Roflumilast partially reverses smoke-induced mucociliary dysfunction

Respiratory Research

Volumn 16, Issue 1, 2015, Pages

  Schmid, Andreas ^a   Baumlin, Nathalie ^a   Ivonnet, Pedro ^a   Dennis, John S ^a   Campos, Michael ^a   Krick, Stefanie ^a   Salathe, Matthias ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Airways; CFTR; Cilia; FRET; Mucociliary clearance; Roflumilast

Indexed keywords

CIGARETTE SMOKE; CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FORMOTEROL; FORSKOLIN; MESSENGER RNA; ROFLUMILAST; SALBUTAMOL; AMINOPYRIDINE DERIVATIVE; BENZAMIDE DERIVATIVE; CFTR PROTEIN, HUMAN; CHLORIDE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOPROPANE DERIVATIVE; FORMOTEROL FUMARATE; PHOSPHODIESTERASE IV INHIBITOR; SMOKE;

AIRWAY EPITHELIAL CELL; ARTICLE; BRONCHUS BIOPSY; CHLORIDE CONDUCTANCE; CILIARY MOTILITY; CONTROLLED STUDY; DRUG POTENTIATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MUCOCILIARY CLEARANCE; SMOKING; SMOKING CESSATION; ADVERSE EFFECTS; BRONCHUS; CELL CULTURE; DRUG EFFECTS; EPITHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC PROCEDURES; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; SECOND MESSENGER; SMOKE; TIME FACTOR;

ALBUTEROL; AMINOPYRIDINES; BENZAMIDES; BIOSENSING TECHNIQUES; BRONCHI; CELLS, CULTURED; CHLORIDES; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLOPROPANES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FORMOTEROL FUMARATE; HUMANS; MUCOCILIARY CLEARANCE; PHOSPHODIESTERASE 4 INHIBITORS; RNA, MESSENGER; SECOND MESSENGER SYSTEMS; SMOKE; SMOKING; TIME FACTORS; TRANSFECTION;

EID: 84945916683     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/s12931-015-0294-3     Document Type: Article

References (45)

