Skip to main content
Log in

Flicker in erythrocytes. I. Theoretical models and registration techniques

  • Reviews
  • Published:
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

The phenomenon of stochastic low-frequency oscillations of erythrocyte cell membrane, termed usually the flicker of erythrocytes, is reviewed. The first part describes the theoretical models of erythrocyte flickering and the registration techniques. The relations are given and analyzed which connect the shape of both the frequency and the spatial spectra of stochastic membrane oscillations with geometrical and mechanical parameters of the erythrocyte and with the ambient physical characteristics. The existing concepts of excitation mechanisms of the membrane flickering are presented.

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

Access this article

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. Brohard, F. and Lennon, J.F., Frequency Spectrum of the Flicker Phenomenon in Erythrocytes, J. Phys. (Fr.), 1975, vol. 36, no. 11, pp. 1035–1047.

    Article  Google Scholar 

  2. Zeman, K., Engelhard, H., and Sackmann E. Bending Undulations and Elasticity of the Erythrocyte Membrane: Effects of Cell Shape and Membrane Organization, Eur. Biophys. J., 1990, vol. 18, no. 4, pp. 203–219.

    Article  PubMed  CAS  Google Scholar 

  3. Tishler, R.B. and Carlson, F.D., A Study of Dynamic Properties of the Human Red Blood Cell Membrane Using Quasi-Elastic Light-Scattering Spectroscopy, Biophys. J., 1993, vol. 65, no. 6, pp. 2586–2600.

    Article  PubMed  CAS  Google Scholar 

  4. Strey, H., Peterson, M., and Sackmann, E., Measurement of Erythrocyte Membrane Elasticity by Flicker Eigenmode Decomposition, Biophys. J., 1995, vol. 69, no. 2, pp. 478–488.

    Article  PubMed  CAS  Google Scholar 

  5. Rytov, C.M., Vvedenie v statisticheskuyu radiofiziku (Introduction to Statistical Radiophysics), Moscow, Nauka, 1966.

    Google Scholar 

  6. Hoffman, E.K. and Simonsen, L.O., Membrane Mechanisms in Volume and pH Regulation in Vertebrate Cells, Physiological Reviews, 1989, vol. 69, no. 2, pp. 315–382.

    Google Scholar 

  7. Mohandas, N. and Evans, E., Mechanical Properties of the Red Cell Membrane in Relation to Molecular Structure and Genetic Defects, Annu. Rev. Biophys. Biomol. Struct., 1994, vol. 23, pp. 787–818.

    Article  PubMed  CAS  Google Scholar 

  8. Evans, E.A. and Skalak, R., Mechanics and Thermodynamics of Biomembranes, Boca Raton, Florida, CRC-Press, 1980.

    Google Scholar 

  9. Kozlov, M.M. and Markin, V.S., Membrane Skeleton of Erythrocyte. The Theoretical Model, Biologicheskie Membrany (Rus.), 1986, vol. 3, no. 4, pp. 404–422.

    CAS  Google Scholar 

  10. Gov, N., Zilman, A.G., and Safran, S., Cytoskeleton Confinement and Tension of Red Blood Cell Membranes, Phys. Rev. Lett., 2003, vol. 90, no. 22, p. 228101.

    Article  PubMed  CAS  Google Scholar 

  11. Gov, N. and Safran, S.A., Pinning of Fluid Membranes by Periodic Harmonic Potentials, Phys. Rev. E., 2004, vol. 69, no. 1, p. 011101(10).

    Article  CAS  Google Scholar 

  12. Fournier, J.-B., Lacoste, D., and Raphael, E., Fluctuation Spectrum of Fluid Membranes Coupled to an Elastic Meshwork: Jump of the Effective Surface Tension at the Mesh Size, Phys. Rev. Lett., 2004, vol. 92, no. 1, p. 018102.

    Article  PubMed  CAS  Google Scholar 

  13. Gov, N.S. and Safran, S.A., Red Blood Cell Membrane Fluctuations and Shape Controlled by ATP-Induced Cytoskeletal Defects, Biophys. J., 2005, vol. 88, no. 3, pp. 1859–1874.

