Highly water-permeable type I alveolar epithelial cells confer high water permeability between the airspace and vasculature in rat lung

Water permeability measured between the airspace and vasculature in intact sheep and mouse lungs is high. More than 95% of the internal surface area of the lung is lined by alveolar epithelial type I cells. The purpose of this study was to test whether osmotic water permeability (P(f)) in type I alveolar epithelial cells is high enough to account for the high P(f) of the intact lung. P(f) measured between the airspace and vasculature in the perfused fluid-filled rat lung by the pleural surface fluorescence method was high (0.019 ± 0.004 cm/s at 12°C) and weakly temperature-dependent (activation energy 3.7 kcal/mol). To resolve the contributions of type I and type II alveolar epithelial cells to lung water permeability, P(f) was measured by stopped-flow light scattering in suspensions of purified type I or type II cells obtained by immunoaffinity procedures. In response to a sudden change in external solution osmolality from 300 to 600 mOsm, the volume of type I cells decreased rapidly with a half-time (t(1/2)) of 60–80 ms at 10°C, giving a plasma membrane P(f) of 0.06–0.08 cm/s. P(f) in type I cells was independent of osmotic gradient size and was weakly temperature-dependent (activation energy 3.4 kcal/mol). In contrast, t(1/2) for type II cells in suspension was much slower, ≈1 s; P(f) for type II cells was 0.013 cm/s. Vesicles derived from type I cells also had a very high P(f) of 0.06–0.08 cm/s at 10°C that was inhibited 95% by HgCl(2). The P(f) in type I cells is the highest measured for any mammalian cell membrane and would account for the high water permeability of the lung.