Role of mechanical stress in regulating airway surface hydration and mucus clearance rates

Respiratory Physiology and Neurobiology

Volumn 163, Issue 1-3, 2008, Pages 189-201

  Button, Brian ^a   Boucher, Richard C ^a  

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

Author keywords

Airway hydration; Mechanical stress; Mucociliary clearance

Indexed keywords

ADENOSINE; ADENOSINE TRIPHOSPHATE; NUCLEOSIDE; NUCLEOTIDE; PURINE; PYRIMIDINE; SODIUM CHLORIDE COTRANSPORTER; URIDINE TRIPHOSPHATE;

ARTICLE; CELL CULTURE; CELL METABOLISM; CELL SURFACE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CILIARY MOTILITY; CYSTIC FIBROSIS; DEFENSE MECHANISM; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDRATION; INNATE IMMUNITY; ION TRANSPORT; LUNG CLEARANCE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MUCOCILIARY CLEARANCE; MUCUS; MUCUS SECRETION; OSCILLATION; PRIORITY JOURNAL; RESPIRATION CONTROL; RESPIRATORY EPITHELIUM; STIMULATION; VIBRATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; EXTRACELLULAR FLUID; HUMANS; ION TRANSPORT; MUCOCILIARY CLEARANCE; RESPIRATORY MUCOSA; RESPIRATORY TRACT DISEASES; STRESS, MECHANICAL;

EID: 54049116737     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2008.04.020     Document Type: Article

References (145)

1. Alsuwaidan S., Li Wan Po A., Morrison G., Redmond A., Dodge J.A., McElnay J., Stewart E., and Stanford C.F. Effect of exercise on the nasal transmucosal potential difference in patients with cystic fibrosis and normal subjects. Thorax 49 (1994) 1249-1250
2. App E.M., Kieselmann R., Reinhardt D., Lindemann H., Dasgupta B., King M., and Brand P. Sputum rheology changes in cystic fibrosis lung disease following two different types of physiotherapy: flutter vs. autogenic drainage. Chest 114 (1998) 171-177
3. Bankston L.A., and Guidotti G. Characterization of ATP transport into chromaffin granule ghosts. Synergy of ATP and serotonin accumulation in chromaffin granule ghosts. J. Biol. Chem. 271 (1996) 17132-17138
4. Basser P.J., McMahon T.A., and Griffith P. The mechanism of mucus clearance in cough. J. Biomech. Eng. 111 (1989) 288-297
5. Bennett W.D., Foster W.M., and Chapman W.F. Cough-enhanced mucus clearance in the normal lung. J. Appl. Physiol. 69 (1990) 1670-1675
6. Bennett W.D., Olivier K.N., Zeman K.L., Hohneker K.W., Boucher R.C., and Knowles M.R. Effect of uridine 5′-triphosphate plus amiloride on mucociliary clearance in adult cystic fibrosis. Am. J. Respir. Crit. Care Med. 153 (1996) 1796-1801
7. Bennett W.D., and Zeman K.L. Effect of enhanced supramaximal flows on cough clearance. J. Appl. Physiol. 77 (1994) 1577-1583
8. Bennett W.D., Zeman K.L., Foy C., Shaffer C.L., Johnson F.L., Regnis J.A., Sannuti A., and Johnson J. Effect of aerosolized uridine 5′-triphosphate on mucociliary clearance in mild chronic bronchitis. Am. J. Respir. Crit. Care Med. 164 (2001) 302-306
9. Benos D.J. Sensing tension: recognizing ENaC as a stretch sensor. Hypertension 44 (2004) 616-617
10. Bodin P., and Burnstock G. Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J. Cardiovasc. Pharmacol. 38 (2001) 900-908
11. Boucher R.C. Human airway ion transport. Part one. Am. J. Respir. Crit. Care Med. 150 (1994) 271-281
12. Boucher R.C. An overview of the pathogenesis of cystic fibrosis lung disease. Adv. Drug. Deliv. Rev. 54 (2002) 1359-1371
13. Boucher R.C. Regulation of airway surface liquid volume by human airway epithelia. Pflugers Arch. 445 (2003) 495-498
14. Boucher R.C. Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu. Rev. Med. 58 (2007) 157-170
15. Boudreault F., and Grygorczyk R. Cell swelling-induced ATP release is tightly dependent on intracellular calcium elevations. J. Physiol. 561 (2004) 499-513