    Article  PubMed  CAS  Google Scholar 

  14. Zhang, R. and Brown, F.L.H., Cytoskeleton Mediated Effective Elastic Properties of Model Red Blood Cell Membranes, J. Chem Phys., 2008, vol. 129, no. 6, p. 065101(14).

    Google Scholar 

  15. Lenormand, G., Henon, S., Richert, A., Simeon, J., and Gallet, F., Direct Measurement of the Area Expansion and Shear Moduli of the Human Red Blood Cell Membrane Skeleton, Biophys. J., 2001, vol. 81, no. 1, pp. 43–56.

    Article  PubMed  CAS  Google Scholar 

  16. Manno, S., Takakuwa, Y., Nagao, K., and Mohandas, N., Modulation of Erythrocyte Membrane Mechanical Function by Beta-Spectrin Phosphorylation and Dephosphorylation, J. Biol. Chem., 1995, vol. 270, no. 10, pp. 5659–5665.

    Article  PubMed  CAS  Google Scholar 

  17. Manno, S., Takakuwa, Y., and Mohandas, N., Modulation of Erythrocyte Membrane Mechanical Function by Protein 4.1 Phosphorylation, J. Biol. Chem., 2005, vol. 280, no. 9, pp. 7581–7587.

    Article  PubMed  CAS  Google Scholar 

  18. Henon, S., Lenormand, G., Richert, A., and Gallet, F., A New Determination of the Shear Modulus of the Human Erythrocyte Membrane Using Optical Tweezers, Biophys. J., 1999, vol. 76, no. 2, pp. 1145–1151.

    Article  PubMed  CAS  Google Scholar 

  19. Lenormand, G., Henon, S., Richert, A., Simeon, J., and Gallet, F., Elasticity of the Human Red Blood Cell Skeleton, Biorheology, 2003, vol. 40, nos. 1–3, pp. 247–251.

    PubMed  CAS  Google Scholar 

  20. Schneider, M.B., Jenkins, J.T., and Webb, W.W., Thermal Fluctuations of Large Quasi-Spherical Bimolecular Phospholipid Vesicles, J. de Physique, 1984, vol. 49, no. 9, pp. 1457–1472.

    Article  Google Scholar 

  21. Milner, S.T. and Safran, S.A., Dynamic Fluctuations of Droplets Microemulsions and Vesicles, Phys. Rev. A., 1987, vol. 36, no. 9, pp. 4371–4379.

    Article  PubMed  CAS  Google Scholar 

  22. Peterson, M.A., Shape Dynamics of Nearly Spherical Membrane Bounded Fluid Cells, Molecular Crystals and Liquid Crystals, 1985, vol. 127, nos. 1–4, pp. 257–272.

    Article  CAS  Google Scholar 

  23. Peterson, M.A., Shape Fluctuations of Red Blood Cells, Molecular Crystals and Liquid Crystals, 1985, vol. 127, nos. 1–4, pp. 159–186.

    Article  Google Scholar 

  24. Frey, E. and Nelson, D.R., Dynamics of Flat Membranes and Flickering in Red Blood Cells, J. Phys. I France., 1991, vol. 1, no. 12, pp. 1715–1757.

    Article  CAS  Google Scholar 

  25. Kononenko, V.L. and Shimkus, Ya.K., Coherent and Noncoherent Optical Probing of Dynamic Fluctuations of Erythrocyte Shape, Izvestiya Rossiiskoi Akademii Nauk. Seriya Fizicheskaya (Rus.), 1999, vol. 63, no. 6, pp. 1166–1172. [Engl. Transl.: Bulletin of the Russian Academy of Sciences. Physics, 1999, vol. 63, no. 6, pp. 927–932.]

    CAS  Google Scholar 

  26. Rochal, S.B. and Lorman, V.L., Cytoskeleton Influence on Normal and Tangent Fluctuation Modes in the Red Blood Cells, Phys. Rev. Lett., 2006, vol. 96, no. 24, p. 248102(4).

    Article  CAS  Google Scholar 

  27. Kononenko, V.L. and Shimkus, J.K., Coherent Versus Noncoherent Optical Probing of Dynamic Shape Fluctuations in Red Blood Cells, Proceedings of SPIE, 1999, vol. 3732, pp. 326–335.

