:3542-3548. (Pubitemid 33117359)
51. Kudoh S, Azuma A, Yamamoto M, Izumi T, Ando M. Improvement in survival of patients with diffuse panbronchiolitis treated with low dose erythromycin. Am J Respir Crit Care Med 1998;157:1829-1832.
52. Kadota J, Mukae H, Ishii H, Nagata T, Kaida H, Tomono K, Kohno S. Long-term efficacy and safety of clarithromycin treatment in patients with diffuse panbronchiolitis. Respir Med 2003;97:844-850. (Pubitemid 36763898)
53. Everard ML, Sly P, Brenan S, Ryan G. Macrolide antibiotics in diffuse panbronchiolitis and in cystic fibrosis. Eur Respir J 1997;10:2926. (Pubitemid 28052814)
54. Jaffe A, Francis J, Rosenthal M, Bush A. Long-term azithromycin may improve lung function in children with cystic fibrosis. Lancet 1998;351:420.
55. Wolter J, Seeney S, Bell S, Bowler S, Masel P, McCormack J. Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: a randomized trial. Thorax 2002;57:212-216. (Pubitemid 34214405)
56. Jeffery PK. Remodeling and inflammation of bronchi in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc 2004;1:176-183.
57. Sidebotham HJ, Roche WR. Asthma deaths; persistent and preventable mortality. Histopathology 2003;43:105-117. (Pubitemid 36963154)
58. Kuyper LM, Pare PD, Hogg JC, Lambert RK, Lonescu D, Woods R, Bai TR. Characterization of airway plugging in fatal asthma. Am J Med 2003;115:6-11. (Pubitemid 36831115)
59. Okamoto K, Kim JS, Rubin BK. Secretory phospholipases A2 stimulate mucus secretion, induce airway inflammation, and produce secretory hyperresponsiveness to neutrophil elastase in ferret trachea. Am J Physiol Lung Cell Mol Physiol 2007;292:L62-L67. (Pubitemid 46103430)
60. Schmidt HJ, Bhandari V, Bhandari A, Davies J, Marshall BC, Praud JP, Zar HJ, Rubin BK. The future in paediatric respirology. Respirology 2010;15:733-741.