1. Salathe M. Regulation of mammalian ciliary beating. Annu Rev Physiol. 2007;69:401-22.
2. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell. 1998;95:1005-15.
3. Maurice DH, Ke H, Ahmad F, Wang Y, Chung J, Manganiello VC. Advances in targeting cyclic nucleotide phosphodiesterases. Nat Rev Drug Discov. 2014;13:290-314.
4. Zhang KY, Ibrahim PN, Gillette S, Bollag G. Phosphodiesterase-4 as a potential drug target. Expert Opin Ther Targets. 2005;9:1283-305.
5. Michalski JM, Golden G, Ikari J, Rennard SI. PDE4: a novel target in the treatment of chronic obstructive pulmonary disease. Clin Pharmacol Ther. 2012;91:134-42.
6. Giembycz MA, Field SK. Roflumilast: first phosphodiesterase 4 inhibitor approved for treatment of COPD. Drug Des Devel Ther. 2010;4:147-58.
7. Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest. 2013;144:498-506.
8. Sloane PA, Shastry S, Wilhelm A, Courville C, Tang LP, Backer K, et al. A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease. PLoS One. 2012;7, e39809.
9. Raju SV, Jackson PL, Courville CA, McNicholas CM, Sloane PA, Sabbatini G, et al. Cigarette smoke induces systemic defects in cystic fibrosis transmembrane conductance regulator function. Am J Respir Crit Care Med. 2013;188:1321-30.
10. Cobb BR, Fan L, Kovacs TE, Sorscher EJ, Clancy JP. Adenosine receptors and phosphodiesterase inhibitors stimulate Cl- secretion in Calu-3 cells. Am J Respir Cell Mol Biol. 2003;29:410-8.
11. Fuhrmann M, Jahn HU, Seybold J, Neurohr C, Barnes PJ, Hippenstiel S, et al. Identification and function of cyclic nucleotide phosphodiesterase isoenzymes in airway epithelial cells. Am J Respir Cell Mol Biol. 1999;20:292-302.
12. Bernacki SH, Nelson AL, Abdullah L, Sheehan JK, Harris A, Davis CW, et al. Mucin gene expression during differentiation of human airway epithelia in vitro. Muc4 and muc5b are strongly induced. Am J Respir Cell Mol Biol. 1999;20:595-604.
13. Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski LE, Conner GE, et al. Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells. J Cell Sci. 2006;119:4176-86.
14. Nlend MC, Bookman RJ, Conner GE, Salathe M. Regulator of G-protein signaling protein 2 modulates purinergic calcium and ciliary beat frequency responses in airway epithelia. Am J Respir Cell Mol Biol. 2002;27:436-45.
15. Fragoso MA, Fernandez V, Forteza R, Randell SH, Salathe M, Conner GE. Transcellular thiocyanate transport by human airway epithelia. J Physiol. 2004;561:183-94.
16. De Palma M, Naldini L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 2002;346:514-29.
17. Zaccolo M, Pozzan T. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science. 2002;295:1711-5.
18. Ostrowski LE, Hutchins JR, Zakel K, O'Neal WK. Targeting expression of a transgene to the airway surface epithelium using a ciliated cell-specific promoter. Mol Ther. 2003;8:637-45.
19. Salathe M, Bookman RJ. Mode of Ca2+ action on ciliary beat frequency in single ovine airway epithelial cells. J Physiol. 1999;520(Pt 3):851-65.
20. Harvey PR, Tarran R, Garoff S, Myerburg MM. Measurement of the airway surface liquid volume with simple light refraction microscopy. Am J Respir Cell Mol Biol. 2011;45:592-9.
21. Celli BR, MacNee W, Force AET. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J. 2004;23:932-46.
22. Martorana PA, Lunghi B, Lucattelli M, De Cunto G, Beume R, Lungarella G. Effect of roflumilast on inflammatory cells in the lungs of cigarette smoke-exposed mice. BMC Pulm Med. 2008;8:17.
23. Sanz MJ, Cortijo J, Taha MA, Cerda-Nicolas M, Schatton E, Burgbacher B, et al. Roflumilast inhibits leukocyte-endothelial cell interactions, expression of adhesion molecules and microvascular permeability. Br J Pharmacol. 2007;152:481-92.
24. Grootendorst DC, Gauw SA, Verhoosel RM, Sterk PJ, Hospers JJ, Bredenbroker D, et al. Reduction in sputum neutrophil and eosinophil numbers by the PDE4 inhibitor roflumilast in patients with COPD. Thorax. 2007;62:1081-7.
25. Dunkern TR, Feurstein D, Rossi GA, Sabatini F, Hatzelmann A. Inhibition of TGF-beta induced lung fibroblast to myofibroblast conversion by phosphodiesterase inhibiting drugs and activators of soluble guanylyl cyclase. Eur J Pharmacol. 2007;572:12-22.
26. Lagente V, Martin-Chouly C, Boichot E, Martins MA, Silva PM. Selective PDE4 inhibitors as potent anti-inflammatory drugs for the treatment of airway diseases. Mem Inst Oswaldo Cruz. 2005;100 Suppl 1:131-6.
27. Dinavahi SS, Nyayapathy S, Perumal Y, Dharmarajan S, Viswanadha S. Combined inhibition of PDE4 and PI3Kdelta modulates the inflammatory component involved in the progression of chronic obstructive pulmonary disease. Drug Res (Stuttg). 2014;64:214-9.
28. Fabbri LM, Calverley PM, Izquierdo-Alonso JL, Bundschuh DS, Brose M, Martinez FJ, et al. Roflumilast in moderate-to-severe chronic obstructive pulmonary disease treated with longacting bronchodilators: two randomised clinical trials. Lancet. 2009;374:695-703.
29. Calverley PM, Rabe KF, Goehring UM, Kristiansen S, Fabbri LM, Martinez FJ, et al. Roflumilast in symptomatic chronic obstructive pulmonary disease: two randomised clinical trials. Lancet. 2009;374:685-94.
30. Wanner A, Salathe M, O'Riordan TG. Mucociliary clearance in the airways. Am J Respir Crit Care Med. 1996;154:1868-902.
31. Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M. Pannexin 1 Contributes to ATP Release in Airway Epithelia. Am J Respir Cell Mol Biol. 2009;41:525-34.
32. Nlend MC, Schmid A, Sutto Z, Ransford GA, Conner GE, Fregien N, et al. Calcium-mediated, purinergic stimulation and polarized localization of calcium-sensitive adenylyl cyclase isoforms in human airway epithelia. FEBS Lett. 2007;581:3241-6.
33. Lambert JA, Raju SV, Tang LP, McNicholas CM, Li Y, Courville CA, et al. Cystic fibrosis transmembrane conductance regulator activation by roflumilast contributes to therapeutic benefit in chronic bronchitis. Am J Respir Cell Mol Biol. 2014;50:549-58.
34. Milara J, Armengot M, Banuls P, Tenor H, Beume R, Artigues E, et al. Roflumilast N-oxide, a PDE4 inhibitor, improves cilia motility and ciliated human bronchial epithelial cells compromised by cigarette smoke in vitro. Br J Pharmacol. 2012;166:2243-62.
35. Milara J, Serrano A, Peiro T, Artigues E, Gavalda A, Miralpeix M, et al. Aclidinium inhibits cigarette smoke-induced lung fibroblast-to-myofibroblast transition. Eur Respir J. 2013;41:1264-74.
36. Wyatt TA, Forget MA, Adams JM, Sisson JH. Both cAMP and cGMP are required for maximal ciliary beat stimulation in a cell-free model of bovine ciliary axonemes. Am J Physiol Lung Cell Mol Physiol. 2005;288:L546-51.
37. Di Benedetto G, Magnus CJ, Gray PTA, Mehta A. Calcium regulation of ciliary beat frequency in human respiratory epithelium in vitro. J Physiol London. 1991;439:103-13.
38. Salathe M, Pratt MM, Wanner A. Cyclic AMP-dependent phosphorylation of a 26 kD axonemal protein in ovine cilia isolated from small tissue pieces. Am J Respir Cell Mol Biol. 1993;9:306-14.
39. Seybold ZV, Mariassy AT, Stroh D, Kim CS, Gazeroglu H, Wanner A. Mucociliary interaction in vitro: effects of physiological and inflammatory stimuli. J Appl Physiol. 1990;68:1421-6.
40. Cantin AM, Bilodeau G, Ouellet C, Liao J, Hanrahan JW. Oxidant stress suppresses CFTR expression. Am J Physiol Cell Physiol. 2006;290:C262-70.
41. Pezzulo AA, Starner TD, Scheetz TE, Traver GL, Tilley AE, Harvey BG, et al. The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol. 2011;300:L25-31.
42. Leopold PL, O'Mahony MJ, Lian XJ, Tilley AE, Harvey BG, Crystal RG. Smoking is associated with shortened airway cilia. PLoS One. 2009;4, e8157.
43. 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;60:144-52.
44. Kreda SM, Nguyen T, Moussa L, Alonso-Galicia M, Qian M, Freire J. Roflumilast Inhibits Il-13-Induced Mucous Metaplasia In Airway Epithelium. Am J Respir Crit Care Med. 2014;189:A4871.
45. Tannheimer SL, Wright CD, Salmon M. Combination of roflumilast with a beta-2 adrenergic receptor agonist inhibits proinflammatory and profibrotic mediator release from human lung fibroblasts. Respir Res. 2012;13:28.