Skip to main content
SpringerLink
Log in

Theory of protein-induced lateral phase separation in lipid membranes

  • Original Articles
  • Instrumentation and New Methodology
  • Published:
Cell Biophysics Aims and scope Submit manuscript

Abstract

An account is given of the current status of theoretical modeling of the phase equilibria in lipid membranes with intrinsic proteins. Special attention is paid to the description of lateral phase separation, which is important for membrane function since it may lead to biologically differentiated regions. We discuss in particular the mattressmodel approach by Mouritsen and Bloom (37), who take matching between protein and lipid hydrophobic thicknesses as a determining factor for the phase behavior. The model has been developed in the framework of phenomenological thermodynamics solution theory. The predictions of the theory are compared to a variety of experimental measurements, including those of membrane recombinants of the protein content of the reaction center and antenna protein of the bacterial photosynthetic apparatus as well as the erythrocyte band 3 protein. The physical effects of lipid-protein interactions are contrasted to those of lipid-cholesterol interactions. The concept of hydrophobic matching is then used as a basis for discussing a possible relationship between membrane thickness and physiological function.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Watts, A., and De Pont, J. J. H. H. M., eds., (1985),Progress in Protein-Lipid Interactions vol. 1, Elsevier, Amsterdam.

    Google Scholar 

  2. Watts, A., and De Pont, J. J. H. H. M., eds, (1986),Progress in Protein-Lipid Interactions, vol. 2, Elsevier, Amsterdam.

    Google Scholar 

  3. Quinn, P. J., and Chapman, D. (1980),CRC Crit. Rev. Biochem. 8, 1.

    Article  PubMed  CAS  Google Scholar 

  4. Sandermann, H. (1978),Biochim. Biophys. Acta 515, 209.

    PubMed  CAS  Google Scholar 

  5. McElhaney, R. N. (1982),Current Topics in Membranes and Transport, vol. 17 (S. Razin and S. Rottem, eds.), Academic, New York, pp. 317–380.

    Google Scholar 

  6. Curruthers, A. and Melchior, D. L. (1986),Trends Biochem. Sci. 11, 331.

    Article  Google Scholar 

  7. Sackmann, E. (1984),Biological Membranes, vol. 5. (1984), Academic, London, pp. 105–143.

    Google Scholar 

  8. Goldstein, J. L., Anderson, R. G. W., and Brown, M. S. (1979),Nature 279, 679.

    Article  PubMed  CAS  Google Scholar 

  9. Hirata, F. and Axelrod, J. (1980),Science 209, 1082.

    Article  PubMed  CAS  Google Scholar 

  10. Sackmann, E., Kotulla, R., and Heizler, F.-J. (1984),Can. J. Biochem. Cell Biol. 62, 778.

    PubMed  CAS  Google Scholar 

  11. Eisenberg, D. (1984),Ann. Rev. Biochem. 53, 595.

    Article  PubMed  CAS  Google Scholar 

  12. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985),Nature 318, 618.

    Article  Google Scholar 

  13. Bloom, M. and Smith, I. C. P. (1985), in Ref.. pp. 61–88.

    Google Scholar 

  14. Devaux, P. F. (1983),Biological Magnetic Resonance, vol. 5 (L. J. Berliner, and J. Reuben, eds.), Plenum, New York, pp. 183–299.

    Google Scholar 

  15. Devaux, P. F., Hoatson, G. L., Favre, E., Fellmann, P., Farren, B., MacKay, A. L., and Bloom, M. (1986),Biochemistry 25, 3804.

    Article  PubMed  CAS  Google Scholar 

  16. Mouritsen, O. G. (1987),Physics in Living Matter (D. Baeriswyl, M., Droz, A. Malaspinas, and P. Martinoli, eds.), Springer Verlag, Heidelberg, FRG, pp. 76–109.

    Chapter  Google Scholar 

  17. Philips, M. C. and Chapman, D. (1968),Biochim. Biophys. Acta 163, 301.

    Article  Google Scholar 

  18. Lee, A. G. (1977),Biochim. Biophys Acta 472, 285.

    PubMed  CAS  Google Scholar 

  19. Lewis, R. N. A. H., Mak, N., and McElhaney, R. N. (1987),Biochemistry 26, 6118.

    Article  PubMed  CAS  Google Scholar 

  20. Verkleij, A. J., Leunissen-Bijvelt, J., de Kruijff, B., Hope, M., and Cullis, P. R. (1984), inCell Fusion (D. Evered, and J. Whelan, eds.), Pitman, London, pp. 45–72.

    Google Scholar 

  21. Chapman, D., Cornell, B. A., Eliasz, A. W., and Perry, A. (1977),J. Mol. Biol. 113, 517.

    Article  PubMed  CAS  Google Scholar 

  22. Aloia, R. C. and Boggs, J. M. eds., (1985),Membrane Fluidity in Biology, vol. 4, Academic, New York.

    Google Scholar 

  23. Bloom, Y. and Mouritsen, O. G. (1988),Can. J. Chem. 66, 706.

    Article  CAS  Google Scholar 

  24. Inoko, Y. and Mitsui, T. (1978),J. Phys. Soc. Japan 44, 1918.

    CAS  Google Scholar 

  25. Evans, E. and Kwok, R. (1982),Biochemistry 21, 4874.

    Article  PubMed  CAS  Google Scholar 

  26. Mouritsen, O. G. and Zuckermann, M. J. (1985),Eur. Biophys. J. 12, 75.

    Article  PubMed  CAS  Google Scholar 

  27. Papahadjopoulos, D., Jacobson, K., Nir, S., and Isac, T. (1973),Biochim. Biophys. Acta 311, 330.

    Article  PubMed  CAS  Google Scholar 

  28. Nagle, J. F. (1980),Ann. Rev. Phys. Chem. 31, 157.

    Article  CAS  Google Scholar 

  29. Mouritsen, O. G. (1984),Computer Studies of Phase Transitions and Critical Phenomena, Springer Verlag, Heidelberg, chap. 5.

    Google Scholar 

  30. Zuckermann, M. J. and Mouritsen, O. G. (1987),Eur. Biophys. J. 15, 77.

    Article  CAS  Google Scholar 

  31. Barrow, D. A. and Lentz, B. R. (1985),Biophys. J. 48, 221.

    PubMed  CAS  Google Scholar 

  32. Mourtisen, O. G. and Zuckermann, M. J. (1987),Chem. Phys. Lett. 135, 294.

    Article  Google Scholar 

  33. Helm, C. A., Möhwald, H., Kjaer, K., and Als-Nielsen, J. (1987),Biophys. J. 52, 381.

    PubMed  CAS  Google Scholar 

  34. Ipsen, J. H., Karlström, G., Mouritsen, O. G., Wennerström, H., and Zuckermann, M. J. (1987),Biochem. Biophys. Acta 905, 162.

    Article  PubMed  CAS  Google Scholar 

  35. Abney, J. R. and Owicki, J. O. (1985), in Ref. 1. pp. 1–60.

    Google Scholar 

  36. Bloom, M. (1979),Can. J. Phys. 57, 2227.

    CAS  Google Scholar 

  37. Mouritsen, O. G., and Bloom, M. (1984),Biophys. J.,46, 141.

    Article  PubMed  CAS  Google Scholar 

  38. Sperotto, M. M. and Mouritsen, O. G. (1988),Eur. Biophys. J. 16, 1.

    Article  CAS  Google Scholar 

  39. Tanford, C. (1973),The Hydrophobic Effect. Formation of Micelles and Biological Membranes, Wiley, New York.

    Google Scholar 

  40. Silvius, J. R. (1982),Lipid-Protein Interactions, vol. 2, (P. C. Jost, and O. H. Griffith), Wiley-Interscience, New York, pp. 239–281.

    Google Scholar 

  41. Kyte, J. and Doolittle, R. F. (1982),J. Mol. Biol. 157, 105.

    Article  PubMed  CAS  Google Scholar 

  42. Jähnig, F. (1986),Eur. Biophys. J. 14, 63.

    Article  PubMed  Google Scholar 

  43. Braun, J., Abney, J. R., and Owicki, J. C. (1987),Biophys. J. 52, 427, 441.

    PubMed  CAS  Google Scholar 

  44. Riegler, J. and Möhwald, H. (1986),Biophys. J. 49, 1111.

    CAS  PubMed  Google Scholar 

  45. Peschke, J., Riegler, J., and Möhwald, H. (1987),Eur. Biophys. J. 14, 385.

    Article  CAS  Google Scholar 

  46. Williams, J. C., Steiner, L. A., Ogden, R. C., Simon, M. I., and Feher, G. (1983),Proc. Natl. Acad. Sci. USA 80, 6505; Williams, J. C., Steiner, L. A., Feher, G., and Simon, M. I. (1984),Proc. Natl. Acad. Sci. USA 81, 7303.