16. Boyton R.J., and Openshaw P.J. Pulmonary defences to acute respiratory infection. Br. Med. Bull. 61 (2002) 1-12
17. Bradley, J., Moran, F., 2002. Physical training for cystic fibrosis. Cochrane Database Syst. Rev. CD002768.
18. Bramley A.M., Thomson R.J., Roberts C.R., and Schellenberg R.R. Hypothesis: excessive bronchoconstriction in asthma is due to decreased airway elastance. Eur. Respir. J. 7 (1994) 337-341
19. Braunstein G.M., Roman R.M., Clancy J.P., Kudlow B.A., Taylor A.L., Shylonsky V.G., Jovov B., Peter K., Jilling T., Ismailov II, Benos D.J., Schwiebert L.M., Fitz J.G., and Schwiebert E.M. Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation. J. Biol. Chem. 276 (2001) 6621-6630
20. Button B., Picher M., and Boucher R.C. Differential effects of cyclic and constant stress on ATP release and mucociliary transport by human airway epithelia. J. Physiol. 580 (2007) 577-592
21. Chang X.B., Tabcharani J.A., Hou Y.X., Jensen T.J., Kartner N., Alon N., Hanrahan J.W., and Riordan J.R. Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all 10 PKA consensus phosphorylation sites. J. Biol. Chem. 268 (1993) 11304-11311
22. Chrzanowska-Wodnicka M., and Burridge K. Rho, rac and the actin cytoskeleton. Bioessays 14 (1992) 777-778
23. Clancy J.P., Ruiz F.E., and Sorscher E.J. Adenosine and its nucleotides activate wild-type and R117H CFTR through an A2B receptor-coupled pathway. Am. J. Physiol. 276 (1999) C361-369
24. Clapham D.E. TRP channels as cellular sensors. Nature 426 (2003) 517-524
25. Clarke L.L., and Boucher R.C. Chloride secretory response to extracellular ATP in human normal and cystic fibrosis nasal epithelia. Am. J. Physiol. 263 (1992) C348-C356
26. Crews A., Taylor A.E., and Ballard S.T. Liquid transport properties of porcine tracheal epithelium. J. Appl. Physiol. 91 (2001) 797-802
27. Davis I.C., Lazarowski E.R., Hickman-Davis J.M., Fortenberry J.A., Chen F.P., Zhao X., Sorscher E., Graves L.M., Sullender W.M., and Matalon S. Leflunomide prevents alveolar fluid clearance inhibition by respiratory syncytial virus. Am. J. Respir. Crit. Care Med. 173 (2006) 673-682
28. Davis I.C., Sullender W.M., Hickman-Davis J.M., Lindsey J.R., and Matalon S. Nucleotide-mediated inhibition of alveolar fluid clearance in BALB/c mice after respiratory syncytial virus infection. Am. J. Physiol. Lung Cell Mol. Physiol. 286 (2004) L112-120
29. Devor D.C., Bridges R.J., and Pilewski J.M. Pharmacological modulation of ion transport across wild-type and DeltaF508 CFTR-expressing human bronchial epithelia. Am. J. Physiol. Cell Physiol. 279 (2000) C461-479
30. Devor D.C., and Pilewski J.M. UTP inhibits Na+ absorption in wild-type and DeltaF508 CFTR-expressing human bronchial epithelia. Am. J. Physiol. 276 (1999) C827-837
31. Dietl P., Haller T., Mair N., and Frick M. Mechanisms of surfactant exocytosis in alveolar type II cells in vitro and in vivo. News Physiol. Sci. 16 (2001) 239-243
32. Donaldson S.H., Lazarowski E.R., Picher M., Knowles M.R., Stutts M.J., and Boucher R.C. Basal nucleotide levels, release, and metabolism in normal and cystic fibrosis airways. Mol. Med. 6 (2000) 969-982
33. Dudek S.M., and Garcia J.G. Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91 (2001) 1487-1500
34. Elad D., Naftali S., Rosenfeld M., and Wolf M. Physical stresses at the air-wall interface of the human nasal cavity during breathing. J. Appl. Physiol. 100 (2006) 1003-1010
35. Evans J.H., and Sanderson M.J. Intracellular calcium oscillations regulate ciliary beat frequency of airway epithelial cells. Cell Calcium 26 (1999) 103-110
36. Even-Tzur N., Elad D., Zaretsky U., Randell S.H., Haklai R., and Wolf M. Custom-designed wells and flow chamber for exposing air-liquid interface cultures to wall shear stress. Ann. Biomed. Eng. 34 (2006) 1890-1895
