The cystic fibrosis transmembrane conductance regulator potentiator ivacaftor augments mucociliary clearance abrogating cystic fibrosis transmembrane conductance regulator inhibition by cigarette smoke

American Journal of Respiratory Cell and Molecular Biology

Volumn 56, Issue 1, 2017, Pages 99-108

  Raju, S Vamsee ^a,b   Lin, Vivian Y ^a   Liu, Limbo ^c   McNicholas, Carmel M ^b,d   Karki, Suman ^a   Sloane, Peter A ^a   Tang, Liping ^a,b   Jackson, Patricia L ^a,b   Wang, Wei ^b,d   Wilson, Landon ^e   MacOn, Kevin J ^f   Mazur, Marina ^b   Kappes, John C ^a,b   DeLucas, Lawrence J ^b,f   Barnes, Stephen ^e,g   Kirk, Kevin ^b,d   Tearney, Guillermo J ^c   Rowe, Steven M ^a,b,d,h  

^a University of Alabama at Birmingham   (United States)

^b Cystic Fibrosis Research Center   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Cell Developmental and Integrative Biology   (United States)

^e Targeted Metabolomics and Proteomics Laboratory   (United States)

^f Department of Optometry ^*  (United States)

^g Departtment of Pharmacology   (United States)

^h UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cigarette smoke; Cystic fibrosis transmembrane conductance regulator potentiator; Ivacaftor; Mucociliary transport; Optical coherence tomography

Indexed keywords

ACROLEIN; CIGARETTE SMOKE; CYSTEINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; IVACAFTOR; LYSINE; AMINOPHENOL DERIVATIVE; QUINOLONE DERIVATIVE;

ARTICLE; BIOTINYLATION; BRONCHUS; BRONCHUS MUCOSA; CHANNEL GATING; CILIARY MOTILITY; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; ION TRANSPORT; MASS SPECTROMETRY; MUCOCILIARY CLEARANCE; MUCOCILIARY TRANSPORT; OPTICAL COHERENCE TOMOGRAPHY; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; ADVERSE EFFECTS; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CHEMISTRY; CILIUM; DRUG EFFECTS; METABOLISM; MUCOSA; PATHOLOGY; SMOKING; TRACHEA;

ACROLEIN; AMINO ACID SEQUENCE; AMINOPHENOLS; BRONCHI; CELLS, CULTURED; CILIA; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; HUMANS; ION CHANNEL GATING; MUCOCILIARY CLEARANCE; MUCOUS MEMBRANE; QUINOLONES; SMOKING; TOMOGRAPHY, OPTICAL COHERENCE; TRACHEA;

EID: 85008428244     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0226OC     Document Type: Article

References (38)

