Mechanisms of acid and base secretion by the airway epithelium

Journal of Membrane Biology

Volumn 211, Issue 3, 2006, Pages 139-150

  Fischer, Horst ^a   Widdicombe, Jonathan H ^b  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BICARBONATE; CARRIER PROTEIN; CHLORIDE CHANNEL; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; PROTON; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM PROTON EXCHANGE PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ACID BASE BALANCE; ACID SECRETION; ACIDITY; AIRWAY; AIRWAY SURFACE LIQUID; ANTIMICROBIAL ACTIVITY; APICAL MEMBRANE; CILIATED EPITHELIUM; COUGHING; CYSTIC FIBROSIS; HUMAN; INFECTION PREVENTION; ION TRANSPORT; MEMBRANE TRANSPORT; NONHUMAN; PH; PROTEIN FUNCTION; PROTON TRANSPORT; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT MUCOSA; REVIEW;

ACID-BASE EQUILIBRIUM; ACIDS; ANIMALS; BIOLOGICAL TRANSPORT; BRONCHOALVEOLAR LAVAGE FLUID; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; RESPIRATORY MUCOSA;

EID: 33751269096     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-006-0861-0     Document Type: Review

References (107)

1. + exchanger in isolated epithelial tracheal cells from sheep. Involvement in tracheal proton secretion. Exp. Physiol. 78:383-394
2. Adler, K., Wooten, O., Philippoff, W., Lerner, E., Dulfano, M. 1972. Physical properties of sputum. 3. Rheologic variability and intrinsic relationships. Am. Rev. Respir. Dis. 106:86-96
3. Alton, E.W.F.W., Currie, A.D., Logan-Sinclair, R., Warner, J.O., Hodson, M.E., Geddes, D.M. 1990. Nasal potential difference: a clinical test for cystic fibrosis. Eur. Resp. J. 3:922-926
4. + channel by extracellular acidification. Am. J. Physiol. 279:C1896-1905
5. + exchanger isoform 2 is the predominant NHE isoform in murine colonic crypts and its lack causes NHE3 upregulation. Am. J. Physiol. 287:G125-G133
6. Ballard S.T., Trout L., Garrison J., Inglis S.K. 2005. Ionic mechanism of forskolin-induced liquid secretion by porcine bronchi. Am. J. Physiol. 290:L97-L104
7. Boat, T.F., Cheng, P.W. 1980. Biochemistry of airway mucus secretions. Fed. Proc. 39:3067-74
8. Bodem, C., Lampton, L., Miller, D., Tarka, E., Everett, E. 1983. Endobronchial pH. Relevance of aminoglycoside activity in gram-negative bacillary pneumonia. Am. Rev. Respir. Dis. 127:39-41
9. Boers, J.E., Ambergen, A.W., Thunnissen, F.B.J.M. 1999. Number and proliferation of clara cells in normal human airway epithelium. Am. J. Respir. Crit. Care Med. 159:1585-1591
10. Boucher, R.C. 1999. Molecular insights into the physiology of the 'thin film' of airway surface liquid. J. Physiol. Lond. 516:631-638
11. Bowman, E.J., Siebers, A., Altendorf, K. 1988. Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976
12. Breuninger, H. 1964. Über das physikalisch-chemische Verhalten des Nasenschleims. Eur. Arch. Oto-Rhino-Laryng. 184:133-138
13. Byeon, M., Westerman, M., Maroulakou, I., Henderson, K., Suster, S., Zhang, X., Papas, T., Vesely, J., Willingham, M., Green, J., Schweinfest, C. 1996. The downregulated in adenoma (DRA) gene encodes an intestine-specific membrane glycoprotein. Oncogene 12:387-396
14. + channel. Am. J. Physiol. 276:C477-C486
15. Ciaccio, C., De Sanctis, G., Marini, S., Sinibaldi, F., Santucci, R., Arcovito, A., Bellelli, A., Ghibaudi, E., Ferrari Rosa, P., Coletta, M. 2004. Proton Linkage for CO Binding and Redox Properties of Bovine Lactoperoxidase. Biophys. J. 86:448-454
16. - secretion in human nasal epithelium: responses of apical and basolateral membranes. Am. J. Physiol. 263:C1190-C1199
