Abstract
Langmuir isotherms and fluorescence and atomic force microscopy images of synthetic model lung surfactants were used to determine the influence of palmitic acid and synthetic peptides based on the surfactant-specific proteins SP-B and SP-C on the morphology and function of surfactant monolayers. Lung surfactant-specific protein SP-C and peptides based on SP-C eliminate the loss to the subphase of unsaturated lipids necessary for good adsorption and respreading by inducing a transition between monolayers and multilayers within the fluid phase domains of the monolayer. The morphology and thickness of the multilayer phase depends on the lipid composition of the monolayer and the concentration of SP-C or SP-C peptide. Lung surfactant protein SP-B and peptides based on SP-B induce a reversible folding transition at monolayer collapse that allows all components of surfactant to be retained at the interface during respreading. Supplementing Survanta, a clinically used replacement lung surfactant, with a peptide based on the first 25 amino acids of SP-B also induces a similar folding transition at monolayer collapse. Palmitic acid makes the monolayer rigid at low surface tension and fluid at high surface tension and modifies SP-C function. Identifying the function of lung surfactant proteins and lipids is essential to the rational design of replacement surfactants for treatment of respiratory distress syndrome.
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- Bachofen H., Schürch S., Urbinelli M., Weibel E. R. Relations among alveolar surface tension, surface area, volume, and recoil pressure. J Appl Physiol (1985) 1987 May;62(5):1878–1887. doi: 10.1152/jappl.1987.62.5.1878. [DOI] [PubMed] [Google Scholar]
- Bastacky J., Lee C. Y., Goerke J., Koushafar H., Yager D., Kenaga L., Speed T. P., Chen Y., Clements J. A. Alveolar lining layer is thin and continuous: low-temperature scanning electron microscopy of rat lung. J Appl Physiol (1985) 1995 Nov;79(5):1615–1628. doi: 10.1152/jappl.1995.79.5.1615. [DOI] [PubMed] [Google Scholar]
- Batenburg J. J., Haagsman H. P. The lipids of pulmonary surfactant: dynamics and interactions with proteins. Prog Lipid Res. 1998 Sep;37(4):235–276. doi: 10.1016/s0163-7827(98)00011-3. [DOI] [PubMed] [Google Scholar]
- Bernhard W., Mottaghian J., Gebert A., Rau G. A., von Der HARDT H., Poets C. F. Commercial versus native surfactants. Surface activity, molecular components, and the effect of calcium. Am J Respir Crit Care Med. 2000 Oct;162(4 Pt 1):1524–1533. doi: 10.1164/ajrccm.162.4.9908104. [DOI] [PubMed] [Google Scholar]
- Bruni R., Taeusch H. W., Waring A. J. Surfactant protein B: lipid interactions of synthetic peptides representing the amino-terminal amphipathic domain. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7451–7455. doi: 10.1073/pnas.88.16.7451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cochrane C. G., Revak S. D. Pulmonary surfactant protein B (SP-B): structure-function relationships. Science. 1991 Oct 25;254(5031):566–568. doi: 10.1126/science.1948032. [DOI] [PubMed] [Google Scholar]
- Davis A. J., Jobe A. H., Häfner D., Ikegami M. Lung function in premature lambs and rabbits treated with a recombinant SP-C surfactant. Am J Respir Crit Care Med. 1998 Feb;157(2):553–559. doi: 10.1164/ajrccm.157.2.97-08019. [DOI] [PubMed] [Google Scholar]
- Gericke A., Flach C. R., Mendelsohn R. Structure and orientation of lung surfactant SP-C and L-alpha-dipalmitoylphosphatidylcholine in aqueous monolayers. Biophys J. 1997 Jul;73(1):492–499. doi: 10.1016/S0006-3495(97)78087-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):79–89. doi: 10.1016/s0925-4439(98)00060-x. [DOI] [PubMed] [Google Scholar]