    Article  Google Scholar 

  28. Kononenko, V.L., Dielectro-Deformations and Flicker of Erythrocytes: Fundamental Aspects of Medical Diagnostics Applications, Proceedings of SPIE, 2002, vol. 4707, pp. 134–143.

    Article  Google Scholar 

  29. Kononenko, V.L., Flicker Spectroscopy of Erythrocytes: A Comparative Study of Several Theoretical Models, Proceedings of SPIE, 1994, vol. 2082, pp. 236–247.

    Article  Google Scholar 

  30. Dubus, C. and Fournier, J.-B., A Gaussian Model for the Membrane of Red Blood Cells with Cytoskeletal Defects, Europhysics Letters, 2006, vol. 75, no. 1, pp. 181–187.

    Article  CAS  Google Scholar 

  31. Peterson, M.A., Strey, H., and Sackmann, E., Theoretical and Phase Contrast Microscopic Eigenmode Analysis of Erythrocyte Flicker Amplitudes, J. Phys. (Fr.). II, 1992, vol. 2, no. 5, pp. 1273–1285.

    Article  Google Scholar 

  32. Prost, J. and Bruinsma, R., Shape Fluctuations of Active Membranes, Europhysics Letters, 1996, vol. 33, no. 4, pp. 321–326.

    Article  CAS  Google Scholar 

  33. Manneville, J.-B., Bassereau, P., Ramaswamy, S., and Prost, J., Active Membrane Fluctuations Studied by Micropipet Aspiration, Phys. Rev. E, 2001, vol. 64, no. 2, p. 021908(10).

    Article  CAS  Google Scholar 

  34. Girard, P., Prost, J., and Bassereau, P., Passive or Active Fluctuations in Membranes Containing Proteins, Phys. Rev. Lett., 2005, vol. 94, no. 8, p. 088102(4).

    Article  CAS  Google Scholar 

  35. Gov, N., Membrane Undulations Driven by Force Fluctuations of Active Proteins, Phys. Rev. Lett., 2004, vol. 93, no. 26, p. 268104(4).

    Article  CAS  Google Scholar 

  36. Gov, N.S., Active Elastic Network: Cytoskeleton of the Red Blood Cell, Phys. Rev. E, 2007, vol. 75, no. 1, p. 011921(6).

    Article  CAS  Google Scholar 

  37. Gimsa, J. and Reid, C., Do Band 3 Protein Conformational Changes Mediate Shape Changes of Human Erythrocytes? Molecular Membrane Biology, 1995, vol. 12, no. 3, pp. 247–254.

    Article  PubMed  CAS  Google Scholar 

  38. Lomholt, M.A.. Fluctuation Spectrum of Quasispherical Membranes with Force-Dipole Activity, Phys. Rev. E, 2006, vol. 73, no. 6, p. 061914(9).

    Google Scholar 

  39. Fricke, K. and Sackmann, E., Variation of Frequency Spectrum of the Erythrocyte Flickering Caused by Aging, Osmolarity, Temperature and Pathological Changes, Biochim. Biophys. Acta, 1984, vol. 803, no. 3, pp. 145–152.

    Article  PubMed  CAS  Google Scholar 

  40. Bitler, A., Barbul, A., and Korenstein, R., Detection of Movement at the Erythrocyte’s Edge by Scanning Phase Contrast Microscopy, J. Microscopy, 1999, vol. 193,pt 2, no. 2, pp. 171–178.

    Article  CAS  Google Scholar 

  41. Humpert, C. and Baumann, M., Local Membrane Curvature Affects Spontaneous Membrane Fluctuation Characteristics, Molecular Membrane Biology, 2003, vol. 20, no. 2, pp. 155–162.

    Article  PubMed  CAS  Google Scholar 

  42. Zilker, A., Engelhardt, H., and Sackmann, E., Dynamic Reflection Interference Contrast (RIC-) Microscopy: A New Method to Study Excitations of Cells and to Measure Membrane Bending Elastic Moduli, J. de Physique, 1987, vol. 48, no. 12, pp. 2139–2151.

    Article  Google Scholar 

  43. Evans, J., Gratzer, W., Mohandas, N., Parker, K., and Sleep, J., Fluctuations of the Red Blood Cell Membrane: Relation to Mechanical Properties and Lack of ATP Dependence, Biophys. J., 2008, vol. 94, no. 5, pp. 4134–4144.

