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Cell Biochemistry and Biophysics

, Volume 41, Issue 3, pp 391–414 | Cite as

Optical techniques for imaging membrane topography

  • Raghuveer Parthasarathy
  • Jay T. Groves
Review Article

Abstract

In recent years three powerful optical imaging techniques have emerged that provide nanometer-scale information about the topography of membrane surfaces, whether cellular or artificial: intermembrane fluorescence resonance energy transfer (FRET), fluorescence interference contrast microscopy (FLIC), and reflection interference contrast microscopy (RICM). In intermembrane FRET, the sharp distance dependence of resonant energy transfer between fluorophores allows topographic measurements in the Ångstrom to few-nanometer range. In FLIC and RICM, interference between light from a membrane (either from fluorescent probes, or reflected illumination) and light reflected by a planar substrate provide spatial sensitivity in the few to hundreds of nanometer range, with few-nanometer resolution. All of these techniques are fairly easy to implement. We discuss the physics and optics behind each of these tools, as well as practical concerns regarding their uses. We also provide examples of their application in imaging molecular-scale structures at intermembrane junctions.

Index Entries

Membrane topography interference contrast microscopy FRET FLIC RICM 

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References

  1. 1.
    Simon, S. I. and Goldsmith, H. L. (2002) Leukocyte adhesion dynamics in shear flow. Ann. Biomed. Eng. 30, 315–332.PubMedCrossRefGoogle Scholar
  2. 2.
    Dworak, H. A. and Sink, H. (2002) Myoblast fusion in Drosophila. BioEssays 24, 591–601.PubMedCrossRefGoogle Scholar
  3. 3.
    Gilbert, S. F. (2000) Developmental Biology, 6th ed. Sinauer, Sunderland, MA.Google Scholar
  4. 4.
    Singer, S. J. (1992) Intercellular communication and cell-cell adhesion. Science 255, 1671–1677.PubMedCrossRefGoogle Scholar
  5. 5.
    Dustin, M. L. and Colman, D. R. (2002) Neural and immunological synaptic relations. Science 29, 785–789.CrossRefGoogle Scholar
  6. 6.
    Grakoui, A., Bromley, S. K., Sumen, C., Davis, M. M., Shaw, A. S., Allen, P. M., et al. (1999) The immunological synapse: a molecular machine controlling T-cell activation. Science 285, 221–227.PubMedCrossRefGoogle Scholar
  7. 7.
    Weber, I. (2003) Reflection interference contrast microscopy. Meth. Enzymol. 361, 34–47.PubMedGoogle Scholar
  8. 8.
    Wiegand, G., Neumaier, K. R., and Sackmann, E. (1998) Microinterferometry: three-dimensional reconstruction of surface microtopography for thin-film and wetting studies by reflection interference contrast microscopy (RICM). Appl. Opt. 37, 6892–6905.PubMedGoogle Scholar
  9. 9.
    Axelrod, D., Hellen, E. H., and Fulbright, R. M. (1992) Total internal reflection fluorescence, in Topics in Fluorescence Spectroscopy, vol. 3 (Lakowicz, J. R., ed.), Plenum, New York.Google Scholar
  10. 10.
    Thompson, N. L., Drake, A. W., Chen, L., and Vanden Broek, W. (1997) Equilibrium, kinetics, diffusion and self-association of proteins at membrane surfaces: measurement by total internal reflection fluorescence microscopy. Photochem. Photobiol. 65, 39–46.PubMedGoogle Scholar
  11. 11.
    Ajo-Franklin C. M., Kam, L., and Boxer, S. G. (2001) High refractive index substrates for fluorescence microscopy of biological interfaces with high z contrast. Proc. Natl. Acad. Sci. USA 98, 13643–13648.PubMedCrossRefGoogle Scholar
  12. 12.
    Selvin, P. R. (2000) The renaissance of fluorescence resonance energy transfer. Nat. Struct. Biol. 7, 730–734.PubMedCrossRefGoogle Scholar
  13. 13.
    Clegg, R. M. (1995) Fluorescence resonance energy transfer. Curr. Op. Biotech. 6, 103–110.CrossRefGoogle Scholar
  14. 14.
    Clegg, R. M. (1996) Fluorescence resonance energy transfer, in Fluorescence Imaging Spectroscopy and Microscopy (Wang, X. F. and Herman, B., ed.), John Wiley & Sons, New York.Google Scholar
  15. 15.
    Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, Kluwer Academic/Plenum, New York.Google Scholar
  16. 16.