- Gordon L. M., Horvath S., Longo M. L., Zasadzinski J. A., Taeusch H. W., Faull K., Leung C., Waring A. J. Conformation and molecular topography of the N-terminal segment of surfactant protein B in structure-promoting environments. Protein Sci. 1996 Aug;5(8):1662–1675. doi: 10.1002/pro.5560050820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gordon L. M., Lee K. Y., Lipp M. M., Zasadzinski J. A., Walther F. J., Sherman M. A., Waring A. J. Conformational mapping of the N-terminal segment of surfactant protein B in lipid using 13C-enhanced Fourier transform infrared spectroscopy. J Pept Res. 2000 Apr;55(4):330–347. doi: 10.1034/j.1399-3011.2000.00693.x. [DOI] [PubMed] [Google Scholar]
- Grunder R., Gehr P., Bachofen H., Schürch S., Siegenthaler H. Structures of surfactant films: a scanning force microscopy study. Eur Respir J. 1999 Dec;14(6):1290–1296. doi: 10.1183/09031936.99.14612909. [DOI] [PubMed] [Google Scholar]
- Hawgood S., Derrick M., Poulain F. Structure and properties of surfactant protein B. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):150–160. doi: 10.1016/s0925-4439(98)00064-7. [DOI] [PubMed] [Google Scholar]
- Ikegami M., Horowitz A. D., Whitsett J. A., Jobe A. H. Clearance of SP-C and recombinant SP-C in vivo and in vitro. Am J Physiol. 1998 Jun;274(6 Pt 1):L933–L939. doi: 10.1152/ajplung.1998.274.6.L933. [DOI] [PubMed] [Google Scholar]
- Ikegami M., Jobe A. H. Surfactant protein-C in ventilated premature lamb lung. Pediatr Res. 1998 Dec;44(6):860–864. doi: 10.1203/00006450-199812000-00006. [DOI] [PubMed] [Google Scholar]
- Ingenito E. P., Mark L., Morris J., Espinosa F. F., Kamm R. D., Johnson M. Biophysical characterization and modeling of lung surfactant components. J Appl Physiol (1985) 1999 May;86(5):1702–1714. doi: 10.1152/jappl.1999.86.5.1702. [DOI] [PubMed] [Google Scholar]
- Jobe A. H. Hot topics in and new strategies for surfactant research. Biol Neonate. 1998 Sep;74 (Suppl 1):3–8. doi: 10.1159/000047028. [DOI] [PubMed] [Google Scholar]
- Johansson J. Structure and properties of surfactant protein C. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):161–172. doi: 10.1016/s0925-4439(98)00065-9. [DOI] [PubMed] [Google Scholar]
- Krol S., Ross M., Sieber M., Künneke S., Galla H. J., Janshoff A. Formation of three-dimensional protein-lipid aggregates in monolayer films induced by surfactant protein B. Biophys J. 2000 Aug;79(2):904–918. doi: 10.1016/S0006-3495(00)76346-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krueger MA, Gaver DP., 3rd A Theoretical Model of Pulmonary Surfactant Multilayer Collapse under Oscillating Area Conditions. J Colloid Interface Sci. 2000 Sep 15;229(2):353–364. doi: 10.1006/jcis.2000.7029. [DOI] [PubMed] [Google Scholar]
- Lipp M. M., Lee K. Y., Waring A., Zasadzinski J. A. Fluorescence, polarized fluorescence, and Brewster angle microscopy of palmitic acid and lung surfactant protein B monolayers. Biophys J. 1997 Jun;72(6):2783–2804. doi: 10.1016/S0006-3495(97)78921-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lipp M. M., Lee K. Y., Zasadzinski J. A., Waring A. J. Phase and morphology changes in lipid monolayers induced by SP-B protein and its amino-terminal peptide. Science. 1996 Aug 30;273(5279):1196–1199. doi: 10.1126/science.273.5279.1196. [DOI] [PubMed] [Google Scholar]
- Longo M. L., Bisagno A. M., Zasadzinski J. A., Bruni R., Waring A. J. A function of lung surfactant protein SP-B. Science. 1993 Jul 23;261(5120):453–456. doi: 10.1126/science.8332910. [DOI] [PubMed] [Google Scholar]
- Mizuno K., Ikegami M., Chen C. M., Ueda T., Jobe A. H. Surfactant protein-B supplementation improves in vivo function of a modified natural surfactant. Pediatr Res. 1995 Mar;37(3):271–276. doi: 10.1203/00006450-199503000-00004. [DOI] [PubMed] [Google Scholar]
