Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 Oct;81(4):2172–2180. doi: 10.1016/S0006-3495(01)75865-1

Discrepancy between phase behavior of lung surfactant phospholipids and the classical model of surfactant function.

B Piknova 1, W R Schief 1, V Vogel 1, B M Discher 1, S B Hall 1
PMCID: PMC1301689  PMID: 11566788

Abstract

The studies reported here used fluorescence microscopy and Brewster angle microscopy to test the classical model of how pulmonary surfactant forms films that are metastable at high surface pressures in the lungs. The model predicts that the functional film is liquid-condensed (LC) and greatly enriched in dipalmitoyl phosphatidylcholine (DPPC). Both microscopic methods show that, in monolayers containing the complete set of phospholipids from calf surfactant, an expanded phase persists in coexistence with condensed domains at surface pressures approaching 70 mN/m. Constituents collapsed from the interface above 45 mN/m, but the relative area of the two phases changed little, and the LC phase never occupied more than 30% of the interface. Calculations based on these findings and on isotherms obtained on the continuous interface of a captive bubble estimated that collapse of other constituents increased the mol fraction of DPPC to no higher than 0.37. We conclude that monolayers containing the complete set of phospholipids achieve high surface pressures without forming a homogeneous LC film and with a mixed composition that falls far short of the nearly pure DPPC predicted previously. These findings contradict the classical model.

Full Text

The Full Text of this article is available as a PDF (562.0 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. Bangham A. D., Morley C. J., Phillips M. C. The physical properties of an effective lung surfactant. Biochim Biophys Acta. 1979 Jun 21;573(3):552–556. doi: 10.1016/0005-2760(79)90229-7. [DOI] [PubMed] [Google Scholar]
  3. Clements J. A. Functions of the alveolar lining. Am Rev Respir Dis. 1977 Jun;115(6 Pt 2):67–71. doi: 10.1164/arrd.1977.115.S.67. [DOI] [PubMed] [Google Scholar]
  4. Crane J. M., Hall S. B. Rapid compression transforms interfacial monolayers of pulmonary surfactant. Biophys J. 2001 Apr;80(4):1863–1872. doi: 10.1016/S0006-3495(01)76156-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crane J. M., Putz G., Hall S. B. Persistence of phase coexistence in disaturated phosphatidylcholine monolayers at high surface pressures. Biophys J. 1999 Dec;77(6):3134–3143. doi: 10.1016/S0006-3495(99)77143-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Discher B. M., Maloney K. M., Grainger D. W., Sousa C. A., Hall S. B. Neutral lipids induce critical behavior in interfacial monolayers of pulmonary surfactant. Biochemistry. 1999 Jan 5;38(1):374–383. doi: 10.1021/bi981386h. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Discher B. M., Schief W. R., Vogel V., Hall S. B. Phase separation in monolayers of pulmonary surfactant phospholipids at the air-water interface: composition and structure. Biophys J. 1999 Oct;77(4):2051–2061. doi: 10.1016/S0006-3495(99)77046-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goerke J., Gonzales J. Temperature dependence of dipalmitoyl phosphatidylcholine monolayer stability. J Appl Physiol Respir Environ Exerc Physiol. 1981 Nov;51(5):1108–1114. doi: 10.1152/jappl.1981.51.5.1108. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Hildebran J. N., Goerke J., Clements J. A. Pulmonary surface film stability and composition. J Appl Physiol Respir Environ Exerc Physiol. 1979 Sep;47(3):604–611. doi: 10.1152/jappl.1979.47.3.604. [DOI] [PubMed] [Google Scholar]
  12. Horie T., Hildebrandt J. Dynamic compliance, limit cycles, and static equilibria of excised cat lung. J Appl Physiol. 1971 Sep;31(3):423–430. doi: 10.1152/jappl.1971.31.3.423. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Putz G., Goerke J., Schürch S., Clements J. A. Evaluation of pressure-driven captive bubble surfactometer. J Appl Physiol (1985) 1994 Apr;76(4):1417–1424. doi: 10.1152/jappl.1994.76.4.1417. [DOI] [PubMed] [Google Scholar]
  17. Schürch S., Bachofen H., Goerke J., Possmayer F. A captive bubble method reproduces the in situ behavior of lung surfactant monolayers. J Appl Physiol (1985) 1989 Dec;67(6):2389–2396. doi: 10.1152/jappl.1989.67.6.2389. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Schürch S., Qanbar R., Bachofen H., Possmayer F. The surface-associated surfactant reservoir in the alveolar lining. Biol Neonate. 1995;67 (Suppl 1):61–76. doi: 10.1159/000244207. [DOI] [PubMed] [Google Scholar]
  20. Van Golde L. M., Batenburg J. J., Robertson B. The pulmonary surfactant system: biochemical aspects and functional significance. Physiol Rev. 1988 Apr;68(2):374–455. doi: 10.1152/physrev.1988.68.2.374. [DOI] [PubMed] [Google Scholar]
  21. Veldhuizen E. J., Haagsman H. P. Role of pulmonary surfactant components in surface film formation and dynamics. Biochim Biophys Acta. 2000 Aug 25;1467(2):255–270. doi: 10.1016/s0005-2736(00)00256-x. [DOI] [PubMed] [Google Scholar]
  22. Watkins J. C. The surface properties of pure phospholipids in relation to those of lung extracts. Biochim Biophys Acta. 1968 Mar 4;152(2):293–306. doi: 10.1016/0005-2760(68)90037-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES