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 a;nd 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 st 12 degrees 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 degrees 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, approximate to 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 degrees C that was inhibited 95% by HgCl2. 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.