Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2000 Jan;78(1):257–266. doi: 10.1016/S0006-3495(00)76589-1

Distinct steps in the adsorption of pulmonary surfactant to an air-liquid interface.

R W Walters 1, R R Jenq 1, S B Hall 1
PMCID: PMC1300634  PMID: 10620290

Abstract

To investigate the mechanisms by which vesicles of pulmonary surfactant adsorb to an air-liquid interface, we measured the effect of different phospholipids and of their concentration both in the subphase and at the interface on this process. Adsorbing vesicles contained the hydrophobic surfactant proteins mixed with the following four sets of surfactant phospholipids that varied the content of anionic headgroups and mixed acyl chains independently: the complete set of purified phospholipids (PPL) from calf surfactant; modified PPL (mPPL) from which the anionic phospholipids were removed; a mixture of dipalmitoyl phosphatidylcholine (DPPC) and dipalmitoyl phosphatidylglycerol (DPPG) (9:1, mol:mol); and DPPC alone. The initial reduction in surface tension depended strongly on the anionic phospholipids and the subphase concentration. The acyl groups had no effect. Adsorption beyond the initial stage depended more on the mixed acyl groups, became increasingly independent of subphase concentration, and was determined instead by the interfacial concentration of the surface film. The different constituents produced the same effects in vesicles adsorbing to a clean interface or in a preexisting film to which vesicles of SP:DPPC adsorbed. Adsorption for vesicles of SP:PPL adsorbing to DPPC or of SP:DPPC to PPL above a certain threshold surface concentration followed exactly the same isotherm. Our results fit best with a two-step model for adsorption. The anionic phospholipids first promote the initial juxtaposition of vesicles to the interface. Compounds with mixed acyl constituents at the point of contact between vesicle and interface then facilitate fusion with the surface.

Full Text

The Full Text of this article is available as a PDF (146.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  2. Chernomordik L., Chanturiya A., Green J., Zimmerberg J. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys J. 1995 Sep;69(3):922–929. doi: 10.1016/S0006-3495(95)79966-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chu J., Clements J. A., Cotton E. K., Klaus M. H., Sweet A. Y., Tooley W. H., Bradley B. L., Brandorff L. C. Neonatal pulmonary ischemia. I. Clinical and physiological studies. Pediatrics. 1967 Oct;40(4 Suppl):709–782. [PubMed] [Google Scholar]
  4. Davies R. J., Genghini M., Walters D. V., Morley C. J. The behaviour of lung surfactant in electrolyte solutions. Biochim Biophys Acta. 1986 Sep 12;878(2):135–145. doi: 10.1016/0005-2760(86)90139-6. [DOI] [PubMed] [Google Scholar]
  5. Discher B. M., Maloney K. M., Schief W. R., Jr, Grainger D. W., Vogel V., Hall S. B. Lateral phase separation in interfacial films of pulmonary surfactant. Biophys J. 1996 Nov;71(5):2583–2590. doi: 10.1016/S0006-3495(96)79450-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Enhorning G. Pulsating bubble technique for evaluating pulmonary surfactant. J Appl Physiol Respir Environ Exerc Physiol. 1977 Aug;43(2):198–203. doi: 10.1152/jappl.1977.43.2.198. [DOI] [PubMed] [Google Scholar]
  7. Feigenson G. W. On the nature of calcium ion binding between phosphatidylserine lamellae. Biochemistry. 1986 Sep 23;25(19):5819–5825. doi: 10.1021/bi00367a071. [DOI] [PubMed] [Google Scholar]
  8. Hall S. B., Venkitaraman A. R., Whitsett J. A., Holm B. A., Notter R. H. Importance of hydrophobic apoproteins as constituents of clinical exogenous surfactants. Am Rev Respir Dis. 1992 Jan;145(1):24–30. doi: 10.1164/ajrccm/145.1.24. [DOI] [PubMed] [Google Scholar]
  9. Hall S. B., Wang Z., Notter R. H. Separation of subfractions of the hydrophobic components of calf lung surfactant. J Lipid Res. 1994 Aug;35(8):1386–1394. [PubMed] [Google Scholar]
  10. Hayashi H., Adachi H., Kataoka K., Sato H., Akino T. Molecular species profiles of acidic phospholipids in lung fractions of adult and perinatal rabbits. Biochim Biophys Acta. 1990 Jan 16;1042(1):126–131. doi: 10.1016/0005-2760(90)90066-7. [DOI] [PubMed] [Google Scholar]
  11. Israelachvili J., Wennerström H. Role of hydration and water structure in biological and colloidal interactions. Nature. 1996 Jan 18;379(6562):219–225. doi: 10.1038/379219a0. [DOI] [PubMed] [Google Scholar]
  12. Kahn M. C., Anderson G. J., Anyan W. R., Hall S. B. Phosphatidylcholine molecular species of calf lung surfactant. Am J Physiol. 1995 Nov;269(5 Pt 1):L567–L573. doi: 10.1152/ajplung.1995.269.5.L567. [DOI] [PubMed] [Google Scholar]
  13. Kaplan R. S., Pedersen P. L. Sensitive protein assay in presence of high levels of lipid. Methods Enzymol. 1989;172:393–399. doi: 10.1016/s0076-6879(89)72025-5. [DOI] [PubMed] [Google Scholar]
  14. King R. J., Clements J. A. Surface active materials from dog lung. 3. Thermal analysis. Am J Physiol. 1972 Sep;223(3):727–733. doi: 10.1152/ajplegacy.1972.223.3.727. [DOI] [PubMed] [Google Scholar]
  15. Leikin S., Parsegian V. A., Rau D. C., Rand R. P. Hydration forces. Annu Rev Phys Chem. 1993;44:369–395. doi: 10.1146/annurev.pc.44.100193.002101. [DOI] [PubMed] [Google Scholar]
  16. McIntosh T. J., Advani S., Burton R. E., Zhelev D. V., Needham D., Simon S. A. Experimental tests for protrusion and undulation pressures in phospholipid bilayers. Biochemistry. 1995 Jul 11;34(27):8520–8532. doi: 10.1021/bi00027a002. [DOI] [PubMed] [Google Scholar]
  17. McIntosh T. J., Simon S. A. Hydration and steric pressures between phospholipid bilayers. Annu Rev Biophys Biomol Struct. 1994;23:27–51. doi: 10.1146/annurev.bb.23.060194.000331. [DOI] [PubMed] [Google Scholar]
  18. Notter R. H., Finkelstein J. N., Taubold R. D. Comparative adsorption of natural lung surfactant, extracted phospholipids, and artificial phospholipid mixtures to the air-water interface. Chem Phys Lipids. 1983 Jul;33(1):67–80. doi: 10.1016/0009-3084(83)90009-9. [DOI] [PubMed] [Google Scholar]
  19. Oosterlaken-Dijksterhuis M. A., Haagsman H. P., van Golde L. M., Demel R. A. Characterization of lipid insertion into monomolecular layers mediated by lung surfactant proteins SP-B and SP-C. Biochemistry. 1991 Nov 12;30(45):10965–10971. doi: 10.1021/bi00109a022. [DOI] [PubMed] [Google Scholar]
  20. Oosterlaken-Dijksterhuis M. A., Haagsman H. P., van Golde L. M., Demel R. A. Interaction of lipid vesicles with monomolecular layers containing lung surfactant proteins SP-B or SP-C. Biochemistry. 1991 Aug 20;30(33):8276–8281. doi: 10.1021/bi00247a024. [DOI] [PubMed] [Google Scholar]
  21. Portis A., Newton C., Pangborn W., Papahadjopoulos D. Studies on the mechanism of membrane fusion: evidence for an intermembrane Ca2+-phospholipid complex, synergism with Mg2+, and inhibition by spectrin. Biochemistry. 1979 Mar 6;18(5):780–790. doi: 10.1021/bi00572a007. [DOI] [PubMed] [Google Scholar]
  22. Schlame M., Casals C., Rüstow B., Rabe H., Kunze D. Molecular species of phosphatidylcholine and phosphatidylglycerol in rat lung surfactant and different pools of pneumocytes type II. Biochem J. 1988 Jul 1;253(1):209–215. doi: 10.1042/bj2530209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schlame M., Rüstow B., Kunze D., Rabe H., Reichmann G. Phosphatidylglycerol of rat lung. Intracellular sites of formation de novo and acyl species pattern in mitochondria, microsomes and surfactant. Biochem J. 1986 Nov 15;240(1):247–252. doi: 10.1042/bj2400247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schürch S. Surface tension at low lung volumes: dependence on time and alveolar size. Respir Physiol. 1982 Jun;48(3):339–355. doi: 10.1016/0034-5687(82)90038-x. [DOI] [PubMed] [Google Scholar]
  25. Takahashi A., Fujiwara T. Proteolipid in bovine lung surfactant: its role in surfactant function. Biochem Biophys Res Commun. 1986 Mar 13;135(2):527–532. doi: 10.1016/0006-291x(86)90026-4. [DOI] [PubMed] [Google Scholar]
  26. Wang Z., Hall S. B., Notter R. H. Roles of different hydrophobic constituents in the adsorption of pulmonary surfactant. J Lipid Res. 1996 Apr;37(4):790–798. [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES