Optical Sensing of Red Blood Cell Dynamics

  • YongKeun Park
  • Catherine A. Best
  • Gabriel Popescu
Chapter

Abstract

Human red blood cell membrane (RBC) has remarkable deformability, which is crucial for its oxygen transportation in the blood circulatory system. This deformability of the RBC membrane can be altered by several patho-physiological conditions. Here we present recent development of optical imaging techniques to measure dynamic fluctuations in the RBC membrane, from which RBC membrane mechanical properties are probed non-invasively.

Keywords

Sucrose Filtration Transportation Hexagonal Adenosine 

Notes

Acknowledgements

The authors are grateful for the mentoring provided by the late Michael Feld. The authors acknowledge fruitful collaborations with the groups lead by Subra Suresh, Alex Levine, Nir Gov, and Sam Safran.

References

  1. 1.
    Mohandas N and Gallagher P G (2008) Red cell membrane: past, present, and future. Blood 112:3939–3948CrossRefGoogle Scholar
  2. 2.
    Cotran R, Kumar V, Collins T et al (2004) Robbins pathologic basis of disease. Philadelphia: WB SaundersGoogle Scholar
  3. 3.
    Bao G and Suresh S (2003) Cell and molecular mechanics of biological materials. Nature Mat 2:715–725CrossRefGoogle Scholar
  4. 4.
    Fournier J B, Lacoste D, and Rapha E (2004) Fluctuation spectrum of fluid membranes coupled to an elastic meshwork: jump of the effective surface tension at the mesh size. Phys Rev Lett 92:18102CrossRefGoogle Scholar
  5. 5.
    Discher D E, Mohandas N, and Evans E A (1994) Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science 266:1032–1035CrossRefGoogle Scholar
  6. 6.
    Engelhardt H, Gaub H, and Sackmann E (1984) Viscoelastic properties of erythrocyte membranes in high-frequency electric fields. Nature 307:378–380CrossRefGoogle Scholar
  7. 7.
    Puig-de-Morales-Marinkovic M, Turner K T, Butler J P et al (2007) Viscoelasticity of the human red blood cell. Am J Physiol Cell Physiol 293:597–605CrossRefGoogle Scholar
  8. 8.
    Browicz T (1890) Further observation of motion phenomena on red blood cells in pathological states. Zbl med Wissen 28: 625–627Google Scholar
  9. 9.
    Gov N, Zilman A G, and Safran S (2003) Cytoskeleton confinement and tension of red blood cell membranes. Phys Rev Lett 90:228101CrossRefGoogle Scholar
  10. 10.
    Zilker A, Ziegler M, and Sackmann E (1992) Spectral-analysis of erythrocyte flickering in the 0.3-4-mu-m-1 regime by microinterferometry combined with fast image-processing. Phys Rev A 46:7998–8002CrossRefGoogle Scholar
  11. 11.
    Popescu G, Ikeda T, Dasari R R et al (2006) Diffraction phase microscopy for quantifying cell structure and dynamics. Opt Lett 31:775–777CrossRefGoogle Scholar
  12. 12.
    Tuvia S, Levin S, Bitler A et al (1998) Mechanical fluctuations of the membrane-skeleton are dependent on F-Actin ATPase in human erythrocytes. Proc Natl Acad Sci USA 141:1551–1561Google Scholar
  13. 13.
    Gov N S and Safran S A (2005) Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J 88:1859CrossRefGoogle Scholar
  14. 14.
    Lawrence C L L, Gov N, and Brown F L H (2006) Nonequilibrium membrane fluctuations driven by active proteins. J Chem Phys 124:074903CrossRefGoogle Scholar
  15. 15.
    Tuvia S, Levin S, Bitler A et al (1998) Mechanical fluctuations of the membrane-skeleton are dependent on F-actin ATPase in human erythrocytes. J Cell Biol 141:1551–1561CrossRefGoogle Scholar
