Continuous mucociliary transport by primary human airway epithelial cells in vitro

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 2, 2015, Pages L99-L108

  Sears, Patrick R ^a   Yin, Wei Ning ^a   Ostrowski, Lawrence E ^a  

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

Author keywords

Airway; Cilia; Human; Mucociliary; Mucus

Indexed keywords

FORSKOLIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CILIARY MOTILITY; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MUCOCILIARY TRANSPORT; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; CYTOLOGY; EUKARYOTIC FLAGELLUM; METABOLISM; MUCOCILIARY CLEARANCE; MUCUS; PHASE CONTRAST MICROSCOPY; PHYSIOLOGY; RESPIRATORY SYSTEM; SECRETION (PROCESS); ULTRASTRUCTURE;

CELLS, CULTURED; CILIA; EPITHELIAL CELLS; HUMANS; IN VITRO TECHNIQUES; MICROSCOPY, PHASE-CONTRAST; MUCOCILIARY CLEARANCE; MUCUS; RESPIRATORY SYSTEM;

EID: 84937485376     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00024.2015     Document Type: Article

References (48)

1. Bennett WD. Effect of beta-adrenergic agonists on mucociliary clearance. J Allergy Clin Immunol 110: S291-S297, 2002.
2. Bennett WD, Laube BL, Corcoran T, Zeman K, Sharpless G, Thomas K, Wu J, Mogayzel PJ Jr, Pilewski J, Donaldson S. Multisite comparison of mucociliary and cough clearance measures using standardized methods. J Aerosol Med 26: 157-164, 2013.
3. Bhashyam AR, Mogayzel PJ Jr, McGrath-Morrow S, Neptune E, Malinina A, Fox J, Laube BL. A pilot study to examine the effect of chronic treatment with immunosuppressive drugs on mucociliary clearance in a vagotomized murine model. PLos One 7: e45312, 2012.
4. Bush A, Hogg C. Primary ciliary dyskinesia: recent advances in epidemiology, diagnosis, management and relationship with the expanding spectrum of ciliopathy. Expert Rev Respir Med 6: 663-682, 2012.
5. Button B, Boucher RC. Role of mechanical stress in regulating airway surface hydration and mucus clearance rates. Respir Physiol Neurobiol 163: 189-201, 2008.
6. Button B, Okada SF, Frederick CB, Thelin WR, Boucher RC. Mechanosensitive ATP release maintains proper mucus hydration of airways. Sci Signal 6: ra46, 2013.
7. Cooper JL, Quinton PM, Ballard ST. Mucociliary transport in porcine trachea: differential effects of inhibiting chloride and bicarbonate secretion. Am J Physiol Lung Cell Mol Physiol 304: L184-L190, 2013.
8. Donaldson SH, Corcoran TE, Laube BL, Bennett WD. Mucociliary clearance as an outcome measure for cystic fibrosis clinical research. Proc Am Thorac Soc 4: 399-405, 2007.
9. Fahy JV, Dickey BF. Airway mucus function and dysfunction. N Engl J Med 363: 2233-2247, 2010.
10. Foster WM, Walters DM, Longphre M, Macri K, Miller LM. Methodology for the measurement of mucociliary function in the mouse by scintigraphy. J Appl Physiol 90: 1111-1117, 2001.
11. Francis R, Lo C. Ex vivo method for high resolution imaging of cilia motility in rodent airway epithelia. J Vis Exp 78: e50343, 2013.
12. Francis RJ, Chatterjee B, Loges NT, Zentgraf H, Omran H, Lo CW. Initiation and maturation of cilia-generated flow in newborn and postnatal mouse airway. Am J Physiol Lung Cell Mol Physiol 296: L1067-L1075, 2009.
13. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 107: 183-206, 2005.
14. Fulcher ML, Randell SH. Human nasal and tracheo-bronchial respiratory epithelial cell culture. Methods Mol Biol 945: 109-121, 2013.
15. Gray TE, Guzman K, Davis CW, Abdullah LH, Nettesheim P. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 14: 104-112, 1996.
16. Grubb BR, Jones JH, Boucher RC. Mucociliary transport determined by in vivo microdialysis in the airways of normal and CF mice. Am J Physiol Lung Cell Mol Physiol 286: L588-L595, 2004.
17. Guirao B, Meunier A, Mortaud S, Aguilar A, Corsi JM, Strehl L, Hirota Y, Desoeuvre A, Boutin C, Han YG, Mirzadeh Z, Cremer H, Montcouquiol M, Sawamoto K, Spassky N. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12: 341-350, 2010.
18. Henderson AG, Ehre C, Button B, Abdullah LH, Cai LH, Leigh MW, DeMaria GC, Matsui H, Donaldson SH, Davis CW, Sheehan JK, Boucher RC, Kesimer M. Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J Clin Invest 124: 3047-3060, 2014.
19. Hill DB, Vasquez PA, Mellnik J, McKinley SA, Vose A, Mu F, Henderson AG, Donaldson SH, Alexis NE, Boucher RC, Forest MG. A biophysical basis for mucus solids concentration as a candidate biomarker for airways disease. PLos One 9: e87681, 2014.
20. Hoegger MJ, Awadalla M, Namati E, Itani OA, Fischer AJ, Tucker AJ, Adam RJ, McLennan G, Hoffman EA, Stoltz DA, Welsh MJ. Assessing mucociliary transport of single particles in vivo shows variable speed and preference for the ventral trachea in newborn pigs. Proc Natl Acad Sci U S A 111: 2355-2360, 2014.
21. Kesimer M, Kirkham S, Pickles RJ, Henderson AG, Alexis NE, Demaria G, Knight D, Thornton DJ, Sheehan JK. Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? Am J Physiol Lung Cell Mol Physiol 296: L92-L100, 2009.
22. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109: 571-577, 2002.
23. Lay JC, Stang MR, Fisher PE, Yankaskas JR, Bennett WD. Airway retention of materials of different solubility following local intrabronchial deposition in dogs. J Aerosol Med 16: 153-166, 2003.
24. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA. Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 11: 473-487, 2009.
25. Liu L, Chu KK, Houser GH, Diephuis BJ, Li Y, Wilsterman EJ, Shastry S, Dierksen G, Birket SE, Mazur M, Byan-Parker S, Grizzle WE, Sorscher EJ, Rowe SM, Tearney GJ. Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography. PLos One 8: e54473, 2013.
26. Look DC, Walter MJ, Williamson MR, Pang L, You Y, Sreshta JN, Johnson JE, Zander DS, Brody SL. Effects of paramyxoviral infection on airway epithelial cell Foxj1 expression, ciliogenesis, and mucociliary function. Am J Pathol 159: 2055-2069, 2001.
27. Lundin M, Sandberg T, Caldwell KD, Blomberg E. Comparison of the adsorption kinetics and surface arrangement of "as received" and purified bovine submaxillary gland mucin (BSM) on hydrophilic surfaces. J Colloid Interface Sci 336: 30-39, 2009.
28. 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.
29. Matsui H, Randell SH, Peretti SW, Davis CW, Boucher RC. Coordinated clearance of periciliary liquid and mucus from airway surfaces. J Clin Invest 102: 1125-1131, 1998.
30. Matsui H, Verghese MW, Kesimer M, Schwab UE, Randell SH, Sheehan JK, Grubb BR, Boucher RC. Reduced three-dimensional motility in dehydrated airway mucus prevents neutrophil capture and killing bacteria on airway epithelial surfaces. J Immunol 175: 1090-1099, 2005.
31. 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.
32. Ostrowski LE, Yin W, Rogers TD, Busalacchi KB, Chua M, O'Neal WK, Grubb BR. Conditional deletion of dnaic1 in a murine model of primary ciliary dyskinesia causes chronic rhinosinusitis. Am J Respir Cell Mol Biol 43: 55-63, 2010.
33. Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG. Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Respir Cell Mol Biol 42: 450-460, 2010.
34. Rogers DF. Mucociliary dysfunction in COPD: effect of current pharmacotherapeutic options. Pulm Pharmacol Ther 18: 1-8, 2005.
35. Sabater JR, Mao YM, Shaffer C, James MK, O'Riordan TG, Abraham WM. Aerosolization of P2Y(2)-receptor agonists enhances mucociliary clearance in sheep. J Appl Physiol 87: 2191-2196, 1999.
36. Satir P, Barkalow K, Hamasaki T. Ciliary beat frequency is controlled by a dynein light chain phosphorylation. Biophys J 68: 222S, 1995.
37. Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski LE, Conner GE, Fregien N, Salathe M. Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells. J Cell Sci 119: 4176-4186, 2006.
38. Seagrave J, Albrecht HH, Hill DB, Rogers DF, Solomon G. Effects of guaifenesin, N-acetylcysteine, and ambroxol on MUC5AC and mucociliary transport in primary differentiated human tracheal-bronchial cells. Respir Res 13: 98, 2012.
39. Seibert FS, Chang XB, Aleksandrov AA, Clarke DM, Hanrahan JW, Riordan JR. Influence of phosphorylation by protein kinase A on CFTR at the cell surface and endoplasmic reticulum. Biochim Biophys Acta 1461: 275-283, 1999.
40. Smith CM, Hirst RA, Bankart MJ, Jones DW, Easton AJ, Andrew PW, O'Callaghan C. Cooling of cilia allows functional analysis of the beat pattern for diagnostic testing. Chest 140: 186-190, 2011.
41. Sutto Z, Conner GE, Salathe M. Regulation of human airway ciliary beat frequency by intracellular pH. J Physiol 560: 519-532, 2004.
42. Tarran R, Button B, Boucher RC. Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress. Annu Rev Physiol 68: 543-561, 2006.
43. Tarran R, Button B, Picher M, Paradiso AM, Ribeiro CM, Lazarowski ER, Zhang L, Collins PL, Pickles RJ, Fredberg JJ, Boucher RC. Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J Biol Chem 280: 35751-35759, 2005.
44. Thornton DJ, Gray T, Nettesheim P, Howard M, Koo JS, Sheehan JK. Characterization of mucins from cultured normal human tracheobronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 278: L1118-L1128, 2000.
45. Vladar EK, Bayly RD, Sangoram AM, Scott MP, Axelrod JD. Microtubules enable the planar cell polarity of airway cilia. Curr Biol 22: 2203-2212, 2012.
46. Wanner A, Salathe M, O'Riordan TG. Mucociliary clearance in the airways. Am J Respir Crit Care Med 154: 1868-1902, 1996.
47. Zahm JM, Gaillard D, Dupuit F, Hinnrasky J, Porteous D, Dorin JR, Puchelle E. Early alterations in airway mucociliary clearance and inflammation of the lamina propria in CF mice. Am J Physiol Cell Physiol 272: C853-C859, 1997.
48. Zhang L, Button B, Gabriel SE, Burkett S, Yan Y, Skiadopoulos MH, Dang YL, Vogel LN, McKay T, Mengos A, Boucher RC, Collins PL, Pickles RJ. CFTR delivery to 25% of surface epithelial cells restores normal rates of mucus transport to human cystic fibrosis airway epithelium. PLoS Biol 7: e1000155, 2009.