Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1999 Feb;76(2):869–877. doi: 10.1016/S0006-3495(99)77250-4

Bidirectional transepithelial water transport: measurement and governing mechanisms.

J E Phillips 1, L B Wong 1, D B Yeates 1
PMCID: PMC1300088  PMID: 9929488

Abstract

In the search for the mechanisms whereby water is transported across biological membranes, we hypothesized that in the airways, the hydration of the periciliary fluid layer is regulated by luminal-to-basolateral water transport coupled to active transepithelial sodium transport. The luminal-to-basolateral (JWL-->B) and the basolateral-to-luminal (JWB-->L) transepithelial water fluxes across ovine tracheal epithelia were measured simultaneously. The JWL-->B (6.1 microliter/min/cm2) was larger than JWB-->L (4.5 microliter/min/cm2, p < 0.05, n = 30). The corresponding water diffusional permeabilities were PdL-->B = 1.0 x 10(-4) cm/s and PdB-->L = 7.5 x 10(-5) cm/s. The activation energy (Ea) of JWL-->B (11.6 kcal/mol) was larger than the Ea of JWB-->L (6.5 kcal/mol, p < 0.05, n = 5). Acetylstrophanthidin (100 microM basolateral) reduced JWL-->B from 6.1 to 4.4 microliter/min/cm2 (p < 0. 05, n = 5) and abolished the PD. Amiloride (10 microM luminal) reduced JWL-->B from 5.7 to 3.7 microliter/min/cm2 (p < 0.05, n = 5) and reduced PD by 44%. Neither of these agents significantly changed JWB-->L. These data indicate that in tracheal epithelia under homeostatic conditions, JWB-->L was dominated by diffusion (Ea = 4.6 kcal/mol), whereas approximately 30% of JWL-->B was coupled to the active Na+,K+-ATPase pump (Ea = 27 kcal/mol).