1. National Heart, Lung, and Blood Institute. Unpublished Tabulations of the National Health Interview Survey. 2010 [accessed 2016 Aug 20]. Available from: http://www.nhlbi.nih.gov/files/docs/research/2012-ChartBook-508.pdf Data Source http://www.cdc.gov/nchs/nhis/nhis-2010-data-release.htm
2. Xu JQ, Kochanek KD, Murphy SL, Tejada-Vera B. Deaths: Final data for 2007. National vital statistics reports; vol 58 no 19. Hyattsville, MD: National Center for Health Statistics. 2010 [accessed 2016 Aug 20]. Available from: http://www.cdc.gov/nchs/data/nvsr/nvsr58/nvsr58-19.pdf
3. National Heart, Lung, and Blood Institute. COPD: the more you know, the better for you and your loved ones. Sep 2013 [accessed 2014 Jun 10]. Available from: https://www.nhlbi.nih.gov/health/educational/copd/campaign-materials/pub/copd-atrisk.pdf
4. Clunes LA, Davies CM, Coakley RD, Aleksandrov AA, Henderson AG, Zeman KL, Worthington EN, Gentzsch M, Kreda SM, Cholon D, et al. Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration. FASEB J 2012;26:533-545.
5. Kreindler JL, Jackson AD, Kemp PA, Bridges RJ, Danahay H. Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am J Physiol Lung Cell Mol Physiol 2005;288:L894-L902.
6. Savitski AN, Mesaros C, Blair IA, Cohen NA, Kreindler JL. Secondhand smoke inhibits both Cl2 and K1 conductances in normal human bronchial epithelial cells. Respir Res 2009;10:120.
7. Raju SV, Jackson PL, Courville CA, McNicholas CM, Sloane PA, Sabbatini G, Tidwell S, Tang LP, Liu B, Fortenberry JA, et al. Cigarette smoke induces systemic defects in cystic fibrosis transmembrane conductance regulator function. Am J Respir Crit Care Med 2013;188: 1321-1330.
8. Sloane PA, Shastry S, Wilhelm A, Courville C, Tang LP, Backer K, Levin E, Raju SV, Li Y, Mazur M, et al. A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease. PLoS One 2012;7:e39809.
9. Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, Gaggar A, Steele C, Tang LP, Liu B, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest 2013;144:498-506.
10. Courville CA, Tidwell S, Liu B, Accurso FJ, Dransfield MT, Rowe SM. Acquired defects in CFTR-dependent b-adrenergic sweat secretion in chronic obstructive pulmonary disease. Respir Res 2014;15:25.
11. 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 2006;173:1139-1144.
12. Hassan F, NuovoGJ, CrawfordM, Boyaka PN,KirkbyS,Nana-SinkamSP, Cormet-Boyaka E. MiR-101 and miR-144 regulate the expression of the CFTR chloride channel in the lung. PLoS One 2012;7:e50837.
13. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Cao D, Neuberger T, Turnbull A, Singh A, Joubran J, Hazlewood A, et al. Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci USA 2009;106:18825-18830.
14. Rowe SM, Pyle LC, Jurkevante A, Varga K, Collawn J, Sloane PA, Woodworth B, Mazur M, Fulton J, Fan L, et al. DeltaF508 CFTR processing correction and activity in polarized airway and nonairway cell monolayers. Pulm Pharmacol Ther 2010;23:268-278.
15. Jurkuvenaite A, Varga K, Nowotarski K, Kirk KL, Sorscher EJ, Li Y, Clancy JP, Bebok Z, Collawn JF. Mutations in the amino terminus of the cystic fibrosis transmembrane conductance regulator enhance endocytosis. J Biol Chem 2006;281:3329-3334.
16. McClure M, DeLucas LJ, Wilson L, Ray M, Rowe SM, Wu X, Dai Q, Hong JS, Sorscher EJ, Kappes JC, et al. Purification of CFTR for mass spectrometry analysis: identification of palmitoylation and other post-translational modifications. Protein Eng Des Sel 2012;25:7-14.
17. Liu L, Gardecki JA, Nadkarni SK, Toussaint JD, Yagi Y, Bouma BE, Tearney GJ. Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography. Nat Med 2011;17:1010-1014.
18. Liu L, Chu KK, Houser GH, Diephuis BJ, Li Y, Wilsterman EJ, Shastry S, Dierksen G, Birket SE, Mazur M, et al. Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography. PLoS One 2013;8:e54473.
19. van der Toorn M, Rezayat D, Kauffman HF, Bakker SJ, Gans RO, Koëter GH, Choi AM, van Oosterhout AJ, Slebos DJ. Lipid-soluble components in cigarette smoke induce mitochondrial production of reactive oxygen species in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009;297:L109-L114.
20. Lambert JA, Raju SV, Tang LP, McNicholas CM, Li Y, Courville CW, Faris RF, Coricor GE, Smoot LH, Mazur MM, et al. Cystic fibrosis transmembrane conductance regulator activation by roflumilast contributes to therapeutic benefit in chronic bronchitis. Am J Respir Cell Mol Biol 2014;50:549-558.
21. Raju SV, Tate JH, Peacock SK, Fang P, Oster RA, Dransfield MT, Rowe SM. Impact of heterozygote CFTR mutations in COPD patients with chronic bronchitis. Respir Res 2014;15:18.
22. Moran AR, Norimatsu Y, Dawson DC, MacDonald KD. Aqueous cigarette smoke extract induces a voltage-dependent inhibition of CFTR expressed in Xenopus oocytes. Am J Physiol Lung Cell Mol Physiol 2014;306:L284-L291.
23. Eiserich JP, van der Vliet A, Handelman GJ, Halliwell B, Cross CE. Dietary antioxidants and cigarette smoke-induced biomolecular damage: a complex interaction. Am J Clin Nutr 1995;62(6 suppl):1490S-1500S.
24. Lambert C, Li J, Jonscher K, Yang TC, Reigan P, Quintana M, Harvey J, Freed BM. Acrolein inhibits cytokine gene expression by alkylating cysteine and arginine residues in the NF-kB1 DNA binding domain. J Biol Chem 2007;282:19666-19675.
25. Cai J, Bhatnagar A, Pierce WM Jr. Protein modification by acrolein: formation and stability of cysteine adducts. Chem Res Toxicol 2009; 22:708-716.
26. Uchida K, Kanematsu M, Morimitsu Y, Osawa T, Noguchi N, Niki E. Acrolein is a product of lipid peroxidation reaction: formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 1998;273:16058-16066.
27. Deshmukh HS, Case LM, Wesselkamper SC, Borchers MT, Martin LD, Shertzer HG, Nadel JA, Leikauf GD. Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation. Am J Respir Crit Care Med 2005;171: 305-314.
28. Birket SE, Chu KK, Liu L, Houser GH, Diephuis BJ, Wilsterman EJ, Dierksen G, Mazur M, Shastry S, Li Y, et al. A functional anatomic defect of the cystic fibrosis airway. Am J Respir Crit Care Med 2014; 190:421-432.
29. Innes AL, Woodruff PG, Ferrando RE, Donnelly S, Dolganov GM, Lazarus SC, Fahy JV. Epithelial mucin stores are increased in the large airways of smokers with airflow obstruction. Chest 2006;130: 1102-1108.
30. Jih KY, Hwang TC. Vx-770 potentiates CFTR function by promoting decoupling between the gating cycle and ATP hydrolysis cycle. Proc Natl Acad Sci USA 2013;110:4404-4409.
31. Flume PA, Liou TG, Borowitz DS, Li H, Yen K, Ordoñez CL, Geller DE; VX 08-770-104 Study Group. Ivacaftor in subjects with cystic fibrosis who are homozygous for the F508del-CFTR mutation. Chest 2012; 142:718-724.
32. Guimbellot JS, Fortenberry JA, Siegal GP, Moore B, Wen H, Venglarik C, Chen YF, Oparil S, Sorscher EJ, Hong JS. Role of oxygen availability in CFTR expression and function. Am J Respir Cell Mol Biol 2008;39: 514-521.
33. Tilley AE, StaudtMR, Salit J, Van de Graaf B, Strulovici-Barel Y, Kaner RJ, Vincent T, Agosto-Perez F, Mezey JG, Raby BA, et al. Cigarette smoking induces changes in airway epithelial expression of genes associated with monogenic lung disorders. Am J Respir Crit Care Med 2016;193:215-217.
34. Le Gars M, Descamps D, Roussel D, Saussereau E, Guillot L, Ruffin M, Tabary O, Hong SS, Boulanger P, Paulais M, et al. Neutrophil elastase degrades cystic fibrosis transmembrane conductance regulator via calpains and disables channel function in vitro and in vivo. Am J Respir Crit Care Med 2013;187: 170-179.
35. Moss RB, Flume PA, Elborn JS, Cooke J, Rowe SM, McColley SA, Rubenstein RC, Higgins M; VX11-770-110 (KONDUCT) Study Group. Efficacy and safety of ivacaftor in patients with cystic fibrosis who have an Arg117His-CFTR mutation: a double-blind, randomised controlled trial. Lancet Respir Med 2015; 3:524-533.
36. Solomon GM, Raju SV, Dransfield MT, Rowe SM. Therapeutic approaches to acquired cystic fibrosis transmembrane conductance regulator dysfunction in chronic bronchitis. Ann Am Thorac Soc 2016;13:S169-S176.
37. Bennett WD, Almond MA, Zeman KL, Johnson JG, Donohue JF. Effect of salmeterol on mucociliary and cough clearance in chronic bronchitis. Pulm Pharmacol Ther 2006;19: 96-100.
38. Schwarzer C, Wong S, Shi J, Matthes E, Illek B, Ianowski JP, Arant RJ, Isacoff E, Vais H, Foskett JK, et al. Pseudomonas aeruginosa homoserine lactone activates store-operated cAMP and cystic fibrosis transmembrane regulator-dependent Cl2 secretion by human airway epithelia. J Biol Chem 2010;285: 34850-34863.