Skip to main content
SpringerLink
Log in

Lipid monolayers: Mechanisms of protein penetration with regard to membrane models

  • Published:
Lipids

Abstract

The influence of lipid and protein on the properties of the air-water interface is analyzed with the view to formulate a mechanism of interaction of protein with lipid monolayers. The increase in surface pressure (ΔΠ) and the quantity of protein incorporated in the lipid film after injection of protein under lipid monolayers were studied as a function of both lipid structure and protein structure. With rabbit γ-globulin, the values of ΔΠ were cholesterol > phosphatidyl choline > sphingomyelin. Similar results were obtained with ribonuclease, lysozyme and serum albumin. The quantities of protein found in films of either cholesterol or phosphatidyl choline (egg lecithin) were much larger than those calculated from a geometric model in which a protein monolayer occupies the area made available by the compressed lipid. Arguments are produced against penetration based on simple mechanisms of compressibility of the lipid film. The mechanisms operating in the incorporation of protein into lipid monolayers are grouped into three categories: (a) free penetration, typical of lecithin; (b) binding-mediated penetration, typical of cholesterol and some glycosphingolipids; and (c) binding-inhibited penetration, typical of the albumin-ganglioside system and a specific lipid hapten-antibody system. A model is described in which nonspecific protein interacts with polymeric lecithin structures (surface micelles). In the sequence of events X»Y»Z, the globular protein X is activated into the expanded or extended form Y by contact with the lipid and then restructured into a compact form Z with release of water and free energy. The resulting lipid-protein assembly has a mosaic structure in which lipid and protein polar surfaces are exposed to water. Accessibility of lecithin to phospholipase A is consistent with the model and with current views on the state of protein in biological membranes; according to such views, protein is more likely structured inside the lipid milieu and not simply denatured on the lipid-water interface.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Colacicco, G., and M. M. Rapport, J. Lipid Res. 7:258–263 (1966).

    PubMed  CAS  Google Scholar 

  2. Shah, D. O., and J. H. Schulman, J. Colloid Interface Sci. 25:107–119 (1967).

    Article  CAS  Google Scholar 

  3. Bangham, A. D., and R. M. C. Dawson, Biochem. J. 75:133–138 (1960).

    PubMed  CAS  Google Scholar 

  4. Colacicco, G., M. M. Rapport and D. Shapiro, J. Colloid Interface Sci. 25:5–15 (1967).

    Article  CAS  Google Scholar 

  5. Colacicco, G., and M. M. Rapport, Adv. Chem. Series 84:157–168 (1968).

    Google Scholar 

  6. Doty, P., and J. H. Schulman, Discuss. Faraday Soc. 6:21–27 (1949).

    Article  Google Scholar 

  7. Eley, D. D., and D. G. Hedge, Ibid. 21:221–228 (1956).

    Article  Google Scholar 

  8. Eley, D. D., and D. G. Hedge, J. Colloid Sci. 11:445–450 (1956).

    Article  CAS  Google Scholar 

  9. Khaiat, A., and I. R. Miller, Biochim. Biophys. Acta 183:309–319 (1969).

    Article  PubMed  CAS  Google Scholar 

  10. Colacicco, G., J. Colloid Interface Sci. 29:345–364 (1969).

    Article  PubMed  CAS  Google Scholar 

  11. Camejo, G., G. Colacicco and M. M. Rapport, J. Lipid Res. 9:562–569 (1968).

    PubMed  CAS  Google Scholar 

  12. Danielli, J. F., and H. A. Davson, J. Cell. Comp. Physiol. 5:495–508 (1935).

    Article  CAS  Google Scholar 

  13. Sjostrand, F. A., Nature 199:1262–1264 (1963).

    Article  Google Scholar 

  14. Benson, A. A., JAOCS 43:265–270 (1966).

    PubMed  CAS  Google Scholar 

  15. Lenard, J., and S. J. Singer, Proc. Natl. Acad. Sci. U.S.A. 56:1828–1835 (1966).

    Article  PubMed  CAS  Google Scholar 

  16. Robertson, J. D., Progr. Biophysics 10:343–418 (1960).

    CAS  Google Scholar 

  17. Colacicco, G., “Membrane Models.” Read before the Third International Conference on Biological Membranes. Stresa, Italy, June 1969.

  18. Ledeen, R., JAOCS 43:57–66 (1966).

    PubMed  CAS  Google Scholar 

  19. Satake, M., Y. Murata and T. Suzuki, J. Biochem. Tokyo 53:438–447 (1963).

    PubMed  CAS  Google Scholar 

  20. Hughes, A., Biochem. J. 29:437–444 (1935).

    PubMed  CAS  Google Scholar 

  21. Schulman, J. H., and E. K. Rideal, Ibid. 27:1581–1597 (1933).

    PubMed  CAS  Google Scholar 

  22. Yamashita, T., and H. B. Bull, J. Colloid Interface Sci. 24:310–316 (1967).

    Article  PubMed  CAS  Google Scholar 

  23. Eley, D. D., and D. G. Hedge, J. Colloid Sci. 12:419–429 (1957).

    Article  CAS  Google Scholar 

  24. Colacicco, G., “Concentration of Protein by Gibbs Equation and by Protein Analysis.” Read before the 156th Meeting of the American Chemical Society, Atlantic City, September 1968, Paper No. Coll 030.

