Roflumilast combined with adenosine increases mucosal hydration in human airway epithelial cultures after cigarette smoke exposure

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 10, 2015, Pages 1-10

  Tyrrell, Jean ^a   Qian, Xiaozhong ^b   Freire, Jose ^b   Tarran, Robert ^a  

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

^b FOREST RESEARCH INSTITUTE   (United States)

Author keywords

Airway hydration; Camp; Chronic obstructive pulmonary disease; Cystic fibrosis transmembrane conductance regulator; Roflumilast

Indexed keywords

ADENOSINE; CIGARETTE SMOKE; CYCLIC AMP; ISOPRENALINE; ROFLUMILAST; SALMETEROL; AMINOPYRIDINE DERIVATIVE; ANALGESIC AGENT; BENZAMIDE DERIVATIVE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CYCLOPROPANE DERIVATIVE; PHOSPHODIESTERASE IV INHIBITOR;

AIRWAY SURFACE LIQUID; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL LINING FLUID; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYDRATION; LONG TERM EXPOSURE; MUCOCILIARY CLEARANCE; PRIORITY JOURNAL; REHYDRATION; RESPIRATORY EPITHELIUM; ADVERSE EFFECTS; BRONCHUS; DIET THERAPY; METABOLISM; PATHOLOGY; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY TRACT MUCOSA; SMOKING;

ADENOSINE; ADRENERGIC BETA-AGONISTS; AMINOPYRIDINES; ANALGESICS; BENZAMIDES; BRONCHI; CYCLIC AMP; CYCLOPROPANES; HEK293 CELLS; HUMANS; ISOPROTERENOL; PHOSPHODIESTERASE 4 INHIBITORS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY MUCOSA; SMOKING;

EID: 84930844766     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00395.2014     Document Type: Article

References (57)