    Periasami, A. (2001) Fluorescence resonance energy transfer microscopy: a mini-review. J. Biomed. Opt. 6, 287–291.CrossRefGoogle Scholar
  17. 17.
    Wu, P. and Brand, L. (1994) Resonance energy transfer: methods and applications. Anal. Biochem. 218, 1–13.PubMedCrossRefGoogle Scholar
  18. 18.
    Förster, T. (1948) Zwischenmolekulare energiewanderung und fluoreszenz. Ann. Physik. 2, 55–75.CrossRefGoogle Scholar
  19. 19.
    Förster, T. (1959) Transfer mechanisms of electronic excitation. Discuss. Faraday Soc. 27, 7–17.CrossRefGoogle Scholar
  20. 20.
    Förster, T. (1965) Delocalized excitation and excitation transfer, in Modern Quantum Chemistry, vol. 3 (Sinanoglu, O., ed.), Academic Press, New York.Google Scholar
  21. 21.
    Kuhn, H. (1971) Classical aspects of energy transfer in molecular systems. J. Chem. Phys. 53, 101–108.CrossRefGoogle Scholar
  22. 22.
    Stryer, L. and Haugland, R. P. (1967) Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. USA 58, 719–726.PubMedCrossRefGoogle Scholar
  23. 23.
    Stryer, L. (1978) Fluorescence resonance energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47, 819–846.PubMedCrossRefGoogle Scholar
  24. 24.
    Clegg, R. M., Murchie, A. I. H., Zechel, A., and Lilley, D. M. J. (1993) Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 90, 2994–2998.PubMedCrossRefGoogle Scholar
  25. 25.
    Mergny, J.-L., Boutorine, A. S., Garestier, T., Belloc, G., Rougé, M., Bulychev, N. V., et al. (1994) Fluorescence resonance energy transfer as a probe for nucleic acid structures and sequences. Nucleic Acids Res. 22, 920–928.PubMedCrossRefGoogle Scholar
  26. 26.
    Suzuki, Y., Yasunaga, T., Ohkura, R., Wakabayashi, T., and Sutoh, K. (1998) Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396, 380–383.PubMedCrossRefGoogle Scholar
  27. 27.
    Sadqi, M., Lapidus, L. J., and Muñoz, V. (2003) How fast is protein hydrophobic collapse?. Proc. Natl. Acad. Sci. USA 100, 12117–12122.PubMedCrossRefGoogle Scholar
  28. 28.
    Corbalan-Garcia, S., Teruel, J. A., and Gomez-Fernandez, J. C. (1993) Intramolecular distances within the Ca2+-ATPase from sarcoplasmic reticulum as estimated through fluorescence energy transfer between probes. Eur. J. Biochem. 217, 737–744.PubMedCrossRefGoogle Scholar
  29. 29.
    Baker, K. J., East, J. M., and Lee, A. C. (1994) Localization of the hinge region of the Ca2+-ATPase of sarcoplasmic reticulum using resonance energy transfer. Biochim. Biophys. Acta 1192, 53–60.PubMedCrossRefGoogle Scholar
  30. 30.
    Miyawaki, A. and Tsien, R. Y. (2000). Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Meth. Enzym. 327, 472–500.PubMedCrossRefGoogle Scholar
  31. 31.
    Varma, R. and Mayor, S. (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798–801.PubMedCrossRefGoogle Scholar
  32. 32.
    Kenworthy, A. K., Petranova, N., and Edidin, M. (2000) High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol. Biol. Cell 11, 1645–1655.PubMedGoogle Scholar
  33. 33.
    Niles, W. D., Silvius, J. R., and Cohen, F. S. (1996) Resonance energy transfer imaging of phospholipid vesicle interaction with a planar phospholipid membrane: undulations and attachment sites in the region of calcium-mediated membrane-membrane adhesion. J. Gen. Physiol. 107, 329–351.PubMedCrossRefGoogle Scholar
  34. 34.
    Wong, A. P. and Groves, J. T. (2001) Topographical imaging of an intermembrane junction by combined fluorescence interference and energy transfer microscopies. J. Am. Chem. Soc. 123, 12414–12415.PubMedCrossRefGoogle Scholar
  35. 35.
    Wong, A. P. and Groves, J. T. (2002) Molecular topography imaging by intermembrane fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 99, 14147–14152.PubMedCrossRefGoogle Scholar
  36. 36.
    Sackmann, E. (1996) Supported membranes: scientific and practical applications. Science 271, 43–48.PubMedCrossRefGoogle Scholar
  37. 37.
    Boxer, S. G. (2000) Molecular transport and organization in supported lipid membranes. Curr. Opin. Chem. Biol. 4, 704–709.PubMedCrossRefGoogle Scholar
  38. 38.
    Groves, J. T. and Boxer, S. G. (2002) Micropattern formation in supported lipid membranes. Acc. Chem. Res. 35, 149–157.PubMedCrossRefGoogle Scholar
  39. 39.
