Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1998 Mar;74(3):1101–1109. doi: 10.1016/s0006-3495(98)77828-2

Differential partitioning of pulmonary surfactant protein SP-A into regions of monolayers of dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylcholine/dipalmitoylphosphatidylglycerol.

M L Ruano 1, K Nag 1, L A Worthman 1, C Casals 1, J Pérez-Gil 1, K M Keough 1
PMCID: PMC1299462  PMID: 9512012

Abstract

The interaction of the pulmonary surfactant protein SP-A fluorescently labeled with Texas Red (TR-SP-A) with monolayers of dipalmitoylphosphatidylcholine (DPPC) and DPPC/dipalmitoylphosphatidylglycerol 7:3 w/w has been investigated. The monolayers were spread on aqueous subphases containing TR-SP-A. TR-SP-A interacted with the monolayers of DPPC to accumulate at the boundary regions between liquid condensed (LC) and liquid expanded (LE) phases. Some TR-SP-A appeared in the LE phase but not in the LC phase. At intermediate surface pressures (10-20 mN/m), the protein caused the occurrence of more, smaller condensed domains, and it appeared to be excluded from the monolayers at surface pressure in the range of 30-40 mN/m. TR-SP-A interaction with DPPC/dipalmitoylphosphatidylglycerol monolayers was different. The protein did not appear in either LE or LC but only in large aggregates at the LC-LE boundary regions, a distribution visually similar to that of fluorescently labeled concanavalin A adsorbed onto monolayers of DPPC. The observations are consistent with a selectivity of interaction of SP-A with DPPC and for its accumulation in boundaries between LC and LE phase.

Full Text

The Full Text of this article is available as a PDF (393.0 KB).