    Article  PubMed  CAS  Google Scholar 

  44. Krol, A.Ju., Grinfeldt, M.G., and Levin, S.V., The “Spontaneous” Oscillations of Cell Surface in Frequency Range 0.2–30 Hz, Tsitologiya (Rus.), 1989, vol. 31, no. 5, pp. 556–562.

    Google Scholar 

  45. Krol, A.Ju., Grinfeldt, M.G., Smilgavichus, A.D., and Levin, S.V., Fast Local Oscillations of Human Erythrocyte Surface, Tsitologiya (Rus.), 1989, vol. 31, no. 5, pp. 563–567.

    Google Scholar 

  46. Tuvia, S., Levin, S., Bitler, A., and Korenstein, R., Mechanical Fluctuations of the Membrane Skeleton Are Dependent on F-Actin ATPase in Human Erythrocytes, J. Cell Biol., 1998, vol. 141, no. 7, pp. 1551–1561.

    Article  PubMed  CAS  Google Scholar 

  47. Popescu, G., Ikeda, T., Best, C.A., Badizadegan, K., and Dasari, R.R., Erythrocyte Structure and Dynamics Quantified by Hilbert Phase Microscopy, J. Biomed. Opt., 2005, vol. 10, no. 6. p. 060503.

    Article  PubMed  Google Scholar 

  48. Popescu, G., Badizadegan, K., Dasari, R.R., and Feld, M.S., Observation of Dynamic Subdomains in Red Blood Cells, J. Biomed. Opt., 2006, vol. 11, no. 4, p. 040503.

    Article  PubMed  Google Scholar 

  49. Popescu, G., Ikeda, T., Dasari, R.R., and Feld, M.S., Diffraction Phase Microscopy for Quantifying Cell Structure and Dynamics, Optics Letters, 2006, vol. 31, no. 6, pp. 775–777.

    Article  PubMed  Google Scholar 

  50. Mesquita, L.G., Agero, U., and Mesquita, O.N., Defocusing Microscopy: An Approach for Red Blood Cell Optics, Appl. Phys. Lett., 2006, vol. 88, no. 13, p. 133901.

    Article  CAS  Google Scholar 

  51. Kononenko, V.L. and Shimkus, J.K., Spontaneous and Forced Oscillations of Cell Membrane of Normal Human Erythrocytes: Absence of Resonant Frequencies in a Range of 0.03–500 Hz, Biologicheskie Membrany (Rus.), 2000, vol. 17, no. 3, pp. 289–301 [Engl.Transl.: Membr. Cell Biol., 2000, vol. 14, no. 3, pp. 367–382.]

    CAS  Google Scholar 

  52. Beck, A.M. and Kononenko, V.L., Frequency Spectra of Erythrocyte Membrane Flickering Measured by Laser Light Scattering, Proceedings of SPIE, 1991, vol. 1403,pt. 1, pp. 384–386.

    Article  Google Scholar 

  53. Fricke, K., Wirthensohn, K., Laxhuber, R., and Sackmann, E., Flicker Spectroscopy of Erythrocytes: A Sensitive Method to Study Subtle Changes of Membrane Bending Stiffness, Eur. Biophys. J., 1986, vol. 14, no. 2, pp. 67–81.

    Article  PubMed  CAS  Google Scholar 

  54. Zilker, A., Ziegler, M., and Sackmann, E., Spectral Analysis of Erythrocyte Flickering in the 0.3–4-μ−1 Regime by Microinterferometry Combined with Fast Image Processing, Phys. Rev. A, 1992, vol. 46, no. 12, pp. 7998–8001.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. L. Kononenko.

Additional information

Original Russian Text © V.L. Kononenko, 2009, published in Biologicheskie Membrany, 2009, Vol. 26, No. 5, pp. 352–369.

The article was translated by the author.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kononenko, V.L. Flicker in erythrocytes. I. Theoretical models and registration techniques. Biochem. Moscow Suppl. Ser. A 3, 356–371 (2009). https://doi.org/10.1134/S1990747809040023

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747809040023

Key words

Navigation