37. Farinas J., Kneen M., Moore M., and Verkman A.S. Plasma membrane water permeability of cultured cells and epithelia measured by light microscopy with spatial filtering. J. Gen. Physiol. 110 (1997) 283-296
38. Fredberg J.J., and Moore J.A. The distributed response of complex branching duct networks. J. Acoust. Soc. Am. 63 (1978) 954-961
39. Galbraith C.G., Skalak R., and Chien S. Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil. Cytoskeleton 40 (1998) 317-330
40. Gatof D., Kilic G., and Fitz J.G. Vesicular exocytosis contributes to volume-sensitive ATP release in biliary cells. Am. J. Physiol. Gastrointest. Liver Physiol. 286 (2004) G538-546
41. Gonzalez F.A., Weisman G.A., Erb L., Seye C.I., Sun G.Y., Velazquez B., Hernandez-Perez M., and Chorna N.E. Mechanisms for inhibition of P2 receptors signaling in neural cells. Mol. Neurobiol. 31 (2005) 65-79
42. 2+]i transients and oscillations in mouse fibroblasts are mediated by endogenously released ATP. J. Biol. Chem. 270 (1995) 4451-4456
43. Grubb B.R., and Boucher R.C. Effect of in vivo corticosteroids on Na+ transport across airway epithelia. Am. J. Physiol. 275 (1998) C303-308
44. Grygorczyk R., and Hanrahan J.W. CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. Am. J. Physiol. 272 (1997) C1058-1066
45. Gunst S.J., and Stropp J.Q. Pressure-volume and length-stress relationships in canine bronchi in vitro. J. Appl. Physiol. 64 (1988) 2522-2531
46. Guyot A., and Hanrahan J.W. ATP release from human airway epithelial cells studied using a capillary cell culture system. J. Physiol. 545 (2002) 199-206
47. Hamill O.P. Twenty odd years of stretch-sensitive channels. Pflugers Arch. 453 (2006) 333-351
48. Hebestreit A., Kersting U., Basler B., Jeschke R., and Hebestreit H. Exercise inhibits epithelial sodium channels in patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 164 (2001) 443-446
49. Hentchel-Franks K., Lozano D., Eubanks-Tarn V., Cobb B., Fan L., Oster R., Sorscher E., and Clancy J.P. Activation of airway cl- secretion in human subjects by adenosine. Am. J. Respir. Cell Mol. Biol. 31 (2004) 140-146
50. Hirsh A.J., Stonebraker J.R., van Heusden C.A., Lazarowski E.R., Boucher R.C., and Picher M. Adenosine deaminase 1 and concentrative nucleoside transporters 2 and 3 regulate adenosine on the apical surface of human airway epithelia: implications for inflammatory lung diseases. Biochemistry 46 (2007) 10373-10383
51. Homolya L., Steinberg T.H., and Boucher R.C. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J. Cell Biol. 150 (2000) 1349-1360
52. Jia Y., Mathews C.J., and Hanrahan J.W. Phosphorylation by protein kinase C is required for acute activation of cystic fibrosis transmembrane conductance regulator by protein kinase A. J. Biol. Chem. 272 (1997) 4978-4984
53. Kallok M.J., Lai-Fook S.J., Hajji M.A., and Wilson T.A. Axial distortion of airways in the lung. J. Appl. Physiol. 54 (1983) 185-190
54. Kellerman D., Evans R., Mathews D., and Shaffer C. Inhaled P2Y2 receptor agonists as a treatment for patients with cystic fibrosis lung disease. Adv. Drug Deliv. Rev. 54 (2002) 1463-1474
55. Kellerman D.J. P2Y(2) receptor agonists: a new class of medication targeted at improved mucociliary clearance. Chest 121 (2002) 201S-205S
56. Kempainen R.R., Williams C.B., Hazelwood A., Rubin B.K., and Milla C.E. Comparison of high-frequency chest wall oscillation with differing waveforms for airway clearance in cystic fibrosis. Chest 132 (2007) 1227-1232
57. Kilburn K.H. A hypothesis for pulmonary clearance and its implications. Am. Rev. Respir. Dis. 98 (1968) 449-463
58. King M., Phillips D.M., Gross D., Vartian V., Chang H.K., and Zidulka A. Enhanced tracheal mucus clearance with high frequency chest wall compression. Am. Rev. Respir. Dis. 128 (1983) 511-515