  16. 16.
    Li J, Dao M, Lim C T et al (2005) Spectrin-level moddquo;eling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J 88:3707–3719CrossRefGoogle Scholar
  17. 17.
    Brochard F and Lennon J F (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys 36:1035–1047Google Scholar
  18. 18.
    Kaizuka Y and Groves J T (2006) Hydrodynamic damping of membrane thermal fluctuations near surfaces imaged by fluorescence interference microscopy. Phys Rev Lett 96:118101CrossRefGoogle Scholar
  19. 19.
    Zilker A, Engelhardt H, and Sackmann E (1987) Dynamic reflection interference contrast (Ric-) microscopy – a new method to study surface excitations of cells and to measure membrane bending elastic-moduli. J Phys 48:2139–2151Google Scholar
  20. 20.
    Zernike F (1942) Phase contrast, a new method for the microscopic observation of transparent objects part II. Physica 9:974–986CrossRefGoogle Scholar
  21. 21.
    Zidovska A and Sackmann E (2006) Brownian motion of nucleated cell envelopes impedes adhesion. Phys Rev Lett 96:048103CrossRefGoogle Scholar
  22. 22.
    Popescu G (2008) Quantitative phase imaging of nanoscale cell structure and dynamics. In: B. P. Jena, ed., Methods in Cell Biology. San Diego: ElsevierGoogle Scholar
  23. 23.
    Yang C, Wax A, Hahn M S et al (2001) Phase-referenced interferometer with subwavelength and subhertz sensitivity application to the study of cell membrane dynamics. Opt Lett 26:1271–1273CrossRefGoogle Scholar
  24. 24.
    Yang C H, Wax A, Georgakoudi I et al (2000) Interferometric phase-dispersion microscopy. Opt Lett 25:1526–1528CrossRefGoogle Scholar
  25. 25.
    Choma M A, Ellerbee A K, Yang C H et al (2005) Spectral-domain phase microscopy. Opt Lett 30:1162–1164CrossRefGoogle Scholar
  26. 26.
    Joo C, Akkin T, Cense B et al (2005) Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging. Opt Lett 30:2131–2133CrossRefGoogle Scholar
  27. 27.
    Fang-Yen C, Chu M C, Seung H S et al (2004) Noncontact measurement of nerve displacement during action potential with a dual-beam low-coherence interferometer. Opt Lett 29:2028–2030CrossRefGoogle Scholar
  28. 28.
    Akkin T, Dave D P, Milner T E et al (2004) Detection of neural activity using phase-sensitive optical low-coherence reflectometry. Opt Express 12:2377–2386CrossRefGoogle Scholar
  29. 29.
    Rylander C G, Dave D P, Akkin T et al (2004) Quantitative phase-contrast imaging of cells with phase-sensitive optical coherence microscopy. Opt Lett 29:1509–1511CrossRefGoogle Scholar
  30. 30.
    Zicha D and Dunn G A (1995) An image-processing system for cell behavior studies in subconfluent cultures. J Microsc 179:11–21Google Scholar
  31. 31.
    Dunn G A, Zicha D, and Fraylich P E (1997) Rapid, microtubule-dependent fluctuations of the cell margin. J Cell Sci 110:3091–3098Google Scholar
  32. 32.
    Zicha D, Genot E, Dunn G A et al (1999) TGF beta 1 induces a cell-cycle-dependent increase in motility of epithelial cells. J Cell Sci 112:447–454Google Scholar
  33. 33.
    Paganin D and Nugent K A (1998) Noninterferometric phase imaging with partially coherent light. Phys Rev Lett 80:2586–2589CrossRefGoogle Scholar
  34. 34.
    Allman B E, McMahon P J, Tiller J B et al (2000) Noninterferometric quantitative phase imaging with soft x rays. J Opt Soc Am A Opt Image Sci Vis 17:1732–1743CrossRefGoogle Scholar
