Langmuir isotherms, fluorescence microscopy, and atomic force microscopy were used to study lung surfactant specific proteins SP-B and SP-C in monolayers of dipalmitoylphosphatidylglycerol (DPPG) and palmitoyloleoylphosphatidylglycerol (POPG), which are representative of the anionic lipids in native and replacement lung surfactants. Both SP-B and SP-C eliminate squeeze-out of POPG from mixed DPPG/POPG monolayers by inducing a two- to three-dimensional transformation of the fluid-phase fraction of the monolayer. SP-B induces a reversible folding transition at monolayer collapse, allowing all components of surfactant to remain at the interface during respreading. The folds remain attached to the monolayer, are identical in composition and morphology to the unfolded monolayer, and are reincorporated reversibly into the monolayer upon expansion. In the absence of SP-B or SP-C, the unsaturated lipids are irreversibly lost at high surface pressures. These morphological transitions are identical to those in other lipid mixtures and hence appear to be independent of the detailed lipid composition of the monolayer. Instead they depend on the more general phenomena of coexistence between a liquid-expanded and liquid-condensed phase. These three-dimensional monolayer transitions reconcile how lung surfactant can achieve both low surface tensions upon compression and rapid respreading upon expansion and may have important implications toward the optimal design of replacement surfactants. The overlap of function between SP-B and SP-C helps explain why replacement surfactants lacking in one or the other proteins often have beneficial effects.
Bibliographical noteFunding Information:
J.D., K.Y.C.L., M.M.L., and J.A.Z. were supported by National Institutes of Health grant HL-51177; J.A.Z., J.D., and A.J.W. were also supported by the Tobacco Related Disease Research Program grant 8RT-0077. A.J.W. was also supported by National Institutes of Health grant HL55534, the Drew RCMI Bioinformatics Core (NCRR/RCMI G12 RR 03026), and National Institutes of Health small equipment grant GM 50483. K.Y.C.L. was supported by the March of Dimes Award (5-FY98–0728), the Searle Scholars Program/The Chicago Community Trust (99-C-105), the American Lung Association (RG-085-N), and the Packard Foundation (99–1465).
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