1. Angelis N, Porpodis K, Zarogoulidis P, Spyratos D, Kioumis I, Papaiwannou A, Pitsiou G, Tsakiridis K, Mpakas A, Arikas S, Tsiouda T, Katsikogiannis N, Kougioumtzi I, Machairiotis N, Argyriou M, Kessisis G, Zarogoulidis K. Airway inflammation in chronic obstructive pulmonary disease. J Thorac Dis 6: S167-S172, 2014.
2. Barnes AP, Livera G, Huang P, Sun C, O’Neal WK, Conti M, Stutts MJ, Milgram SL. Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J Biol Chem 280: 7997-8003, 2005.
3. Barnes PJ. Mediators of chronic obstructive pulmonary disease. Pharmacol Rev 56: 515-548, 2004.
4. Bateman ED, Rabe KF, Calverley PM, Goehring UM, Brose M, Bredenbroker D, Fabbri LM. Roflumilast with long-acting beta2-ago-nists for COPD: influence of exacerbation history. Eur Respir J 38: 553-560, 2011.
5. Boswell-Smith V, Page CP. Roflumilast: a phosphodiesterase-4 inhibitor for the treatment of respiratory disease. Expert Opin Investig Drugs 15: 1105-1113, 2006.
6. Boucher RC. Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu Rev Med 58: 157-170, 2007.
7. Boucher RC, Stutts MJ, Knowles MR, Cantley L, Gatzy JT. Na+ transport in cystic fibrosis respiratory epithelia. Abnormal basal rate and response to adenylate cyclase activation. J Clin Invest 78: 1245-1252, 1986.
8. Calverley PM, Anderson JA, Celli B, Ferguson GT, Jenkins C, Jones PW, Yates JC, Vestbo J. Salmeterol and fluticasone propionate and survival in chronic obstructive pulmonary disease. N Engl J Med 356: 775-789, 2007.
9. Calverley PM, Sanchez-Toril F, McIvor A, Teichmann P, Breden-broeker D, Fabbri LM. Effect of 1-year treatment with roflumilast in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176: 154-161, 2007.
10. 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.
11. Cazzola M, Page CP, Calzetta L, Matera MG. Pharmacology and therapeutics of bronchodilators. Pharmacol Rev 64: 450-504, 2012.
12. Chavez-Noriega LE, Stevens CF. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14: 310-317, 1994.
13. Clancy JP, Ruiz FE, Sorscher EJ. Adenosine and its nucleotides activate wild-type and R117H CFTR through an A2B receptor-coupled pathway. Am J Physiol Cell Physiol 276: C361-C369, 1999.
14. Clunes LA, Bridges A, Alexis N, Tarran R. In vivo versus in vitro airway surface liquid nicotine levels following cigarette smoke exposure. J Anal Toxicol 32: 201-207, 2008.
15. 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.
16. Conti M, Beavo J. Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511, 2007.
17. Donaldson SH, Bennett WD, Zeman KL, Knowles MR, Tarran R, Boucher RC. Mucus clearance and lung function in cystic fibrosis with hypertonic saline. N Engl J Med 354: 241-250, 2006.
18. Donohue JF. Therapeutic responses in asthma and COPD. Bronchodilators. Chest 126: 125S-137S;discussion 159S-161S, 2004.
19. Driver AG, Kukoly CA, Ali S, Mustafa SJ. Adenosine in bronchoal-veolar lavage fluid in asthma. Am Rev Respir Dis 148: 91-97, 1993.
20. Fabbri LM, Calverley PM, Izquierdo-Alonso JL, Bundschuh DS, Brose M, Martinez FJ, Rabe KF. Roflumilast in moderate-to-severe chronic obstructive pulmonary disease treated with long-acting bronchodilators: two randomised clinical trials. Lancet 374: 695-703, 2009.
21. Hatzelmann A, Morcillo EJ, Lungarella G, Adnot S, Sanjar S, Beume R, Schudt C, Tenor H. The preclinical pharmacology of roflumilast—a selective, oral phosphodiesterase 4 inhibitor in development for chronic obstructive pulmonary disease. Pulm Pharmacol Ther 23: 235-256, 2010.
22. Hirota N, Martin JG. Mechanisms of airway remodeling. Chest 144: 1026-1032, 2013.
23. Hirsh AJ, Sabater JR, Zamurs A, Smith RT, Paradiso AM, Hopkins S, Abraham WM, Boucher RC. Evaluation of second generation amiloride analogs as therapy for cystic fibrosis lung disease. J Pharmacol Exp Ther 311: 929-938, 2004.
24. Hobbs CA, Blanchard MG, Alijevic O, Tan CD, Kellenberger S, Bencharit S, Cao R, Kesimer M, Walton WG, Henderson AG, Red-inbo MR, Stutts MJ, Tarran R. Identification of SPLUNC1's ENaC-inhibitory domain yields novel strategies to treat sodium hyperabsorption in cystic fibrosis airway cultures. Am J Physiol Lung Cell Mol Physiol 305: L990-L1001, 2013.
25. Hogg JC, Timens W. The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol 4: 435–459, 2009.
26. Houslay MD. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35: 91-100, 2009.
27. Jiang C, Finkbeiner WE, Widdicombe JH, McCray PB Jr, Miller SS. Altered fluid transport across airway epithelium in cystic fibrosis. Science 262: 424-427, 1993.
28. Johnson M. Molecular mechanisms of beta(2)-adrenergic receptor function, response, and regulation. J Allergy Clin Immunol 117: 18-24; quiz 25, 2006.
29. Kaur M, Holden NS, Wilson SM, Sukkar MB, Chung KF, Barnes PJ, Newton R, Giembycz MA. Effect of fj2-adrenoceptor agonists and other cAMP-elevating agents on inflammatory gene expression in human ASM cells: a role for protein kinase A. Am J Physiol Lung Cell Mol Physiol 295: L505-L514, 2008.