17. Coakley, R.D., Grubb, B.R., Paradiso, A.M., Gatzy, J.T., Johnson, L.G., Kreda, S.M., O'Neal, W.K., Boucher, R.C. 2003. Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc. Natl. Acad. Sci. USA 100:16083-16088
18. Conner, G.E., Salathe, M., Forteza, R. 2002. Lactoperoxidase and Hydrogen Peroxide Metabolism in the Airway. Am. J. Respir. Crit. Care Med. 166:57S-61S
19. Cotton, C.U., Stutts, M.J., Knowles, M.R., Gatzy, J.T., Boucher, R.C. 1987. Abnormal apical cell membrane in cystic fibrosis respiratory epithelium. An in vitro electrophysiologic analysis. J. Clin. Invest. 79:80-85
20. DeCoursey, T., Cherny, V. 1995. Voltage-activated proton currents in membrane patches of rat alveolar epithelial cells. J. Physiol. 489:299-307
21. DeCoursey, T.E. 2003. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83:475-579
22. DeCoursey, T.E. 2004. During the Respiratory Burst, Do Phagocytes Need Proton Channels or Potassium Channels or Both? Sci. STKE 2004:pe21
23. +-activated ATPase activities in rat distal colon. Am. J. Physiol. 261:G1005-G1011
24. Devor, D.C., Bridges, R.J., Pilewski, J.M. 2000. Pharmacological modulation of ion transport across wild-type and ΔF508 CFTR-expressing human bronchial epithelia. Am. J. Physiol. 279:C461-C479
25. Devor, D.C., Singh, A.K., Lambert, L.C., DeLuca, A., Frizzell, R.A., Bridges, R.J. 1999. Bicarbonate and chloride secretion in Calu-3 human airway epithelial cells. J. Gen. Physiol. 113:743-760
26. DiPaola, M., Maxfield, F. 1984. Conformational changes in the receptors for epidermal growth factor and asialoglycoproteins induced by the mildly acidic pH found in endocytic vesicles. J. Biol. Chem. 259:9163-9171
27. Dubin, R.F., Robinson, S.K., Widdicombe, J.H. 2004. Secretion of lactoferrin and lysozyme by cultures of human airway epithelium. Am. J. Physiol. 286:L750-L755
28. - exchanger isoforms in proximal and distal human airways. Am. J. Physiol. 276:L971-L978
29. England, R., Homer, J., Knight, L., Ell, S. 1999. Nasal pH measurement: a reliable and repeatable parameter. Clin. Otolaryngol. Allied Sci. 24:67-68
30. Fabricant, N.D. 1941. Significance of the pH of nasal secretions in situ. Arch. Otolaryngology 34:150-163
31. Fischer, H., Widdicombe, J.H., Illek, B. 2002. Acid secretion and proton conductance in human airway epithelium. Am. J. Physiol. 282:C736-C743
32. +-ATPases. J. Biol. Chem. 274:12951-12954
33. Forteza, R., Salathe, M., Miot, F., Forteza, R., Conner, G.E. 2005. Regulated hydrogen peroxide production by duox in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 32:462-469
34. Ganz, T. 2002. Antimicrobial polypeptides in host defense of the respiratory tract. J. Clin. Invest. 109:693-697
35. Gatto, L. 1981. pH of mucus in rat trachea. J. Appl. Physiol. 50:1224-1226
36. Gatto, L. 1985. pH of mucus in rabbit trachea: cholinergic stimulation and block. Lung 163:109-115
37. Geiszt, M., Witta, J., Baffi, J., Lekstrom, K., Leto, T.L. 2003. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 17:1502-1504
38. +-ATPase in the human eccrine sweat duct: immunolocalization and functional demonstration. Am. J. Physiol. 282:C1454-C1460
39. Gray, M.A., Pollard, C.E., Harris, A., Coleman, L., Greenwell, J.R., Argent, B.E. 1990. Anion selectivity and block of the small-conductance chloride channel on pancreatic duct cells. Am. J. Physiol 259:C752-C761
40. Greeley, T., Shumaker, H., Wang, Z., Schweinfest, C.W., Soleimani, M. 2001. Downregulated in adenoma and putative anion transporter are regulated by CFTR in cultured pancreatic duct cells. Am. J. Physiol. 281:G1301-G1308
41. Guerrin, F., Voisin, C., Macquet, V., Robin, H., Lequien, P. 1971. Apport de la pH metrie bronchique in situ. Progr. Respir. Res 6:372-383
42. Guerrin F., Voisin C., Macquet V., Robin H., Wattel F., Boulanger J. 1969. Possibilities de la pH metrie bronchique in situ. In: Hypersecretion Bronchique. pp. 249-256. Clinchy, Poinsot
43. Harkema J.R., Mariassy A., St. George J.A., Hyde D., Plopper C.G. 1991. Epithelial cells of the conducting airways. A species comparison. In: The Airway Epithelium: Physiology, Pathology, and Pharmacology. S.G. Farmer, D.W.P. Hay, editors. Marcel Dekker, Inc, New York. pp. 3-39
44. Harper, R.W., Xu, C., Eiserich, J., Chen, Y., Kao, C.-Y., Thai, P., Setiadi, H., Wu, R. 2005. Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett. 579:4911-4917
45. Hehar, S., Mason, J., Stephen, A., Washington, N., Jones, N., Jackson, S., Bush, D. 1999. Twenty-four hour ambulatory nasal pH monitoring. Clin. Otolaryngol. Allied Sci. 24:24-25
46. Hilding, A. 1930. The common cold. Arch. Otolaryng. 12:133
47. Hoglund, P., Haila, S., Socha, J., Tomaszewski, L., Saarialho-Kere, U., Karjalainen-Lindsberg, M., Airola, K., Holmberg, C., de la Chapelle, A., Kere, J. 1996. Mutations of the Down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat. Genet. 14:316-139
48. Holma, B. 1985. Influence of buffer capacity and pH-dependent rheological properties of respiratory mucus on health effects due to acidic pollution. Sci. Total Environ. 41:101-123
49. Holma, B., Hegg, P.O. 1989. pH and protein-dependent buffer capacity and viscosity of respiratory mucus: their interrelationships and influence on health. Sci. Total Environ. 84:71-82
50. Illek, B., W.-K.Tam, A., Fischer, H., Machen, T.E. 1999. Anion selectivity of apical membrane conductance of Calu 3 human airway epithelia. Pfluegers Arch. 437:812-822
51. - conductance through CFTR in human airway epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 272:L752-L761
52. Inglis, S.K., Finlay, L., Ramminger, S.J., Richard, K., Ward, M.R., Wilson, S.M., Olver, R.E. 2002. Regulation of intracellular pH in Calu-3 human airway cells. J. Physiol. 538:527-539
53. Inglis, S.K., Wilson, S.M., Olver, R.E. 2003. Secretion of acid and base equivalents by intact distal airways. Am. J. Physiol. 284:L855-L862
54. Ireson, N.J., Tait, J.S., MacGregor, G.A., Baker, E.H. 2001. Comparison of nasal pH values in black and white individuals with normal and high blood pressure. Clin. Sci. 100:327-333
55. Jankowski, A., Grinstein, S. 2002. Modulation of the cytosolic and phagosomal pH by the NADPH oxidase. Antioxid. Redox Signal. 4:61-68
56. Jayaraman, S., Song, Y., Verkman, A.S. 2001. Airway surface liquid osmolality measured using fluorophore-encapsulated liposomes. J. Gen. Physiol. 117:423-430
57. Jayaraman, S., Song, Y., Verkman, A.S. 2001. Airway surface liquid pH in welldifferentiated airway epithelial cell cultures and mouse trachea. Am. J. Physiol. 281:C1504-C1511
58. Jayaraman, S., Song, Y., Vetrivel, L., Shankar, L., Verkman, A.S. 2001. Noninvasive in vivo fluorescence measurement of airway-surface liquid depth, salt concentration, and pH. J. Clin. Invest. 107:317-324
59. Knowles, M.R., Buntin, W.H., Bromberg, P.A., Gatzy, J.T., Boucher, R.C. 1982. Measurements of transepithelial electric potential differences in the trachea and bronchi of human subjects in vivo. Am. Rev. Respir. Dis. 126:108-112
60. Kondo, M., Finkbeiner, W.E., Widdicombe, J.H. 1992. Cultures of bovine tracheal epithelium with differentiated ultrastructure and ion transport. In Vitro Cell. Dev. Biol. 29A:19-24
61. Kreda, S.M., Mall, M., Mengos, A., Rochelle, L., Yankaskas, J., Riordan, J.R., Boucher, R.C. 2005. Characterization of wild-type and DF508 cystic fibrosis transmembrane regulator in human respiratory epithelia. Mol. Biol. Cell 16:2154-2167
62. Krouse, M.E., Talbott, J.F., Lee, M.M., Joo, N.S., Wine, J.J. 2004. Acid and base secretion in the Calu-3 model of human serous cells. Am. J. Physiol. 287:L1274-L1283
63. Kyle, H., Ward, J.P., Widdicombe, J.G. 1990. Control of pH of airway surface liquid of the ferret trachea in vitro. J. Appl. Physiol. 68:135-140
64. Lee, M.C., Penland, C.M., Widdicombe, J.H., Wine, J.J. 1998. Evidence that Calu-3 human airway cells secrete bicarbonate. Am. J. Physiol. 274:L450-L453
65. Linsdell, P., Tabcharani, J.A., Rommens, J.M., Hou, Y.X., Chang, X.B., Tsui, L.C., Riordan, J.R., Hanrahan, J.W. 1997. Permeability of wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride channels to polyatomic anions. J. Gen. Physiol. 110:355-364
66. Loffing, J., Moyer, B.D., Reynolds, D., Shmukler, B.E., Alper, S.L., Stanton, B.A. 2000. Functional and molecular characterization of an anion exchanger in airway serous epithelial cells. Am. J. Physiol. 279:C1016-C1023
67. Lucas, A., Douglas, L. 1934. Principles underlying ciliary activity in the respiratory tract. II. A comparison of nasal clearance in man, monkey and other mammals. Arch. Otolaryngol. 20:518-541
68. McShane, D., Davies, J.C., Davies, M.G., Bush, A., Geddes, D.M., Alton, E.W.F.W. 2003. Airway surface pH in subjects with cystic fibrosis. Eur. Respir. J. 21:37-42
69. + exchanger. J. Biol. Chem. 274:22855-22861
70. Metheny, N., Stewart, B., Smith, L., Yan, H., Diebold, M., Clouse, R. 1999. pH and concentration of bilirubin in feeding tube aspirates as predictors of tube placement. Nurs. Res. 48:189-197
71. Mittermaier, R. 1930. Untersuchungen über die Wasserstof- fionenkonzentration an Sekreten und Schleimhäuten, im besonderen bei chronischen Nebenhöhlenerkrankungen. Eur. Arch. Oto-Rhino-Laryngol. 127:149-172
72. Murphy, R., Cherny, V.V., Morgan, D., DeCoursey, T.E. 2005. Voltage-gated proton channels help regulate pHi in rat alveolar epithelium. Am. J. Physiol. 288:L398-L408
73. Palmer, L., Merrill, W., Niederman, M., Ferranti, R., Reynolds, H. 1986. Bacterial adherence to respiratory tract cells. Relationships between in vivo and in vitro pH and bacterial attachment. Am. Rev. Respir. Dis. 133:784-788
74. + exchange in human normal and cystic fibrotic ciliated airway epithelium. Am. J. Physiol. 262:L757-L764
75. + exchange in human normal and cystic fibrosis airway epithelium. Am. J. Physiol. 273:L148-L158
76. Paradiso, A.M., Boucher, R.C 2003. Normal and cystic fibrosis human bronchial epithelial cells exhibit negligible proton conductance across their apical membranes (Abstract). Ped. Pulmonol. Suppl. 25:233
77. - transport in human normal and cystic fibrosis nasal epithelia. J. Physiol. 548:203-218
78. Plopper C.G., Hyde D.M., Buckpitt A.R. 1997. Clara cells. In: The Lung: Scientific Foundations. R.G. Crystal, J.B. West, E.R. Weibel, P.J. Barnes, editors Lippincott-Raven, Philadelphia pp. 517-534
79. Poulsen, J.H., Fischer, H., Illek, B., Machen, T.E. 1994. Bicarbonate conductance and pH regulatory capability of cystic fibrosis transmembrane conductance regulator. Proc. Natl. Acad. Sci. USA 91:5340-4
80. -dependent pHi regulation in tracheal epithelial cells. Pfluegers Arch. 432:546-554
81. -. Nat. Med. 7:292-293
