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Lipids on the frontier: a century of cell-membrane bilayers

Nature Reviews Molecular Cell Biology volume 4, pages 414–418 (2003)Cite this article

Abstract

Our present picture of cell membranes as lipid bilayers is the legacy of a century's study that concentrated on the lipids and proteins of cell-surface membranes. Recent work is changing the picture and is turning the snapshot into a video.

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Figure 1: The unit membrane concept.
Figure 2: The fluid mosaic membrane of Singer and Nicholson.
Figure 3: Membrane domains.

References

  1. Overton E. The probable origin and physiological significance of cellular osmotic properties. Vierteljahrschrift der Naturforschende Gesselschaft (Zurich) 44, 88–135 (1899). Trans. Park, R. B. in Biological Membrane Structure (eds Branton, D. & Park, R. B.) 45–52 (Little, Brown & Co., Boston, 1968).

    Google Scholar 

  2. Robertson, J. D. The ultrastructure of cell membranes and their derivatives. Biochem. Soc. Symp. 16, 3–43 (1959).

    CAS  PubMed  Google Scholar 

  3. Fricke, H. The electric capacity of cell suspensions. Phys. Rev. Series II, 21, 708–709 (1923).

    Google Scholar 

  4. Danielli, J. F. & Harvey, E. N. The tension at the surface of mackerel egg oil, with remarks on the nature of the cell surface. J. Cell. Comp. Physiol. 5, 483 (1935).

    Article  CAS  Google Scholar 

  5. Cole, K. S. Surface forces of the Arbacia egg. J. Cell. Comp. Physiol. 1, 1–9 (1932).

    Article  Google Scholar 

  6. Danielli, J. F. & Davson, H. A contribution to the theory of permeability of thin films. J. Cell. Physiol. 5, 495–508 (1935).

    Article  CAS  Google Scholar 

  7. Langmuir, I. The constitution and fundamental properties of solids and liquids. II. Liquids. J. Amer. Chem. Soc. 39, 1848–1906 (1917).

    Article  CAS  Google Scholar 

  8. Gorter, E. & Grendel, F. On bimolecular layers of lipoids on the chromocytes of the blood. J. Exp. Med. 41, 439–443 (1925).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Deamer, D. W. & Cornwell, D. G. Surface area of human erythrocytes: reinvestigation of experiments on plasma membrane. Science 153, 1010–1012 (1966).

    Article  PubMed  Google Scholar 

  10. Stoeckenius, W. & Engelman, D. M. Current models for the structure of biological membranes. J. Cell Biol. 42, 613–646 (1969).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bretscher, M. S. Membrane structure: some general principles. Science 181, 622–629 (1973).

    Article  CAS  PubMed  Google Scholar 

  12. Fernandez-Morán, H. & Finean, J. B. Electron microscope and low-angle x-ray diffraction studies of the nerve myelin sheath. J. Cell Biol. 3, 725–748 (1957).

    Article  Google Scholar 

  13. Blasie, J. K. & Worthington, C. R. Planar liquid-like arrangement of photopigment molecules in frog retinal receptor disk membranes. J. Mol. Biol. 39, 417–439 (1969).

    Article  CAS  PubMed  Google Scholar 

  14. Chapman, D. Phase transitions and fluidity characteristics of lipids and cell membranes. Quart. Rev. Biophys. 8, 185–235 (1975).

    Article  CAS  Google Scholar 

  15. Frye, L. D. & Edidin, M. The rapid intermixing of cell surface antigens after formation of mouse–human heterokaryons. J. Cell Sci. 7, 319–335 (1970).

    CAS  PubMed  Google Scholar 

  16. Cone, R. A. Rotational diffusion of rhodopsin in the visual receptor membrane. Nature New Biol. 15, 39–43 (1972).

    Article  Google Scholar 

  17. Poo, M. & Cone, R. A. Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature 247, 438–441 (1974).

    Article  CAS  PubMed  Google Scholar 

  18. Fairbanks, G., Steck T. L. & Wallach, D. F. H. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochem. 10, 2606–2617 (1971).

    Article  CAS  Google Scholar 

  19. Singer S. J. & Nicolson, G. L. The fluid mosaic model of cell membranes. Science 175, 720–731 (1972).

    Article  CAS  PubMed  Google Scholar 

  20. Tanford C. The hydrophobic effect and living matter. Science 200, 1012–1018 (1978).

    Article  CAS  PubMed  Google Scholar 

  21. Tomita, M., Furthmayr, H. & Marchesi, V. T. Primary structure of human erythrocyte glycophorin A. Isolation and characterization of peptides and complete amino acid sequence. Biochemistry 17, 4756–4770 (1978).