59. Kitterman J.A. The effects of mechanical forces on fetal lung growth. Clin. Perinatol. 23 (1996) 727-740
60. Knight G.E., Bodin P., De Groat W.C., and Burnstock G. ATP is released from guinea pig ureter epithelium on distension. Am. J. Physiol. Renal Physiol. 282 (2002) F281-288
61. Knowles M.R., and Boucher R.C. Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109 (2002) 571-577
62. Knowles M.R., Clarke L.L., and Boucher R.C. Activation by extracellular nucleotides of chloride secretion in the airway epithelia of patients with cystic fibrosis. [comment]. N. Engl. J. Med. 325 (1991) 533-538
63. Knowles M.R., Robinson J.M., Wood R.E., Pue C.A., Mentz W.M., Wager G.C., Gatzy J.T., and Boucher R.C. Ion composition of airway surface liquid of patients with cystic fibrosis as compared with normal and disease-control subjects. J. Clin. Invest. 100 (1997) 2588-2595
64. Komlosi P., Fintha A., and Bell P.D. Renal cell-to-cell communication via extracellular ATP. Physiology (Bethesda) 20 (2005) 86-90
65. Kreda S.M., Okada S.F., van Heusden C.A., O'Neal W., Gabriel S., Abdullah L., Davis C.W., Boucher R.C., and Lazarowski E.R. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J. Physiol. 584 (2007) 245-259
66. Kunzelmann K., Bachhuber T., Regeer R., Markovich D., Sun J., and Schreiber R. Purinergic inhibition of the epithelial Na+ transport via hydrolysis of PIP2. FASEB J. 19 (2005) 142-143
67. Kunzelmann K., Konig J., Sun J., Markovich D., King N.J., Karupiah G., Young J.A., and Cook D.I. Acute effects of parainfluenza virus on epithelial electrolyte transport. J. Biol. Chem. 279 (2004) 48760-48766
68. Lambert R.K., Codd S.L., Alley M.R., and Pack R.J. Physical determinants of bronchial mucosal folding. J. Appl. Physiol. 77 (1994) 1206-1216
69. Langenderfer B. Alternatives to percussion and postural drainage. A review of mucus clearance therapies: percussion and postural drainage, autogenic drainage, positive expiratory pressure, flutter valve, intrapulmonary percussive ventilation, and high-frequency chest compression with the ThAIRapy Vest. J. Cardiopulm. Rehabil. 18 (1998) 283-289
70. 2+. Biophys. J. 77 (1999) 629-638
71. Lazarowski E.R., and Boucher R.C. UTP as an extracellular signaling molecule. News Physiol. Sci. 16 (2001) 1-5
72. Lazarowski E.R., Boucher R.C., and Harden T.K. Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations. J. Biol. Chem. 275 (2000) 31061-31068
73. Lazarowski E.R., Boucher R.C., and Harden T.K. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64 (2003) 785-795
74. Lazarowski E.R., Paradiso A.M., Watt W.C., Harden T.K., and Boucher R.C. UDP activates a mucosal-restricted receptor on human nasal epithelial cells that is distinct from the P2Y2 receptor. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 2599-2603
75. Lazarowski E.R., Tarran R., Grubb B.R., van Heusden C.A., Okada S., and Boucher R.C. Nucleotide release provides a mechanism for airway surface liquid homeostasis. J. Biol. Chem. 279 (2004) 36855-36864
76. Leith D.E. The development of cough. Am. Rev. Respir Dis. 131 (1985) S39-S42
77. Lethem M.I., Dowell M.L., Van Scott M., Yankaskas J.R., Egan T., Boucher R.C., and Davis C.W. Nucleotide regulation of goblet cells in human airway epithelial explants: normal exocytosis in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 9 (1993) 315-322
78. Levitzky M.G. Pulmonary Physiology (1991), McGraw-Hill, Inc., New York, NY
79. Liu M., Tanswell A.K., and Post M. Mechanical force-induced signal transduction in lung cells. Am. J. Physiol. 277 (1999) L667-683
80. Mall M., Wissner A., Gonska T., Calenborn D., Kuehr J., Brandis M., and Kunzelmann K. Inhibition of amiloride-sensitive epithelial Na(+) absorption by extracellular nucleotides in human normal and cystic fibrosis airways. Am. J. Respir. Cell Mol. Biol. 23 (2000) 755-761