- Nag K., Perez-Gil J., Ruano M. L., Worthman L. A., Stewart J., Casals C., Keough K. M. Phase transitions in films of lung surfactant at the air-water interface. Biophys J. 1998 Jun;74(6):2983–2995. doi: 10.1016/S0006-3495(98)78005-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poulain F. R., Clements J. A. Pulmonary surfactant therapy. West J Med. 1995 Jan;162(1):43–50. [PMC free article] [PubMed] [Google Scholar]
- Robertson B., Halliday H. L. Principles of surfactant replacement. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):346–361. doi: 10.1016/s0925-4439(98)00080-5. [DOI] [PubMed] [Google Scholar]
- Schürch S., Goerke J., Clements J. A. Direct determination of surface tension in the lung. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4698–4702. doi: 10.1073/pnas.73.12.4698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schürch S., Goerke J., Clements J. A. Direct determination of volume- and time-dependence of alveolar surface tension in excised lungs. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3417–3421. doi: 10.1073/pnas.75.7.3417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schürch S., Green F. H., Bachofen H. Formation and structure of surface films: captive bubble surfactometry. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):180–202. doi: 10.1016/s0925-4439(98)00067-2. [DOI] [PubMed] [Google Scholar]
- Taeusch H. W., Keough K. M., Williams M., Slavin R., Steele E., Lee A. S., Phelps D., Kariel N., Floros J., Avery M. E. Characterization of bovine surfactant for infants with respiratory distress syndrome. Pediatrics. 1986 Apr;77(4):572–581. [PubMed] [Google Scholar]
- Tanaka Y., Takei T., Aiba T., Masuda K., Kiuchi A., Fujiwara T. Development of synthetic lung surfactants. J Lipid Res. 1986 May;27(5):475–485. [PubMed] [Google Scholar]
- Tchoreloff P., Gulik A., Denizot B., Proust J. E., Puisieux F. A structural study of interfacial phospholipid and lung surfactant layers by transmission electron microscopy after Blodgett sampling: influence of surface pressure and temperature. Chem Phys Lipids. 1991 Sep;59(2):151–165. doi: 10.1016/0009-3084(91)90004-u. [DOI] [PubMed] [Google Scholar]
- Tokieda K., Whitsett J. A., Clark J. C., Weaver T. E., Ikeda K., McConnell K. B., Jobe A. H., Ikegami M., Iwamoto H. S. Pulmonary dysfunction in neonatal SP-B-deficient mice. Am J Physiol. 1997 Oct;273(4 Pt 1):L875–L882. doi: 10.1152/ajplung.1997.273.4.L875. [DOI] [PubMed] [Google Scholar]
- Tschumperlin D. J., Margulies S. S. Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol (1985) 1999 Jun;86(6):2026–2033. doi: 10.1152/jappl.1999.86.6.2026. [DOI] [PubMed] [Google Scholar]
- Veldhuizen R., Nag K., Orgeig S., Possmayer F. The role of lipids in pulmonary surfactant. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):90–108. doi: 10.1016/s0925-4439(98)00061-1. [DOI] [PubMed] [Google Scholar]
- Walther F. J., Hernández-Juviel J., Bruni R., Waring A. J. Protein composition of synthetic surfactant affects gas exchange in surfactant-deficient rats. Pediatr Res. 1998 May;43(5):666–673. doi: 10.1203/00006450-199805000-00016. [DOI] [PubMed] [Google Scholar]
- Walther F. J., Hernández-Juviel J., Bruni R., Waring A. J. Spiking Survanta with synthetic surfactant peptides improves oxygenation in surfactant-deficient rats. Am J Respir Crit Care Med. 1997 Sep;156(3 Pt 1):855–861. doi: 10.1164/ajrccm.156.3.9611053. [DOI] [PubMed] [Google Scholar]
- Wirtz H. R., Dobbs L. G. The effects of mechanical forces on lung functions. Respir Physiol. 2000 Jan;119(1):1–17. doi: 10.1016/s0034-5687(99)00092-4. [DOI] [PubMed] [Google Scholar]
- von Nahmen A., Schenk M., Sieber M., Amrein M. The structure of a model pulmonary surfactant as revealed by scanning force microscopy. Biophys J. 1997 Jan;72(1):463–469. doi: 10.1016/S0006-3495(97)78687-9. [DOI] [PMC free article] [PubMed] [Google Scholar]