  35. 35.
    Bajt S, Barty A, Nugent K A et al (2000) Quantitative phase-sensitive imaging in a transmission electron microscope. Ultramicroscopy 83:67–73CrossRefGoogle Scholar
  36. 36.
    Mann C J, Yu L F, Lo C M et al (2005) High-resolution quantitative phase-contrast microscopy by digital holography. Opt Express 13:8693–8698CrossRefGoogle Scholar
  37. 37.
    Marquet P, Rappaz B, Magistretti P J et al (2005) Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy. Opt Lett 30:468–470CrossRefGoogle Scholar
  38. 38.
    Iwai H, Fang-Yen C, Popescu G et al (2004) Quantitative phase imaging using actively stabilized phase-shifting low-coherence interferometry. Opt Lett 29:2399–2401CrossRefGoogle Scholar
  39. 39.
    Popescu G, Deflores L P, Vaughan J C et al (2004) Fourier phase microscopy for investigation of biological structures and dynamics. Opt Lett 29:2503–2505CrossRefGoogle Scholar
  40. 40.
    Ikeda T, Popescu G, Dasari R R et al (2005) Hilbert phase microscopy for investigating fast dynamics in transparent systems. Opt Lett 30:1165–1168CrossRefGoogle Scholar
  41. 41.
    Popescu G, Ikeda T, Best C A et al (2005) Erythrocyte structure and dynamics quantified by Hilbert phase microscopy. J Biomed Opt Lett 10:060503CrossRefGoogle Scholar
  42. 42.
    Huang D, Swanson E A, Lin C P et al (1991) Optical coherence tomography. Science 254:1178–1181CrossRefGoogle Scholar
  43. 43.
    deBoer J F, Milner T E, vanGemert M J C et al (1997) Two-dimensional birefringence imaging in biological tissue by polarization-sensitive optical coherence tomography. Opt Lett 22:934–936CrossRefGoogle Scholar
  44. 44.
    Hitzenberger C K and Fercher A F (1999) Differential phase contrast in optical coherence tomography. Gastrointest Endosc 24:622–624Google Scholar
  45. 45.
    Park J, Kemp N J, Milner T E et al (2003) Analysis of the phase retardation in the retinal nerve fiber layer of cynomolus monkey by polarization sensitive optical coherence tomography. Lasers Surg Med 55:55Google Scholar
  46. 46.
    Choma M A, Yang C H, and Izatt J A (2003) Instantaneous quadrature low-coherence interferometry with 3 x 3 fiber-optic couplers. Opt Lett 28:2162–2164CrossRefGoogle Scholar
  47. 47.
    Youn J I, Akkin T, Wong B J F et al (2003) Electrokinetic measurements of cartilage measurements of cartilage using differential phase optical coherence tomography. Lasers Surg Med 56:56Google Scholar
  48. 48.
    Kim J, Telenkov S A, and Milner T E (2004) Measurement of thermo-refractive and thermo-elastic changes in a tissue phantom using differential phase optical coherence tomography. Lasers Surg Med 8:8Google Scholar
  49. 49.
    Wojtkowski M (2010) High-speed optical coherence tomography: basics and applications. Appl Opt 49:30–61CrossRefGoogle Scholar
  50. 50.
    Dunn G and Zicha D (1998) Using the DRIMAPS system of interference microscopy to study cell behavior. In Cell biology: a laboratory handbook 44–53 J. Celis, Ed., Academic pressGoogle Scholar
  51. 51.
    Dunn G A and Zicha D (1995) Dynamics of fibroblast spreading. J Cell Sci 108:1239–1249Google Scholar
  52. 52.
    Gureyev T E, Roberts A, and Nugent K A (1995) Phase retrieval with the transport-of-intensity equation – matrix solution with use of Zernike polynomials. J Opt Soc Am A Opt Image Sci Vis 12:1932–1941MathSciNetCrossRefGoogle Scholar
  53. 53.