  25. Camejo, G., Biochim. Biophys. Acta 175:290–300 (1969).

    PubMed  CAS  Google Scholar 

  26. Schulman, J. H., Discuss. Faraday Soc. 21:272–273 (1956).

    Article  Google Scholar 

  27. Eley, D. D., and G. Miller, “Proceedings of the Third International Congress on Surface Activity,” Vol. 2, Section B, Verlag Druckerei Universitaet Main GMB, Cologne, 1960, p. 157–160

  28. Pethica, B. A., and J. H. Schulman, Biochem. J. 53:177–185 (1952).

    Google Scholar 

  29. Shah, D. O., and J. H. Schulman, J. Lipid Res. 6:341–349 (1965).

    PubMed  CAS  Google Scholar 

  30. Shah, D. O., and J. H. Schulman, Lipids 2:21–27 (1967).

    CAS  PubMed  Google Scholar 

  31. Colacicco, G., “Lipid Monolayers: Surface Potentials of Lecithin and Sphingomyelin With Regard to Ca+ + Binding.” Read before the Third International Biophysics Congress, Cambridge, Massachusetts, August 1969, Paper 11G9.

  32. Colacicco, G., “Lipid Monolayers: Influence of Chemical Structure on Surface Properties.” Read before the AOCS 60th Annual Meeting, San Francisco, April 1969, Paper No. 63.

  33. Benhamou, N., and J. Guastalla, J. Chim. Phys. Physiocochim. Biol. 57:745–751 (1960).

    CAS  Google Scholar 

  34. Trurnit, H., J. Colloid Sci. 15:1–3 (1960).

    Article  CAS  Google Scholar 

  35. Colacicco, G., and S. Fleischer, “Surface Activity of Mitochondrial Structural Protein.” Read before the 52nd Federation Meeting, Atlantic City, April 1968, Paper 1378.

  36. Matalon, R., and J. H. Schulman, Discuss. Faraday Soc. 6:27–39 (1949).

    Google Scholar 

  37. Lenard, J., and S. J. Singer, Science 159:738–739 (1968).

    Article  CAS  PubMed  Google Scholar 

  38. Zahler, W. L., A. Saito and S. Fleischer, Biochem. Biophys. Res. Comm. 32:512–518 (1968).

    Article  PubMed  CAS  Google Scholar 

  39. Sessa, G., J. H. Freer, G. Colacicco and G. Weissmann, J. Biol. Chem. 244:3575–3582 (1969).

    PubMed  CAS  Google Scholar 

  40. Colacicco, G., “Lipid Monolayers: Effect of Lipid Structure on the Interaction With Protein.” Read before the 155th Meeting of the American Chemical Society, San Francisco, April 1968, Paper H90.

  41. Miller, I. R., and D. Bach, J. Colloid Interface Sci. 29:250–260 (1969).

    Article  PubMed  CAS  Google Scholar 

  42. Finean, J. B., Experientia 9:17–19 (1953).

    Article  PubMed  CAS  Google Scholar 

  43. Shah, D. O., J. H. Schulman, Advan. Chem. Ser. 84:189–209 (1968).

    Article  Google Scholar 

  44. Condrea, E., A. De Vries and J. Mager, Biochim. Biophys. Acta 84:60–73 (1964).

    PubMed  CAS  Google Scholar 

  45. Quarles, R. H., and R. M. C. Dawson, Biochem. J. 113:697–705 (1969).

    PubMed  CAS  Google Scholar 

  46. Zull, J. E., and C. G. Sciotto, Biochim. Biophys. Acta 173:409–418 (1969).

    Article  PubMed  CAS  Google Scholar 

  47. Colacicco, G., in “Horizons in Surface Science: Biological Applications,” Edited by L. M. Prince and D. F. Sears, Appleton-Century-Crofts, New York, in press.

  48. Chapman, D., Lipids 4:251–260 (1969).

    PubMed  CAS  Google Scholar 

  49. Chapman, D., R. B. Leslie, R. Hirz and A. M. Scanu, Nature 221:260–261 (1969).

    Article  PubMed  CAS  Google Scholar 

  50. Steim, J. M., O. D. Edner and F. G. Bargoot, Science 162:909–911 (1968).

    Article  PubMed  CAS  Google Scholar 

  51. Bangham, A. D., and D. Papahadjopoulos, Biochim. Biophys. Acta 126:181–184 (1966).

    PubMed  CAS  Google Scholar 

  52. Quinn, P. J., and R. M. C. Dawson, Biochem. J. 115:65–75 (1969).

    PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Giuseppe Colacicco

    Present address: Department of Pediatrics, Albert Einstein College of Medicine, 10461, Bronx, New York

Authors and Affiliations

  1. Department of Biochemistry, Albert Einstein College of Medicine, 10461, Bronx, New York

    Giuseppe Colacicco

Authors
  1. Giuseppe Colacicco
    View author publications

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Colacicco, G. Lipid monolayers: Mechanisms of protein penetration with regard to membrane models. Lipids 5, 636–649 (1970). https://doi.org/10.1007/BF02531343

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02531343

Keywords

Search

Navigation