Selected References

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

  1. Bates S. R., Dodia C., Fisher A. B. Surfactant protein A regulates uptake of pulmonary surfactant by lung type II cells on microporous membranes. Am J Physiol. 1994 Dec;267(6 Pt 1):L753–L760. doi: 10.1152/ajplung.1994.267.6.L753. [DOI] [PubMed] [Google Scholar]
  2. Casals C., Herrera L., Miguel E., Garcia-Barreno P., Municio A. M. Comparison between intra- and extracellular surfactant in respiratory distress induced by oleic acid. Biochim Biophys Acta. 1989 Jun 8;1003(2):201–203. doi: 10.1016/0005-2760(89)90256-7. [DOI] [PubMed] [Google Scholar]
  3. Casals C., Miguel E., Perez-Gil J. Tryptophan fluorescence study on the interaction of pulmonary surfactant protein A with phospholipid vesicles. Biochem J. 1993 Dec 15;296(Pt 3):585–593. doi: 10.1042/bj2960585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Childs R. A., Wright J. R., Ross G. F., Yuen C. T., Lawson A. M., Chai W., Drickamer K., Feizi T. Specificity of lung surfactant protein SP-A for both the carbohydrate and the lipid moieties of certain neutral glycolipids. J Biol Chem. 1992 May 15;267(14):9972–9979. [PubMed] [Google Scholar]
  5. Cockshutt A. M., Weitz J., Possmayer F. Pulmonary surfactant-associated protein A enhances the surface activity of lipid extract surfactant and reverses inhibition by blood proteins in vitro. Biochemistry. 1990 Sep 11;29(36):8424–8429. doi: 10.1021/bi00488a032. [DOI] [PubMed] [Google Scholar]
  6. Dobbs L. G., Wright J. R., Hawgood S., Gonzalez R., Venstrom K., Nellenbogen J. Pulmonary surfactant and its components inhibit secretion of phosphatidylcholine from cultured rat alveolar type II cells. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1010–1014. doi: 10.1073/pnas.84.4.1010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem. 1988 Jul 15;263(20):9557–9560. [PubMed] [Google Scholar]
  8. Grainger D. W., Reichert A., Ringsdorf H., Salesse C. Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: direct observation of enzyme domain formation using fluorescence microscopy. Biochim Biophys Acta. 1990 Apr 30;1023(3):365–379. doi: 10.1016/0005-2736(90)90128-b. [DOI] [PubMed] [Google Scholar]
  9. Hawgood S., Benson B. J., Hamilton R. L., Jr Effects of a surfactant-associated protein and calcium ions on the structure and surface activity of lung surfactant lipids. Biochemistry. 1985 Jan 1;24(1):184–190. doi: 10.1021/bi00322a026. [DOI] [PubMed] [Google Scholar]
  10. Hawgood S., Benson B. J., Schilling J., Damm D., Clements J. A., White R. T. Nucleotide and amino acid sequences of pulmonary surfactant protein SP 18 and evidence for cooperation between SP 18 and SP 28-36 in surfactant lipid adsorption. Proc Natl Acad Sci U S A. 1987 Jan;84(1):66–70. doi: 10.1073/pnas.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hawgood S., Shiffer K. Structures and properties of the surfactant-associated proteins. Annu Rev Physiol. 1991;53:375–394. doi: 10.1146/annurev.ph.53.030191.002111. [DOI] [PubMed] [Google Scholar]
  12. Heckl W. M., Zaba B. N., Möhwald H. Interactions of cytochromes b5 and c with phospholipid monolayers. Biochim Biophys Acta. 1987 Sep 18;903(1):166–176. doi: 10.1016/0005-2736(87)90166-0. [DOI] [PubMed] [Google Scholar]
  13. Horowitz A. D., Baatz J. E., Whitsett J. A. Lipid effects on aggregation of pulmonary surfactant protein SP-C studied by fluorescence energy transfer. Biochemistry. 1993 Sep 21;32(37):9513–9523. doi: 10.1021/bi00088a001. [DOI] [PubMed] [Google Scholar]
  14. Horowitz A. D. Exclusion of SP-C, but not SP-B, by gel phase palmitoyl lipids. Chem Phys Lipids. 1995 May 22;76(1):27–39. doi: 10.1016/0009-3084(94)02426-6. [DOI] [PubMed] [Google Scholar]
  15. Johansson J., Curstedt T., Robertson B. The proteins of the surfactant system. Eur Respir J. 1994 Feb;7(2):372–391. doi: 10.1183/09031936.94.07020372. [DOI] [PubMed] [Google Scholar]
  16. King R. J., Carmichael M. C., Horowitz P. M. Reassembly of lipid-protein complexes of pulmonary surfactant. Proposed mechanism of interaction. J Biol Chem. 1983 Sep 10;258(17):10672–10680. [PubMed] [Google Scholar]
  17. King R. J., Phillips M. C., Horowitz P. M., Dang S. C. Interaction between the 35 kDa apolipoprotein of pulmonary surfactant and saturated phosphatidylcholines. Effects of temperature. Biochim Biophys Acta. 1986 Oct 24;879(1):1–13. doi: 10.1016/0005-2760(86)90259-6. [DOI] [PubMed] [Google Scholar]
  18. Korfhagen T. R., Bruno M. D., Ross G. F., Huelsman K. M., Ikegami M., Jobe A. H., Wert S. E., Stripp B. R., Morris R. E., Glasser S. W. Altered surfactant function and structure in SP-A gene targeted mice. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9594–9599. doi: 10.1073/pnas.93.18.9594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuroki Y., Akino T. Pulmonary surfactant protein A (SP-A) specifically binds dipalmitoylphosphatidylcholine. J Biol Chem. 1991 Feb 15;266(5):3068–3073. [PubMed] [Google Scholar]
  20. Kuroki Y., Gasa S., Ogasawara Y., Makita A., Akino T. Binding of pulmonary surfactant protein A to galactosylceramide and asialo-GM2. Arch Biochem Biophys. 1992 Dec;299(2):261–267. doi: 10.1016/0003-9861(92)90273-y. [DOI] [PubMed] [Google Scholar]
