Nonantibiotic macrolides prevent human neutrophil elastase-induced mucus stasis and airway surface liquid volume depletion

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 304, Issue 11, 2013, Pages

  Tarran, Robert ^a   Sabater, Juan R ^c   Clarke, Tainya C ^c   Tan, Chong D ^a   Davies, Catrin M ^a   Liu, Jia ^b   Yeung, Arthur ^b   Garland, Alaina L ^a   Jackson Stutts, M ^a   Abraham, William M ^c   Phillips, Gary ^b   Baker, William R ^b   Wright, Clifford D ^b   Wilbert, Sibylle ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Gilead Sciences   (United States)

^c MOUNT SINAI MEDICAL CENTER   (United States)

Author keywords

COPD; ENaC; Epithelia; Protease; Sodium absorption

Indexed keywords

2' DESOXY 9 ERYTHROMYCYLAMINE; AZITHROMYCIN; EPITHELIAL SODIUM CHANNEL; ERYTHROMYCYLAMINE; GS 459755; LEUKOCYTE ELASTASE; UNCLASSIFIED DRUG;

AIRWAY SURFACE LIQUID; ANTIBACTERIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOTINYLATION; BRONCHUS MUCOSA; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYSTIC FIBROSIS; DOSE RESPONSE; FEMALE; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; IC 50; MORAXELLA CATARRHALIS; MUCUS; MUCUS SECRETION; MUCUS STASIS; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIA; WATER PERMEABILITY;

COPD; ENAC; EPITHELIA; PROTEASE; SODIUM ABSORPTION;

AZITHROMYCIN; EPITHELIAL SODIUM CHANNELS; ERYTHROMYCIN; HUMANS; LEUKOCYTE ELASTASE; MACROLIDES; MUCUS; RESPIRATORY MUCOSA; RESPIRATORY SYSTEM;

EID: 84878665825     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00292.2012     Document Type: Article

References (48)

1. + transport. J Gen Physiol 130: 611-629, 2007.
2. Albert RK, Connett J, Bailey WC, Casaburi R, Cooper JA Jr, Criner GJ, Curtis JL, Dransfield MT, Han MK, Lazarus SC, Make B, Marchetti N, Martinez FJ, Madinger NE, McEvoy C, Niewoehner DE, Porsasz J, Price CS, Reilly J, Scanlon PD, Sciurba FC, Scharf SM, Washko GR, Woodruff PG, Anthonisen NR. Azithromycin for prevention of exacerbations of COPD. N Engl J Med 365: 689-698, 2011.
3. Amitani R, Wilson R, Rutman A, Read R, Ward C, Burnett D, Stockley RA, Cole PJ. Effects of human neutrophil elastase and Pseudomonas aeruginosa proteinases on human respiratory epithelium. Am J Respir Cell Mol Biol 4: 26-32, 1991.
4. Ballard ST, Spadafora D. Fluid secretion by submucosal glands of the tracheobronchial airways. Respir Physiol Neurobiol 159: 271-277, 2007.
5. Boucher RC. Relationship of airway epithelial ion transport to chronic bronchitis. Proc Am Thorac Soc 1: 66-70, 2004.
6. Butterworth MB, Zhang L, Heidrich EM, Myerburg MM, Thibodeau PH. Activation of the epithelial sodium channel (ENaC) by the alkaline protease from Pseudomonas aeruginosa. J Biol Chem 287: 32556-32565, 2012.
7. + transport. Am J Physiol Lung Cell Mol Physiol 288: L813-L819, 2005.
8. Cantin AM, Hanrahan JW, Bilodeau G, Ellis L, Dupuis A, Liao J, Zielenski J, Durie P. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 173: 1139-1144, 2006.
9. Chambers LA, Rollins BM, Tarran R. Liquid movement across the surface epithelium of large airways. Respir Physiol Neurobiol 159: 256-270, 2007.
10. Chu DTW. Recent developments in 14-and 15-membered macrolides. Expert Opin Investig Drugs 4: 65-94, 1995.
11. Clunes LA, Davies CM, Coakley RD, Aleksandrov AA, Henderson AG, Zeman KL, Worthington EN, Gentzsch M, Kreda SM, Cholon D, Bennett WD, Riordan JR, Boucher RC, Tarran R. Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration. FASEB J 26: 533-545, 2012.
12. Com G, Clancy JP. Adenosine receptors, cystic fibrosis, and airway hydration. Handb Exp Pharmacol 193: 363-381, 2009.
13. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, Gabriel SE. Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem 277: 8338-8345, 2002.
14. Farinas J, Verkman AS. Cell volume and plasma membrane osmotic water permeability in epithelial cell layers measured by interferometry. Biophys J 71: 3511-3522, 1996.
15. Friedlander AL, Albert RK. Chronic macrolide therapy in inflammatory airways diseases. Chest 138: 1202-1212, 2010.
16. + channel and airway surface liquid volume by serine proteases. Pflügers Arch 460: 1-17, 2010.
17. Gerald LB, Bailey WC. Global initiative for chronic obstructive lung disease. J Cardiopulm Rehabil 22: 234-244, 2002.
18. Girod S, Zahm JM, Plotkowski C, Beck G, Puchelle E. Role of the physiochemical properties of mucus in the protection of the respiratory epithelium. Eur Respir J 5: 477-487, 1992.
19. Hassan F, Nuovo GJ, Crawford M, Boyaka PN, Kirkby S, Nana-Sinkam SP, Cormet-Boyaka E. MiR-101 and miR-144 regulate the expression of the CFTR chloride channel in the lung. PLoS One 7: e50837, 2012.
20. Hogg JC, Timens W. The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol 4: 435-459, 2009.
21. + conductance. Proc Natl Acad Sci USA 108: 10260-10265, 2011.
22. Kannan K, Mankin AS. Macrolide antibiotics in the ribosome exit tunnel: species-specific binding and action. Ann NY Acad Sci 1241: 33-47, 2011.
23. Kanoh S, Rubin BK. Mechanisms of action and clinical application of macrolides as immunomodulatory medications. Clin Microbiol Rev 23: 590-615, 2010.
24. Kawabata K, Suzuki M, Sugitani M, Imaki K, Toda M, Miyamoto T. ONO-5046, a novel inhibitor of human neutrophil elastase. Biochem Biophys Res Commun 177: 814-820, 1991.
25. Keicho N, Hijikata M. Genetic predisposition to diffuse panbronchiolitis. Respirology 16: 581-588, 2011.
26. Kleyman TR, Carattino MD, Hughey RP. ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J Biol Chem 284: 20447-20451, 2009.
27. Konstan MW, Hilliard KA, Norvell TM, Berger M. Bronchoalveolar lavage findings in cystic fibrosis patients with stable, clinically mild lung disease suggest ongoing infection and inflammation. Am J Respir Crit Care Med 150: 448-454, 1994.
28. Livraghi A, Randell SH. Cystic fibrosis and other respiratory diseases of impaired mucus clearance. Toxicol Pathol 35: 116-129, 2007.
29. Mannino DM, Homa DM, Akinbami LJ, Ford ES, Redd SC. Chronic obstructive pulmonary disease surveillance-United States, 1971-2000. MMWR Surveill Summ 51: 1-16, 2002.
30. Martinez FJ, Curtis JL, Albert R. Role of macrolide therapy in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 3: 331-350, 2008.
31. Matsui H, Davis CW, Tarran R, Boucher RC. Osmotic water permeabilities of cultured, well-differentiated normal and cystic fibrosis airway epithelia. J Clin Invest 105: 1419-1427, 2000.
32. McArdle JR, Talwalkar JS. Macrolides in cystic fibrosis. Clin Chest Med 28: 347-360, 2007.
33. Piccioni PD, Kramps JA, Rudolphus A, Bulgheroni A, Luisetti M. Proteinase/proteinase inhibitor imbalance in sputum sol phases from patients with chronic obstructive pulmonary disease. Suggestions for a key role played by antileukoprotease. Chest 102: 1470-1476, 1992.
34. Randell SH, Fulcher ML, O'Neal W, Olsen JC. Primary epithelial cell models for cystic fibrosis research. Methods Mol Biol 742: 285-310, 2011.
35. Retsema J, Fu W. Macrolides: structures and microbial targets. Int J Antimicrob Agents 18, Suppl 1: S3-S10, 2001.
36. Rollins BM, Burn M, Coakley RD, Chambers LA, Hirsh AJ, Clunes MT, Lethem MI, Donaldson SH, Tarran R. A2B adenosine receptors regulate the mucus clearance component of the lung's innate defense system. Am J Respir Cell Mol Biol 39: 190-197, 2008.
37. Rubin BK, Ramirez O, Zayas JG, Finegan B, King M. Respiratory mucus from asymptomatic smokers is better hydrated and more easily cleared by mucociliary action. Am Rev Respir Dis 145: 545-547, 1992.
38. Sabater JR, Lee TA, Abraham WM. Comparative effects of salmeterol, albuterol, and ipratropium on normal and impaired mucociliary function in sheep. Chest 128: 3743-3749, 2005.
39. Schmid A, Clunes LA, Salathe M, Verdugo P, Dietl P, Davis CW, Tarran R. Nucleotide-mediated airway clearance. Subcell Biochem 55: 95-138, 2011.
40. Sims DE, Horne MM. Heterogeneity of the composition and thickness of tracheal mucus in rats. Am J Physiol Lung Cell Mol Physiol 273: L1036-L1041, 1997.
41. Sloane PA, Shastry S, Wilhelm A, Courville C, Tang LP, Backer K, Levin E, Raju SV, Li Y, Mazur M, Byan-Parker S, Grizzle W, Sorscher EJ, Dransfield MT, Rowe SM. A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease. PLoS One 7: e39809, 2012.
42. Southern KW, Barker PM, Solis-Moya A, Patel L. Macrolide antibiotics for cystic fibrosis. Cochrane Database Syst Rev 12: CD002203, 2011.
43. + transport in response to apical fluid volume expansion in human H441 airway epithelial cells. Pflügers Arch 462: 431-441, 2011.
44. Tarran R, Grubb BR, Gatzy JT, Davis CW, Boucher RC. The relative roles of passive surface forces and active ion transport in the modulation of airway surface liquid volume and composition. J Gen Physiol 118: 223-236, 2001.
45. Tarran R, Trout L, Donaldson SH, Boucher RC. Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J Gen Physiol 127: 591-604, 2006.
46. Verkman AS, Matthay MA, Song Y. Aquaporin water channels and lung physiology. Am J Physiol Lung Cell Mol Physiol 278: L867-L879, 2000.
47. Watson MJ, Worthington EN, Clunes LA, Rasmussen JE, Jones L, Tarran R. Defective adenosine-stimulated cAMP production in cystic fibrosis airway epithelia: a novel role for CFTR in cell signaling. FASEB J 25: 2996-3003, 2011.
48. Wu DX, Lee CY, Uyekubo SN, Choi HK, Bastacky SJ, Widdicombe JH. Regulation of the depth of surface liquid in bovine trachea. Am J Physiol Lung Cell Mol Physiol 274: L388-L395, 1998.