81. Marks J.H. Airway clearance devices in cystic fibrosis. Paediatr. Respir. Rev. 8 (2007) 17-23
82. Mason S.J., Paradiso A.M., and Boucher R.C. Regulation of transepithelial ion transport and intracellular calcium by extracellular ATP in human normal and cystic fibrosis airway epithelium. Br. J. Pharmacol. 103 (1991) 1649-1656
83. Matsui H., Davis C.W., Tarran R., and Boucher R.C. Osmotic water permeabilities of cultured, well-differentiated normal and cystic fibrosis airway epithelia. J. Clin. Invest. 105 (2000) 1419-1427
84. Matsui H., Randell S.H., Peretti S.W., Davis C.W., and Boucher R.C. Coordinated clearance of periciliary liquid and mucus from airway surfaces. J. Clin. Invest. 102 (1998) 1125-1131
85. Matsui H., Wagner V.E., Hill D.B., Schwab U.E., Rogers T.D., Button B., Taylor II R.M., Superfine R., Rubinstein M., Iglewski B.H., and Boucher R.C. A physical linkage between cystic fibrosis airway surface dehydration and Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 18131-18136
86. Mitchell C.H., Carre D.A., McGlinn A.M., Stone R.A., and Civan M.M. A release mechanism for stored ATP in ocular ciliary epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 7174-7178
87. Moessinger A.C., Harding R., Adamson T.M., Singh M., and Kiu G.T. Role of lung fluid volume in growth and maturation of the fetal sheep lung. J. Clin. Invest. 86 (1990) 1270-1277
88. Moorcroft A.J., Dodd M.E., and Webb A.K. Exercise limitations and training for patients with cystic fibrosis. Disabil. Rehabil. 20 (1998) 247-253
89. Morse D.M., Smullen J.L., and Davis C.W. Differential effects of UTP, ATP, and adenosine on ciliary activity of human nasal epithelial cells. Am. J. Physiol. Cell Physiol. 280 (2001) C1485-C1497
90. North R.A., and Verkhratsky A. Purinergic transmission in the central nervous system. Pflugers Arch. 452 (2006) 479-485
91. Okada S.F., Nicholas R.A., Kreda S.M., Lazarowski E.R., and Boucher R.C. Physiological regulation of ATP release at the apical surface of human airway epithelia. J. Biol. Chem. 281 (2006) 22992-23002
92. Okada S.F., O'Neal W.K., Huang P., Nicholas R.A., Ostrowski L.E., Craigen W.J., Lazarowski E.R., and Boucher R.C. Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells. J. Gen. Physiol. 124 (2004) 513-526
93. Paradiso A.M., Ribeiro C.M., and Boucher R.C. Polarized signaling via purinoceptors in normal and cystic fibrosis airway epithelia. J. Gen. Physiol. 117 (2001) 53-67
94. Pasyk E.A., and Foskett J.K. Cystic fibrosis transmembrane conductance regulator-associated ATP and adenosine 3′-phosphate 5′-phosphosulfate channels in endoplasmic reticulum and plasma membranes. J. Biol. Chem. 272 (1997) 7746-7751
95. Pelleg A., Katchanov G., and Xu J. Purinergic modulation of neural control of cardiac function. J. Auton. Pharmacol. 16 (1996) 401-405
96. Picher M., and Boucher R.C. Biochemical evidence for an ecto alkaline phosphodiesterase I in human airways. Am. J. Respir. Cell Mol. Biol. 23 (2000) 255-261
97. Picher M., Burch L.H., Hirsh A.J., Spychala J., and Boucher R.C. Ecto 5′-nucleotidase and nonspecific alkaline phosphatase. Two AMP-hydrolyzing ectoenzymes with distinct roles in human airways. J. Biol. Chem. 278 (2003) 13468-13479
98. Praetorius H.A., and Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 184 (2001) 71-79
99. Praetorius H.A., and Spring K.R. The renal cell primary cilium functions as a flow sensor. Curr. Opin. Nephrol. Hypertens. 12 (2003) 517-520
100. Prasad S.A., and Cerny F.J. Factors that influence adherence to exercise and their effectiveness: application to cystic fibrosis. Pediatr. Pulmonol. 34 (2002) 66-72
101. Pryor J.A. Physiotherapy for airway clearance in adults. Eur. Respir. J. 14 (1999) 1418-1424
102. Puchelle E., de Bentzmann S., and Zahm J.M. Physical and functional properties of airway secretions in cystic fibrosis-therapeutic approaches. Respiration 62 Suppl. 1 (1995) 2-12
103. Randell S.H., and Boucher R.C. Effective mucus clearance is essential for respiratory health. Am. J. Respir. Cell Mol. Biol. 35 (2006) 20-28
104. Reddy M.M., Quinton P.M., Haws C., Wine J.J., Grygorczyk R., Tabcharani J.A., Hanrahan J.W., Gunderson K.L., and Kopito R.R. Failure of the cystic fibrosis transmembrane conductance regulator to conduct ATP. Science 271 (1996) 1876-1879
105. Reisin I.L., Prat A.G., Abraham E.H., Amara J.F., Gregory R.J., Ausiello D.A., and Cantiello H.F. The cystic fibrosis transmembrane conductance regulator is a dual ATP and chloride channel. J. Biol. Chem. 269 (1994) 20584-20591
106. Ressler B., Lee R.T., Randell S.H., Drazen J.M., and Kamm R.D. Molecular responses of rat tracheal epithelial cells to transmembrane pressure. Am. J. Physiol. Lung Cell Mol. Physiol. 278 (2000) L1264-1272
107. Rich P.B., Douillet C.D., Mahler S.A., Husain S.A., and Boucher R.C. Adenosine triphosphate is released during injurious mechanical ventilation and contributes to lung edema. J. Trauma 55 (2003) 290-297
108. Rubin B.K. Physiology of airway mucus clearance. Respir. Care 47 (2002) 761-768
109. Rubin E.M., Scantlen G.E., Chapman G.A., Eldridge M., Menendez R., and Wanner A. Effect of chest wall oscillation on mucus clearance: comparison of two vibrators. Pediatr. Pulmonol. 6 (1989) 122-126
110. Sackin H. Stretch-activated ion channels. Kidney Int. 48 (1995) 1134-1147
111. Salathe M., Lieb T., and Bookman R.J. Lack of nitric oxide involvement in cholinergic modulation of ovine ciliary beat frequency. J. Aerosol. Med. 13 (2000) 219-229
112. Satir P., and Sleigh M.A. The physiology of cilia and mucociliary interactions. Annu. Rev. Physiol. 52 (1990) 137-155
113. Schneider S.W., Egan M.E., Jena B.P., Guggino W.B., Oberleithner H., and Geibel J.P. Continuous detection of extracellular ATP on living cells by using atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 12180-12185
114. Schneiderman-Walker J., Pollock S.L., Corey M., Wilkes D.D., Canny G.J., Pedder L., and Reisman J.J. A randomized controlled trial of a 3-year home exercise program in cystic fibrosis. J. Pediatr. 136 (2000) 304-310
115. Schumacker P.T. Straining to understand mechanotransduction in the lung. Am. J. Physiol. Lung Cell Mol. Physiol. 282 (2002) L881-882
116. Schwiebert E.M. ABC transporter-facilitated ATP conductive transport. Am. J. Physiol. 276 (1999) C1-8
117. Schwiebert E.M. ATP release mechanisms, ATP receptors and purinergic signalling along the nephron. Clin. Exp. Pharmacol. Physiol. 28 (2001) 340-350
118. Schwiebert E.M., Egan M.E., Hwang T.H., Fulmer S.B., Allen S.S., Cutting G.R., and Guggino W.B. CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP. Cell 81 (1995) 1063-1073
119. Schwiebert E.M., and Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 1615 (2003) 7-32
120. Spring K.R. Epithelial fluid transport-a century of investigation. News Physiol. Sci. 14 (1999) 92-98
121. Strange K., Emma F., and Jackson P.S. Cellular and molecular physiology of volume-sensitive anion channels. Am. J. Physiol. 270 (1996) C711-730
122. Stutts M.J., Canessa C.M., Olsen J.C., Hamrick M., Cohn J.A., Rossier B.C., and Boucher R.C. CFTR as a cAMP-dependent regulator of sodium channels. Science 269 (1995) 847-850
123. Sugita M., Yue Y., and Foskett J.K. CFTR Cl- channel and CFTR-associated ATP channel: distinct pores regulated by common gates. EMBO J. 17 (1998) 898-908
124. Tarran R., Button B., Picher M., Paradiso A.M., Ribeiro C.M., Lazarowski E.R., Zhang L., Collins P.L., Pickles R.J., Fredberg J.J., and Boucher R.C. Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J. Biol. Chem. 280 (2005) 35751-35759