  21. Kuroki Y., Voelker D. R. Pulmonary surfactant proteins. J Biol Chem. 1994 Oct 21;269(42):25943–25946. [PubMed] [Google Scholar]
  22. Maloney K. M., Grandbois M., Grainger D. W., Salesse C., Lewis K. A., Roberts M. F. Phospholipase A2 domain formation in hydrolyzed asymmetric phospholipid monolayers at the air/water interface. Biochim Biophys Acta. 1995 May 4;1235(2):395–405. doi: 10.1016/0005-2736(95)80029-f. [DOI] [PubMed] [Google Scholar]
  23. Möhwald H. Phospholipid and phospholipid-protein monolayers at the air/water interface. Annu Rev Phys Chem. 1990;41:441–476. doi: 10.1146/annurev.pc.41.100190.002301. [DOI] [PubMed] [Google Scholar]
  24. Nag K., Boland C., Rich N., Keough K. M. Epifluorescence microscopic observation of monolayers of dipalmitoylphosphatidylcholine: dependence of domain size on compression rates. Biochim Biophys Acta. 1991 Sep 30;1068(2):157–160. doi: 10.1016/0005-2736(91)90204-l. [DOI] [PubMed] [Google Scholar]
  25. Nag K., Keough K. M. Epifluorescence microscopic studies of monolayers containing mixtures of dioleoyl- and dipalmitoylphosphatidylcholines. Biophys J. 1993 Sep;65(3):1019–1026. doi: 10.1016/S0006-3495(93)81155-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nag K., Perez-Gil J., Cruz A., Keough K. M. Fluorescently labeled pulmonary surfactant protein C in spread phospholipid monolayers. Biophys J. 1996 Jul;71(1):246–256. doi: 10.1016/S0006-3495(96)79221-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nag K., Perez-Gil J., Cruz A., Rich N. H., Keough K. M. Spontaneous formation of interfacial lipid-protein monolayers during adsorption from vesicles. Biophys J. 1996 Sep;71(3):1356–1363. doi: 10.1016/S0006-3495(96)79338-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nag K., Taneva S. G., Perez-Gil J., Cruz A., Keough K. M. Combinations of fluorescently labeled pulmonary surfactant proteins SP-B and SP-C in phospholipid films. Biophys J. 1997 Jun;72(6):2638–2650. doi: 10.1016/S0006-3495(97)78907-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pérez-Gil J., Nag K., Taneva S., Keough K. M. Pulmonary surfactant protein SP-C causes packing rearrangements of dipalmitoylphosphatidylcholine in spread monolayers. Biophys J. 1992 Jul;63(1):197–204. doi: 10.1016/S0006-3495(92)81582-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ruano M. L., Miguel E., Perez-Gil J., Casals C. Comparison of lipid aggregation and self-aggregation activities of pulmonary surfactant-associated protein A. Biochem J. 1996 Jan 15;313(Pt 2):683–689. doi: 10.1042/bj3130683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schürch S., Possmayer F., Cheng S., Cockshutt A. M. Pulmonary SP-A enhances adsorption and appears to induce surface sorting of lipid extract surfactant. Am J Physiol. 1992 Aug;263(2 Pt 1):L210–L218. doi: 10.1152/ajplung.1992.263.2.L210. [DOI] [PubMed] [Google Scholar]
  32. Strayer D. S., Herting E., Sun B., Robertson B. Antibody to surfactant protein A increases sensitivity of pulmonary surfactant to inactivation by fibrinogen in vivo. Am J Respir Crit Care Med. 1996 Mar;153(3):1116–1122. doi: 10.1164/ajrccm.153.3.8630554. [DOI] [PubMed] [Google Scholar]
  33. Suzuki Y., Fujita Y., Kogishi K. Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant. Am Rev Respir Dis. 1989 Jul;140(1):75–81. doi: 10.1164/ajrccm/140.1.75. [DOI] [PubMed] [Google Scholar]
  34. Taneva S., McEachren T., Stewart J., Keough K. M. Pulmonary surfactant protein SP-A with phospholipids in spread monolayers at the air-water interface. Biochemistry. 1995 Aug 15;34(32):10279–10289. doi: 10.1021/bi00032a023. [DOI] [PubMed] [Google Scholar]
  35. Voss T., Eistetter H., Schäfer K. P., Engel J. Macromolecular organization of natural and recombinant lung surfactant protein SP 28-36. Structural homology with the complement factor C1q. J Mol Biol. 1988 May 5;201(1):219–227. doi: 10.1016/0022-2836(88)90448-2. [DOI] [PubMed] [Google Scholar]
  36. White R. T., Damm D., Miller J., Spratt K., Schilling J., Hawgood S., Benson B., Cordell B. Isolation and characterization of the human pulmonary surfactant apoprotein gene. 1985 Sep 26-Oct 2Nature. 317(6035):361–363. doi: 10.1038/317361a0. [DOI] [PubMed] [Google Scholar]
  37. Williams M. C., Hawgood S., Hamilton R. L. Changes in lipid structure produced by surfactant proteins SP-A, SP-B, and SP-C. Am J Respir Cell Mol Biol. 1991 Jul;5(1):41–50. doi: 10.1165/ajrcmb/5.1.41. [DOI] [PubMed] [Google Scholar]
  38. Wright J. R., Youmans D. C. Degradation of surfactant lipids and surfactant protein A by alveolar macrophages in vitro. Am J Physiol. 1995 May;268(5 Pt 1):L772–L780. doi: 10.1152/ajplung.1995.268.5.L772. [DOI] [PubMed] [Google Scholar]
  39. Yu S. H., Possmayer F. Effect of pulmonary surfactant protein A and neutral lipid on accretion and organization of dipalmitoylphosphatidylcholine in surface films. J Lipid Res. 1996 Jun;37(6):1278–1288. [PubMed] [Google Scholar]
  40. van Golde L. M. Potential role of surfactant proteins A and D in innate lung defense against pathogens. Biol Neonate. 1995;67 (Suppl 1):2–17. doi: 10.1159/000244202. [DOI] [PubMed] [Google Scholar]

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

RESOURCES