82. Reddy, M.M., Kopito, R.R., Quinton, P.M. 1998. Cytosolic pH regulates GCl through control of phosphorylation states of CFTR. Am. J. Physiol. 275:C1040-C1047
83. Ricciardolo, F.L.M., Gaston, B., Hunt, J. 2004. Acid stress in the pathology of asthma. J. Allergy Clin. Immunol. 113:610-619
84. Rogers, A.V., Dewar, A., Corrin, B., Jeffery, P.K. 1993. Identification of serous-like cells in the surface epithelium of human bronchioles. Eur. Respir. J. 6:498-504
85. Rose, M.C. 1992. Mucins: structure, function, and role in pulmonary diseases. Am. J. Physiol. 263:L413-L429
86. Schwarzer, C., Machen, T.E., Illek, B., Fischer, H. 2004. NADPH oxidase-dependent acid production in airway epithelial cells. J. Biol. Chem. 279:36454-36461
87. - secretion. Am. J. Physiol. 266:L493-L501
88. Sleigh, M.A., Blake, J.R., Liron, N. 1988. The propulsion of mucus by cilia. Am. Rev. Respir. Dis. 137:726-741
89. Smith, J.J., Welsh, M.J. 1992. cAMP stimulates bicarbonate secretion across normal, but not cystic fibrosis airway epithelia. J. Clin. Invest. 89:1148-1153
90. - - how does the pancreas do it? Clues from computer modelling of the duct cell. J. Pancreas (Online) 2:198-202
91. Song Y., Salinas D., Nielson D.W., Verkman A.S. 2006. Hyperacidity of secreted fluid from submucosal glands in early cystic fibrosis. Am. J. Physiol. 290:C741-C749
92. Song, Y., Thiagarajah, J., Verkman, A.S. 2003. Sodium and Chloride Concentrations, pH, and Depth of Airway Surface Liquid in Distal Airways. J. Gen. Physiol. 122:511-519
93. Steinmann, E. 1956. La secretion bronchique et le pH. Bronches 6:126-129
94. Tamada, T., Hug, M.J., Frizzell, R.A., Bridges, R.J. 2001. Microelectrode and impedance analysis of anion secretion in Calu-3 cells. J. Pancreas (Online) 2:219-228
95. Tandler, B. 1962. Ultrastructure of the human submaxillary gland. I. Architecture and histological relationships of the secretory cells. Am. J. Anat. 111:287-307
96. Tarran, R., Grubb, B.R., Gatzy, J.T., Davis, C.W., Boucher, R.C. 2001. The relative roles of passive surface forces and active ion transport in the modulation of airway surface liquid volume and composition. J. Gen. Physiol. 118:223-236
97. Thomas, R.C., Meech, R.W. 1982. Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones. Nature 299:826-828
98. - exchanger in the small intestine. Am. J. Physiol. 282:G573-G579
99. Wanner, A., Salathe, M., ORiordan, T.G. 1996. Mucociliary clearance in the airways. Am. J. Respir. Crit. Care Med. 154:1868-1902
100. Weibel, E.R. 1963. Morphometry of the Human Lung. Heidelberg, Springer-Verlag
101. - exchange activity in tracheal epithelial cells. Am. J. Physiol. 279:C62-C71
102. Widdicombe, J.G. 1995. Relationships among the composition of mucus, epithelial lining liquid, and adhesion of microorganisms. Am. J. Respir. Crit. Care Med. 151:2088-2092
103. Widdicombe, J.H., Bastacky, S.J., Wu, D.X., Lee, C.Y. 1997. Regulation of depth and composition of airway surface liquid. Eur. Respir. J. 10:2892-2897
104. Widdicombe, J.H., Widdicombe, J.G. 1995. Regulation of human airway surface liquid. Respir Physiol 99:3-12
105. Willumsen, N.J., Boucher, R.C. 1992. Intracellular pH and its relationship to regulation of ion transport in normal and cystic fibrosis human nasal epithelia. J. Physiol. 455:247-269
106. - pathways in cultured human airway epithelium. Am. J. Physiol. 256:C1033-C1044
107. Zippel, R., Meyer, P., Schubel, F. 1965. Eine Methode zur Messung der Wasserstoffionenkonzentration und ihre Ergebnisse an Schleimhautoberflächen in Nase und Mundrachen. Eur. Arch. Oto-Rhino-Laryng. 186:115-127