125. Tarran R., Grubb B.R., Gatzy J.T., Davis C.W., and Boucher R.C. 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 (2001) 223-236
126. Tarran R., Trout L., Donaldson S.H., and Boucher R.C. Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J. Gen. Physiol. 127 (2006) 591-604
127. Thi M.M., Tarbell J.M., Weinbaum S., and Spray D.C. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a "bumper-car" model. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 16483-16488
128. Thiagarajah J.R., Song Y., Haggie P.M., and Verkman A.S. A small molecule CFTR inhibitor produces cystic fibrosis-like submucosal gland fluid secretions in normal airways. FASEB J. 18 (2004) 875-877
129. Thornton D.J., and Sheehan J.K. From mucins to mucus: toward a more coherent understanding of this essential barrier. Proc. Am. Thorac. Soc. 1 (2004) 54-61
130. Tomkiewicz R.P., Biviji A., and King M. Effects of oscillating air flow on the rheological properties and clearability of mucous gel simulants. Biorheology 31 (1994) 511-520
131. Tschumperlin D.J., and Drazen J.M. Chronic effects of mechanical force on airways. Annu. Rev. Physiol. 68 (2006) 563-583
132. Tschumperlin D.J., Oswari J., and Margulies A.S. Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am. J. Respir. Crit. Care Med. 162 (2000) 357-362
133. Tschumperlin D.J., Shively J.D., Swartz M.A., Silverman E.S., Haley K.J., Raab G., and Drazen J.M. Bronchial epithelial compression regulates MAP kinase signaling and HB-EGF-like growth factor expression. Am. J. Physiol. Lung Cell Mol. Physiol. 282 (2002) L904-911
134. Tzima E., Del Pozo M.A., Kiosses W.B., Mohamed S.A., Li S., Chien S., and Schwartz M.A. Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J. 21 (2002) 6791-6800
135. Voynow J.A. What does mucin have to do with lung disease?. Paediatr. Respir. Rev. 3 (2002) 98-103
136. Wanner A., Salathe M., and O'Riordan T.G. Mucociliary clearance in the airways. Am. J. Respir. Crit. Care Med. 154 (1996) 1868-1902
137. Watt W.C., Lazarowski E.R., and Boucher R.C. Cystic fibrosis transmembrane regulator-independent release of ATP. Its implications for the regulation of P2Y2 receptors in airway epithelia. J. Biol. Chem. 273 (1998) 14053-14058
138. Wiggs B.R., Hrousis C.A., Drazen J.M., and Kamm R.D. On the mechanism of mucosal folding in normal and asthmatic airways. J. Appl. Physiol. 83 (1997) 1814-1821
139. 2+, purinergic signaling, tonicity, and viscosity. Am. J. Physiol. Lung Cell Mol. Physiol. 292 (2007) L614-624
140. Winters S.L., and Yeates D.B. Roles of hydration, sodium, and chloride in regulation of canine mucociliary transport system. J. Appl. Physiol. 83 (1997) 1360-1369
141. Yamamoto K., Sokabe T., Matsumoto T., Yoshimura K., Shibata M., Ohura N., Fukuda T., Sato T., Sekine K., Kato S., Isshiki M., Fujita T., Kobayashi M., Kawamura K., Masuda H., Kamiya A., and Ando J. Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice. Nat. Med. 12 (2006) 133-137
142. Yoshitsugu M., Rautiainen M., Matsune S., Nuutinen J., and Ohyama M. Effect of exogenous ATP on ciliary beat of human ciliated cells studied with differential interference microscope equipped with high speed video. Acta Otolaryngol. 113 (1993) 655-659
143. Yue G., Malik B., Yue G., and Eaton D.C. Phosphatidylinositol 4,5-bisphosphate (PIP2) stimulates epithelial sodium channel activity in A6 cells. J. Biol. Chem. 277 (2002) 11965-11969
144. Zhang L., and Sanderson M.J. Oscillations in ciliary beat frequency and intracellular calcium concentration in rabbit tracheal epithelial cells induced by ATP. J. Physiol. 546 (2003) 733-749
145. Zimmermann H. Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch. Pharmacol. 362 (2000) 299-309