    Article  PubMed  CAS  Google Scholar 

  47. McElhaney, R. N. (1982),Chem. Phys. Lipids 30, 229.

    Article  PubMed  CAS  Google Scholar 

  48. Morrow, M. R., Davis, J. H., Sharom, F. J., and Lamb, M. P. (1986),Biochim. Biophys. Acta 858, 13.

    Article  PubMed  CAS  Google Scholar 

  49. Morrow, M. R., Huschilt, J. C., and Davis, J. H. (1985),Biochemistry 24, 5396.

    Article  PubMed  CAS  Google Scholar 

  50. Zuber, H. (1985),Antenma and Reaction Centers of Photosynthetic Bacteria, Springer Series in Chemical Physics, vol. 42, Springer Verlag, Heidelberg, FRG, pp. 2–14.

    Google Scholar 

  51. Jay, D. and Cantley, L. (1986),Ann. Rev. Biochem. 55, 511.

    Article  PubMed  CAS  Google Scholar 

  52. Kopito, R. R. and Lodish, H. F. (1985),Nature 316, 234.

    Article  PubMed  CAS  Google Scholar 

  53. Presti, F. T. in Ref. 22, Aloia, R. C. and Boggs, J. M. eds., (1985),Membrane Fluidity in Biology, vol. 4, Academic, New York. pp. 97–146.

  54. Vist, M. R. (1984), M.Sc. Thesis, University of Guelph, Ontario, Canada.

  55. Davis, J. H. (1988),Proc. Int. School. ‘Enrico Fermi’ on Medical Applications of NMR, Varenna (in press).

  56. Evans, E. and Needham, D. (1986),Faraday Discuss. Chem. Soc. 81, 267.

    Article  PubMed  CAS  Google Scholar 

  57. Yeagle, P. L. (1985),Biochim. Biophys. Acta 822, 267.

    PubMed  CAS  Google Scholar 

  58. Maraviglia, B., Davis, J. H., Bloom, M., Westerman, J., and Wirtz, K. W. A. (1982),Biochim. Biophys. Acta 686, 137.

    Article  PubMed  CAS  Google Scholar 

  59. Jähnig, F. (1981),Biophys. J. 36, 347.

    PubMed  Google Scholar 

  60. Cherry, R. J., Müller, U., Holenstein, C., and Heyn, M. P. (1980),Biochim. Biophys. Acta 596, 145.

    Article  PubMed  CAS  Google Scholar 

  61. Lewis, B. A. and Engelman, D. M. (1983),J. Mol. Biol. 166, 203.

    Article  PubMed  CAS  Google Scholar 

  62. Uzgiris, E. E. and Kornberg, R. D. (1983),Nature 301, 125.

    Article  PubMed  CAS  Google Scholar 

  63. Pink, D. A. (1984),Can. J. Biochem. Cell Biol. 62, 760.

    Article  PubMed  CAS  Google Scholar 

  64. Lookman, T., Pink, D. A., Grundke, E. W., Zuckermann, M. J., and de Verteuil, F. (1982),Biochemistry 21, 5593.

    Article  PubMed  CAS  Google Scholar 

  65. Tessier-Lavigne, M., Boothroyd, A., Zuckermann, M. J., and Pink, D. A. (1982),J. Chem. Phys. 76, 4587.

    Article  CAS  Google Scholar 

  66. MacDonald, A. L. and Pink, D. A. (1987),Biochemistry 26, 1909.

    Article  PubMed  CAS  Google Scholar 

  67. Laidlaw, D. J. and Pink, D. A. (1985),Eur. Biophys. J. 12, 143.

    Article  PubMed  CAS  Google Scholar 

  68. Johannsson, A., Keightley, C. A., Smith, G. A., Richards, C. D., Hesketh, T. R., and Metcalfe, J. C. (1981),J. Biol. Chem. 256, 1643.

    PubMed  CAS  Google Scholar 

  69. East, J. M., Jones, O. T., Simmonds, A. C., and Lee, A. G. (1984),J. Biol. Chem. 259, 8070.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Structural Properties of Materials, The Technical University of Denmark, Building 307, DK-2800, Lyngby, Denmark

    Maria M. Sperotto, John Hjort Ipsen & Ole G. Mouritsen

Authors
  1. Maria M. Sperotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John Hjort Ipsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ole G. Mouritsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Paper presented to the International School of Pure and Applied Biostructure, Erice, Italy, Oct. 4–10, 1987

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sperotto, M.M., Ipsen, J.H. & Mouritsen, O.G. Theory of protein-induced lateral phase separation in lipid membranes. Cell Biophysics 14, 79–95 (1989). https://doi.org/10.1007/BF02797393

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02797393

Index Entries

Search

Navigation