    Article  CAS  PubMed  Google Scholar 

  22. Killian J. A. & von Heijne, G. How proteins adapt to a membrane–water interface. Trends Biochem. Sci. 25, 429–434 (2000).

    Article  CAS  PubMed  Google Scholar 

  23. Smith, R. L. & Oldfield E. Dynamic structure of membranes by deuterium NMR. Science 222, 280–288 (1984).

    Article  Google Scholar 

  24. Edidin, M. Rotational and translational diffusion in membranes. Annu. Rev. Biophys. Bioeng. 3, 179–201 (1974).

    Article  CAS  PubMed  Google Scholar 

  25. Gupte, S. et al. Relationship between lateral diffusion, collision frequency, and electron transfer of mitochondrial inner membrane oxidation–reduction components. Proc. Natl Acad. Sci. USA 81, 2606–2610 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Jans, D. A. The Mobile Receptor Hypothesis: The Role Of Membrane Receptor Lateral Movement In Signal Transduction (RG Landes Bioscience Austin, Texas, 1997).

    Book  Google Scholar 

  27. Jain, M. K. & White, H. B. 3rd. Long range order in biomembranes. Adv. Lipid Res. 15, 1–60 (1977).

    Article  CAS  PubMed  Google Scholar 

  28. Wolf, D. E., Kinsey, W., Lennarz, W. & Edidin, M. Changes in the organization of the sea urchin egg plasma membrane upon fertilization: indications from lateral diffusion rates of lipid-soluble fluorescent dyes. Dev. Biol. 81, 133–138 (1981).

    Article  CAS  PubMed  Google Scholar 

  29. Yechiel, E. & Edidin, M. Micrometer scale domains in fibroblast plasma membranes. J. Cell Biol. 105, 755–760 (1987).

    Article  CAS  PubMed  Google Scholar 

  30. Edidin, M. Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7, 528–532 (1997).

    Article  CAS  PubMed  Google Scholar 

  31. Edidin, M. Shrinking patches and slippery rafts: scales of domains in the plasma membrane. Trends Cell Biol. 11, 492–496 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Simons, K. & van Meer, G. Lipid sorting in epithelial cells. Biochemistry 27, 6197–6202 (1988).

    Article  CAS  PubMed  Google Scholar 

  33. Rodriguez-Boulan, E. & Nelson, W. J. Morphogenesis of the polarized epithelial cell phenotype. Science 245, 718–725 (1989).

    Article  CAS  PubMed  Google Scholar 

  34. Brown, D. A. & Rose, J. K. Sorting of GPI-anchored proteins to glycolipids-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533–544 (1992).

    Article  CAS  PubMed  Google Scholar 

  35. Edidin, M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomolec. Struct. 2003 Jan 16 [epub ahead of print].

  36. Simons, K. & Ikonnen, E. Functional rafts in cell membranes. Nature 389, 569–572 (1997).

    Article  Google Scholar 

  37. Saxton, M. J. & Jacobson, K. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26, 373–399 (1997).

    Article  CAS  PubMed  Google Scholar 

  38. Gheber, L. A. & Edidin, M. A model for membrane patchiness: lateral diffusion in the presence of barriers and vesicle traffic. Biophys. J. 77, 3163–3175 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Steinman, R. M., Mellman, I. S., Muller, W. A. & Cohn, Z. A. Endocytosis and the recycling of plasma membrane. J. Cell Biol. 96, 1–27 (1983).

    Article  CAS  PubMed  Google Scholar 

  40. Axelrod, D. Total internal reflection fluorescence microscopy in cell biology. Traffic 2, 764–774 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Steck, T. L. The organization of proteins of the human red blood cell membrane, a review. J. Cell Biol. 62, 1–19 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. D'Onofrio, T. G. et al. Controlling and measuring the interdependence of local properties in biomembranes. Langmuir 19, 1618–1623 (2003).

    Article  CAS  Google Scholar 

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Acknowledgements

I would like to thank R. A. Cone (Department of Biophysics, Johns Hopkins University, USA) for years of collegial discussions and for access to his file of classic papers in membrane biology, many of which were the subject of a memorable seminar in membranes over 30 years ago.

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  1. the Department of Biology, Johns Hopkins University, 3400 North Charles Street, Baltimore, 21218, Maryland, USA

    Michael Edidin

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Contributions of 20th century women to physics: Agnes Pockels

Michael Edidin's laboratory

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Edidin, M. Lipids on the frontier: a century of cell-membrane bilayers. Nat Rev Mol Cell Biol 4, 414–418 (2003). https://doi.org/10.1038/nrm1102

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