30. Klass DJ. Cigarette smoke exposure in vivo increases cyclic GMP in rat lung. Arch Environ Health 35: 347-350, 1980.
31. Lahu G, Nassr N, Hunnemeyer A. Pharmacokinetic evaluation of roflumilast. Expert Opin Drug Metab Toxicol 7: 1577-1591, 2011.
32. Lambert JA, Raju SV, Tang LP, McNicholas CM, Li Y, Courville CA, Farris RF, Coricor GE, Smoot LH, Mazur MM, Dransfield MT, Bolger GB, Rowe SM. CFTR activation by roflumilast contributes to therapeutic benefit in chronic bronchitis. Am J Respir Cell Mol Biol 50: 549-558, 2014.
33. Lazarowski ER, Tarran R, Grubb BR, van Heusden CA, Okada S, Boucher RC. Nucleotide release provides a mechanism for airway surface liquid homeostasis. J Biol Chem 279: 36855-36864, 2004.
34. Liu S, Veilleux A, Zhang L, Young A, Kwok E, Laliberte F, Chung C, Tota MR, Dube D, Friesen RW, Huang Z. Dynamic activation of cystic fibrosis transmembrane conductance regulator by type 3 and type 4D phosphodiesterase inhibitors. J Pharmacol Exp Ther 314: 846-854, 2005.
35. 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.
36. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015, 1998.
37. McCahill AC, Huston E, Li X, Houslay MD. PDE4 associates with different scaffolding proteins: modulating interactions as treatment for certain diseases. Hand Exp Pharmacol 186: 125-166, 2008.
38. Milara J, Armengot M, Banuls P, Tenor H, Beume R, Artigues E, Cortijo J. Roflumilast N-oxide, a PDE4 inhibitor, improves cilia motility and ciliated human bronchial epithelial cells compromised by cigarette smoke in vitro. Br J Pharmacol 166: 2243-2262, 2012.
39. Mundell SJ, Olah ME, Panettieri RA, Benovic JL, Penn RB. Regulation of G protein-coupled receptor-adenylyl cyclase responsiveness in human airway smooth muscle by exogenous and autocrine adenosine. Am J Respir Cell Mol Biol 24: 155-163, 2001.
40. Naren AP, Cobb B, Li C, Roy K, Nelson D, Heda GD, Liao J, Kirk KL, Sorscher EJ, Hanrahan J, Clancy JP. A macromolecular complex of beta 2 adrenergic receptor, CFTR, and ezrin/radixin/moesin-binding phosphoprotein 50 is regulated by PKA. Proc Natl Acad Sci USA 100: 342–346, 2003.
41. Oldenburger A, Maarsingh H, Schmidt M. Multiple facets of cAMP signalling and physiological impact: cAMP compartmentalization in the lung. Pharmaceuticals (Basel) 5: 1291–1331, 2012.
42. Pappas K, Papaioannou AI, Kostikas K, Tzanakis N. The role of macrophages in obstructive airways disease: Chronic obstructive pulmonary disease and asthma. Cytokine 64: 613–625, 2013.
43. Poggi P, Rota MT, Boratto R. The volatile fraction of cigarette smoke induces alterations in the human gingival fibroblast cytoskeleton. J Peri-odontal Res 37: 230–235, 2002.
44. Rab A, Rowe SM, Raju SV, Bebok Z, Matalon S, Collawn JF. Cigarette smoke and CFTR: implications in the pathogenesis of COPD. Am J Physiol Lung Cell Mol Physiol 305: L530–L541, 2013.
45. Randell SH, Fulcher ML, O’Neal W, Olsen JC. Primary epithelial cell models for cystic fibrosis research. Methods Mol Biol 742: 285–310, 2011.
46. Razvi S, Quittell L, Sewall A, Quinton H, Marshall B, Saiman L. Respiratory microbiology of patients with cystic fibrosis in the United States, 1995 to 2005. Chest 136: 1554–1560, 2009.
47. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M. Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39: 127–132, 2008.
48. 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.
49. Taegtmeyer AB, Leuppi JD, Kullak-Ublick GA. Roflumilast—a phos-phodiesterase-4 inhibitor licensed for add-on therapy in severe COPD. Swiss Med Wkly 142: w13628, 2012.
50. Tarran R, Grubb BR, Parsons D, Picher M, Hirsh AJ, Davis CW, Boucher RC. The CF salt controversy: in vivo observations and therapeutic approaches. Mol Cell 8: 149–158, 2001.
51. 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.
52. Tashkin DP, Fabbri LM. Long-acting beta-agonists in the management of chronic obstructive pulmonary disease: current and future agents. Respir Res 11: 149, 2010.
53. Ulrik CS. Clinical benefit of fixed-dose dual bronchodilation with glyco-pyrronium and indacaterol once daily in patients with chronic obstructive pulmonary disease: a systematic review. Int J Chron Obstruct Pulmon Dis 9: 331–338, 2014.
54. van den Berge M, Hylkema MN, Versluis M, Postma DS. Role of adenosine receptors in the treatment of asthma and chronic obstructive pulmonary disease: recent developments. Drugs R D 8: 13–23, 2007.
55. Versluis M, ten Hacken N, Postma D, Barroso B, Rutgers B, Geerlings M, Willemse B, Timens W, Hylkema M. Adenosine receptors in COPD and asymptomatic smokers: effects of smoking cessation. Virchows Arch 454: 273–281, 2009.
56. Violin JD, DiPilato LM, Yildirim N, Elston TC, Zhang J, Lefkowitz RJ. Beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J Biol Chem 283: 2949–2961, 2008.
57. 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.