    Merritt, E. A., Sarfaty, S., Akker, F. V. D., L'Hoir, C., Martial, J. A., and Hol, W. G. J. (1994) Crystal structure of cholera toxin B-pentamer bound to receptor G(M1) pentasaccharide. Protein Sci. 3, 166–175.PubMedCrossRefGoogle Scholar
  40. 40.
    Parthasarathy, R. and Groves, J. T. (2004) Nonequilibrium adhesion patterns at lipid bilayer junctions. J. Phys. Chem. B. 108, 649–657.CrossRefGoogle Scholar
  41. 41.
    Kaizuka, Y. and Groves, J. T. (2004) Structure and dynamics of supported intermembrane junctions. Biophys. J. 86, 905–912.PubMedCrossRefGoogle Scholar
  42. 42.
    Zeck, G. and Fromherz, P. (2003) Repulsion and attraction by extracellular matrix protein in cell adhesion studied with nerve cells and lipid vesicles on silicon chips. Langmuir 19, 1580–1585.CrossRefGoogle Scholar
  43. 43.
    Iwanaga, Y., Braun, D., and Fromherz, P. (2001) No correlation of focal contacts and close adhesion by comparing GFP-vinculin and fluorescence interference of DiI. Eur. Biophys. J. 30, 17–26.PubMedCrossRefGoogle Scholar
  44. 44.
    Kiessling, V., and Tamm, L. K. (2003) Measuring distances in supported bilayers by fluorescence interference-contrast microscopy: polymer supports and SNARE proteins. Biophys. J. 84, 408–418.PubMedGoogle Scholar
  45. 45.
    Lambacher, A. and Fromherz, P. (1996) Fluorescence interference-contrast microscopy on oxidized silicon using a monomolecular dye layer. Appl. Phys. A 63, 207–216.CrossRefGoogle Scholar
  46. 46.
    Braun, D. and Fromherz, P. (1997) Fluorescence interference contrast microscopy of cell adhesion on silicon. Appl. Phys. A 65, 341–348.CrossRefGoogle Scholar
  47. 47.
    Lambacher, A. and Fromherz, P. (2002) Luminescence of dye molecules on oxidized silicon and fluorescence interference contrast microscopy of biomembranes. J. Opt. Soc. Am. B 19, 1435–1453.Google Scholar
  48. 48.
    Jellison, G. E. and Modine, F.A. (1982) Optical constants for silicon at 300 and 10 K determined from 1.64 to 4.73 eV by ellipsometry. J. Appl. Phys. 53, 3745–3753.CrossRefGoogle Scholar
  49. 49.
    Landolt, H. and Börnstein, R. (1962). Numerical Data and Functional Relationships in Science and Technology, 6th ed., Vol. 2, Springer, Berlin.Google Scholar
  50. 50.
    Swan, A. K., Moiseev, L. A., Cantor, C. R., Davis, B., Ippolito, S. B., Karl, W. C., et al. (2003) Toward nanometer-scale resolution in fluorescence microscopy using spectral self-interference. IEEE J. Sel. Top. Quantum Electron. 9, 294–300.CrossRefGoogle Scholar
  51. 51.
    Eah, S.-K., Jaeger, H. M., Scherer, N. F., Wiederrecht, G. P., and Lin, X.-M. (manuscript in preparation).Google Scholar
  52. 52.
    Medhage, B., Mukhtar, E., Kalman, B., Johansson, L., and Molotkovsky, J. G. (1992) J. Chem. Soc. Faraday Trans. 88, 2845–2841.CrossRefGoogle Scholar
  53. 53.
    Nardi, J., Bruinsma, R., and Sackmann, E. (1998) Adhesion-induced reorganization of charged fluid membranes. Phys. Rev. E 58, 6340–6354.CrossRefGoogle Scholar
  54. 54.
    Gu, M. (2000) Advanced Optical Imaging Theory, Springer, Heidelberg.Google Scholar
  55. 55.
    Parthasarathy, R. and Groves, J. T. (2004) Protein patterns at lipid bilayer junctions. Proc. Natl. Acad. Sci. USA 101, 12,798–12,803.CrossRefGoogle Scholar
  56. 56.
    Curtis, A. S. G. (1964) The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J. Cell Biol. 20, 199–215.PubMedCrossRefGoogle Scholar
  57. 57.
    Ploem, J. S. (1975). Reflection contrast microscopy as a tool for investigation of the attachment of living cells to a glass surface, in Mononuclear Phagocytes in Immunity Infection and Pathology (van Furth, R., ed.), Blackwell, Oxford.Google Scholar
  58. 58.
    Rädler, J. and Sackmann, E. (1993) Imaging optical thicknesses and separation distances of phospholipid vesicles at solid surfaces. J. Phys. II France 3, 727–748.CrossRefGoogle Scholar
  59. 59.
    Verschueren, H. (1985) Interference reflection microscopy in cell biology: methodology and applications. J. Cell. Sci. 75, 279–301.PubMedGoogle Scholar

Copyright information

© Humana Press Inc 2004

Authors and Affiliations

  1. 1.Department of ChemistryUniversity of CaliforniaBerkeley

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