Full Text

The Full Text of this article is available as a PDF (251.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Al-Bazzaz F. J., Al-Awqati Q. Interaction between sodium and chloride transport in canine tracheal mucosa. J Appl Physiol Respir Environ Exerc Physiol. 1979 Jan;46(1):111–119. doi: 10.1152/jappl.1979.46.1.111. [DOI] [PubMed] [Google Scholar]
  2. Apell H. J., Marcus M. M., Anner B. M., Oetliker H., Läuger P. Optical study of active ion transport in lipid vesicles containing reconstituted Na,K-ATPase. J Membr Biol. 1985;85(1):49–63. doi: 10.1007/BF01872005. [DOI] [PubMed] [Google Scholar]
  3. Brink P. R. Effect of deuterium oxide on junctional membrane channel permeability. J Membr Biol. 1983;71(1-2):79–87. doi: 10.1007/BF01870676. [DOI] [PubMed] [Google Scholar]
  4. Cotton C. U., Lawson E. E., Boucher R. C., Gatzy J. T. Bioelectric properties and ion transport of airways excised from adult and fetal sheep. J Appl Physiol Respir Environ Exerc Physiol. 1983 Nov;55(5):1542–1549. doi: 10.1152/jappl.1983.55.5.1542. [DOI] [PubMed] [Google Scholar]
  5. Diamond J. M. Channels in epithelial cell membranes and junctions. Fed Proc. 1978 Oct;37(12):2639–2643. [PubMed] [Google Scholar]
  6. Durand J., Durand-Arczynska W., Haab P. Volume flow, hydraulic conductivity and electrical properties across bovine tracheal epithelium in vitro: effect of histamine. Pflugers Arch. 1981 Nov;392(1):40–45. doi: 10.1007/BF00584580. [DOI] [PubMed] [Google Scholar]
  7. Folkesson H. G., Matthay M. A., Frigeri A., Verkman A. S. Transepithelial water permeability in microperfused distal airways. Evidence for channel-mediated water transport. J Clin Invest. 1996 Feb 1;97(3):664–671. doi: 10.1172/JCI118463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frömter E., Diamond J. Route of passive ion permeation in epithelia. Nat New Biol. 1972 Jan 5;235(53):9–13. doi: 10.1038/newbio235009a0. [DOI] [PubMed] [Google Scholar]
  9. Hays R. M., Franki N., Soberman R. Activation energy for water diffusion across the toad bladder: evidence against the pore enlargement hypothesis. J Clin Invest. 1971 May;50(5):1016–1018. doi: 10.1172/JCI106572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jiang C., Finkbeiner W. E., Widdicombe J. H., McCray P. B., Jr, Miller S. S. Altered fluid transport across airway epithelium in cystic fibrosis. Science. 1993 Oct 15;262(5132):424–427. doi: 10.1126/science.8211164. [DOI] [PubMed] [Google Scholar]
  11. Kuwahara M., Verkman A. S. Direct fluorescence measurement of diffusional water permeability in the vasopressin-sensitive kidney collecting tubule. Biophys J. 1988 Oct;54(4):587–593. doi: 10.1016/S0006-3495(88)82993-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lawaczeck R. Water permeability through biological membranes by isotopic effects of fluorescence and light scattering. Biophys J. 1984 Mar;45(3):491–494. doi: 10.1016/S0006-3495(84)84184-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Loughlin G. M., Gerencser G. A., Crowder M. A., Boyd R. L., Mangos J. A. Fluid fluxes in the ferret trachea. Experientia. 1982 Dec 15;38(12):1451–1452. doi: 10.1007/BF01955764. [DOI] [PubMed] [Google Scholar]
  14. Matthay M. A., Folkesson H. G., Verkman A. S. Salt and water transport across alveolar and distal airway epithelia in the adult lung. Am J Physiol. 1996 Apr;270(4 Pt 1):L487–L503. doi: 10.1152/ajplung.1996.270.4.L487. [DOI] [PubMed] [Google Scholar]
  15. Olver R. E., Strang L. B. Ion fluxes across the pulmonary epithelium and the secretion of lung liquid in the foetal lamb. J Physiol. 1974 Sep;241(2):327–357. doi: 10.1113/jphysiol.1974.sp010659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Phipps R. J., Abraham W. M., Mariassy A. T., Torrealba P. J., Sielczak M. W., Ahmed A., McCray M., Stevenson J. S., Wanner A. Developmental changes in the tracheal mucociliary system in neonatal sheep. J Appl Physiol (1985) 1989 Aug;67(2):824–832. doi: 10.1152/jappl.1989.67.2.824. [DOI] [PubMed] [Google Scholar]
  17. Phipps R. J., Denas S. M., Sielczak M. W., Wanner A. Effects of 0.5 ppm ozone on glycoprotein secretion, ion and water fluxes in sheep trachea. J Appl Physiol (1985) 1986 Mar;60(3):918–927. doi: 10.1152/jappl.1986.60.3.918. [DOI] [PubMed] [Google Scholar]
  18. Phipps R. J., Torrealba P. J., Lauredo I. T., Denas S. M., Sielczak M. W., Ahmed A., Abraham W. M., Wanner A. Bacterial pneumonia stimulates macromolecule secretion and ion and water fluxes in sheep trachea. J Appl Physiol (1985) 1987 Jun;62(6):2388–2397. doi: 10.1152/jappl.1987.62.6.2388. [DOI] [PubMed] [Google Scholar]
  19. Price H. D., Thompson T. E. Properties of liquid bilayer membranes separating two aqueous phases: temperature dependence of water permeability. J Mol Biol. 1969 May 14;41(3):443–457. doi: 10.1016/0022-2836(69)90287-3. [DOI] [PubMed] [Google Scholar]
  20. Ruddy M. K., Drazen J. M., Pitkanen O. M., Rafii B., O'Brodovich H. M., Harris H. W. Modulation of aquaporin 4 and the amiloride-inhibitable sodium channel in perinatal rat lung epithelial cells. Am J Physiol. 1998 Jun;274(6 Pt 1):L1066–L1072. doi: 10.1152/ajplung.1998.274.6.L1066. [DOI] [PubMed] [Google Scholar]
  21. Smith J. J., Welsh M. J. cAMP stimulates bicarbonate secretion across normal, but not cystic fibrosis airway epithelia. J Clin Invest. 1992 Apr;89(4):1148–1153. doi: 10.1172/JCI115696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Welsh M. J., Widdicombe J. H., Nadel J. A. Fluid transport across the canine tracheal epithelium. J Appl Physiol Respir Environ Exerc Physiol. 1980 Nov;49(5):905–909. doi: 10.1152/jappl.1980.49.5.905. [DOI] [PubMed] [Google Scholar]
  23. Winters S. L., Yeates D. B. Roles of hydration, sodium, and chloride in regulation of canine mucociliary transport system. J Appl Physiol (1985) 1997 Oct;83(4):1360–1369. doi: 10.1152/jappl.1997.83.4.1360. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES