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1 Medicine, University of Pittsburgh, Pittsburgh, PA, USA; Mount Desert Island Biological Laboratory, Salisbury Cove, ME, USA
2 Medicine, University of Pittsburgh, Pittsburgh, PA, USA
3 Mount Desert Island Biological Laboratory, Salisbury Cove, ME, USA
4 MPI fur molekulare Physiologie, Dortmund, Germany; Mount Desert Island Biological Laboratory, Salisbury Cove, ME, USA
* To whom correspondence should be addressed. E-mail: zeidel{at}msx.dept-med.pitt.edu.
Barrier apical membranes prevent osmotic and chemical equilibration between compartments separated by epithelia. Teleosts and elasmobranchs are faced with considerable osmotic challenges living in sea water and both use compensatory mechanisms to survive the loss of tissue water (teleosts) and tissue urea (elasmobranchs) across exposed epithelial surfaces. We hypothesized that the gill which has a high surface area for gas exchange must have an apical membrane of exceptionally low permeability to prevent equilibration between seawater and the plasma of fish species. We isolated apical membrane vesicles from the gills of Pleuronectus americanus (winter flounder) and Squalus acanthias (dogfish shark) and demonstrated approximately 6-fold enrichment of the apical marker, ADPase compared to homogenate. We also isolated basolateral membranes from shark gill epithelium (enriched 2.3-fold for Na,K-ATPase compared to homogenate) and using stopped-flow fluorometry measured the membrane permeabilities to water, urea and NH3. Apical membrane water permeabilities were similar between species and quite low (7.4 ± 0.7 x 10-4 cm/s and 6.6 ± 0.8 x 10-4 cm/s for shark and flounder respectively), while shark basolateral membranes showed 2-fold higher water permeability (14 ± 2 x 10-4 cm/s). Permeabilities to urea and NH3 were also low in apical membranes. Due to the much lower apical surface area compared to basolateral membrane surface area we conclude that the apical membrane represents an effective barrier to water and urea. However, the values we obtained were not low enough to account for low water loss (in teleost) and urea loss (in elasmobranch) measured in vivo by others. We conclude that in addition to the low permeability of the lipid bilayer there are other mechanisms utilized by both species to permit gill epithelia to serve as effective barriers to equilibration between seawater and plasma. This conclusion has important implications for the function of other barrier epithelia, such as the gastric mucosa, mammalian bladder, and renal thick ascending limb of Henle.
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