    Gureyev T E, Roberts A, and Nugent K A (1995) Partially coherent fields, the transport-of-intensity equation, and phase uniqueness. J Opt Soc Am A Opt Image Sci Vis 12:1942–1946MathSciNetCrossRefGoogle Scholar
  54. 54.
    Goodman J W and Lawrence R W (1967) Digital image formation from electronically detected holograms. Appl Phys Lett 11:77CrossRefGoogle Scholar
  55. 55.
    Gabor D (1948) A new microscopic principle. Nature 161:777CrossRefGoogle Scholar
  56. 56.
    Goodman J (2005) Introduction to Fourier optics. Englewood Cliffs: Roberts & CompanyGoogle Scholar
  57. 57.
    Yamaguchi I and Zhang T (1997) Phase-shifting digital holography. Opt Lett 22:1268–1270CrossRefGoogle Scholar
  58. 58.
    Carl D, Kemper B, Wernicke G et al (2004) Parameter-optimized digital holographic microscope for high-resolution living-cell analysis. Appl Opt 43:6536–6544CrossRefGoogle Scholar
  59. 59.
    Lue N, Choi W, Popescu G et al (2007) Quantitative phase imaging of live cells using fast Fourier phase microscopy. Appl Opt 46:1836CrossRefGoogle Scholar
  60. 60.
    Park Y K, Popescu G, Badizadegan K et al (2006) Diffraction phase and fluorescence microscopy. Opt Exp 14:8263CrossRefGoogle Scholar
  61. 61.
    Park Y K, Popescu G, Badizadegan K et al (2006) Diffraction phase and fluorescence microscopy. Opt Express 14:8263–8268CrossRefGoogle Scholar
  62. 62.
    Takeda M, Ina H, and Kobayashi S (1982) Fourier-transform method of fringe-pattern analysis for computer-based topography and interferometry. J Opt Soc Am 72:156–160CrossRefGoogle Scholar
  63. 63.
    Park Y K, Diez-Silva M, Popescu G et al (2008) Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc Natl Acad Sci U S A 105:13730CrossRefGoogle Scholar
  64. 64.
    Park Y, Yamauchi Y, Choi W, Dasari R and Feld M (2009) Spectroscopic phase microscopy for quantifying hemoglobin concentrations in intact red blood cells. Optics Letters 34: 3668–3670Google Scholar
  65. 65.
    Angelova M I, Soleau S, Meleard P et al (1992) Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Prog Colloid Polym Sci 89:122CrossRefGoogle Scholar
  66. 66.
    Popescu G, Ikeda T, Goda K et al (2006) Optical measurement of cell membrane tension. Phys Rev Lett 97:218101CrossRefGoogle Scholar
  67. 67.
    Evans E and Rawicz W (1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett 64:2094–2097CrossRefGoogle Scholar
  68. 68.
    Best C A, Cluette-Brown J E, Teruya M et al (2003) Red blood cell fatty acid ethyl esters: a significant component of fatty acid ethyl esters in the blood. J Lipid Res 44:612–620CrossRefGoogle Scholar
  69. 69.
    Lim H W G, Wortis M, and Mukhopadhyay R (2002) Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer-couple hypothesis from membrane mechanics. Proc Natl Acad Sci U S A 99:16766–16769CrossRefGoogle Scholar
  70. 70.
    Gov N, Zilman A, and Safran S (2003) Cytoskeleton confinement of red blood cell membrane fluctuations. Biophys J 84:486AGoogle Scholar
  71. 71.
    Discher D E, Boal D H, and Boey S K (1998) Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys J 75:1584–1597CrossRefGoogle Scholar
  72. 72.
    Park Y, Best C, Badizadegan K et al (2010) Measurement of red blood cell mechanics during morphological changes. Proc Natl Acad Sci U S A 107:6731CrossRefGoogle Scholar
  73. 73.
    Kuriabova T and Levine A J (2008) Nanorheology of viscoelastic shells: applications to viral capsids. Phys Rev E 77:031921MathSciNetCrossRefGoogle Scholar
  74. 74.
    Chaikin P M and Lubensky T C (1995) Principles of condensed matter physics. Cambridge: Cambridge University PressGoogle Scholar
  75. 75.
    Kuriabova T and Levine A (2008) Nanorheology of viscoelastic shells: applications to viral capsids. Phys Rev E 77:31921MathSciNetCrossRefGoogle Scholar
  76. 76.
    Waugh R and Evans E A (1979) Thermoelasticity of red blood cell membrane. Biophys J 26:115–131CrossRefGoogle Scholar
  77. 77.
    Dao M, Lim C T, and Suresh S (2003) Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 51:2259–2280CrossRefGoogle Scholar
  78. 78.
    Tang W and Thorpe M F (1988) Percolation of elastic networks under tension. Phys Rev B 37:5539CrossRefGoogle Scholar
  79. 79.
    Bursac P, Lenormand G, Fabry B et al (2005) Cytoskeletal remodelling and slow dynamics in the living cell. Nat Mater 4:557–561CrossRefGoogle Scholar
  80. 80.
    Siegel D (1985) Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J Cell Biol 100:775–785CrossRefGoogle Scholar
  81. 81.
    Marko J F and Siggia E D (1995) Stretching DNA. Macromolecules 28:8759–8770CrossRefGoogle Scholar
  82. 82.
    Park Y, Best C, Kuriabova T, Henle M L, Feld M S, Levine A J and Popescu G, Measurement of the nonlinear elasticity of red blood cell membrane. Phys Rev Lett (under review)Google Scholar
  83. 83.
    Popescu G, Park Y, Lue N et al (2008) Optical imaging of cell mass and growth dynamics. Am J Physiol Cell Physiol 295:C538CrossRefGoogle Scholar
  84. 84.
    Evans E and Fung Y C (1972) Improved measurements of the erythrocyte geometry. Microvasc Res 4:335–347CrossRefGoogle Scholar
  85. 85.
    Savitz D, Sidel V W, and Solomon A K (1964) Osmotic Properties of human red cells. J Gen Physiol 48:79–94CrossRefGoogle Scholar
  86. 86.
    Friebel M and Meinke M (2006) Model function to calculate the refractive index of native hemoglobin in the wavelength range of 250–1100 nm dependent on concentration. Appl Opt 45:2838–2842CrossRefGoogle Scholar
  87. 87.
    Schmid-SchoNbein H, Wells R O E, and Goldstone J (1969) Influence of deformability of human red cells upon blood viscosity. Circ Res 25:131–143Google Scholar
  88. 88.
    Mohandas N, Clark M R, Jacobs M S et al (1980) Analysis of factors regulating erythrocyte deformability. J Clin Invest 66:563CrossRefGoogle Scholar
  89. 89.
    Wells R and Schmid-Schonbein H (1969) Red cell deformation and fluidity of concentrated cell suspensions. J Appl Physiol 27:213–217Google Scholar
  90. 90.
    Kilejian A (1979) Characterization of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum. Proc Natl Acad Sci U S A 76:4650–4653CrossRefGoogle Scholar
  91. 91.
    Sherman I W (1979) Biochemistry of Plasmodium (malarial parasites). Microbiol Rev 43:453MathSciNetGoogle Scholar
  92. 92.
    Goldberg D E, Slater A F G, Cerami A et al (1990) Hemoglobin degradation in the malaria parasite Plasmodium falciparum: an ordered process in a unique organelle. Proc Natl Acad Sci U S A 87:2931–2935CrossRefGoogle Scholar
  93. 93.
    Nash G B, O’Brien E, Gordon-Smith E C et al (1989) Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum. Blood 74:855–861Google Scholar
  94. 94.
    Cranston H A, Boylan C W, Carroll G L et al (1984) Plasmodium falciparum maturation abolishes physiologic red cell deformability. Science 223:400–403CrossRefGoogle Scholar
  95. 95.
    Paulitschke M and Nash G B (1993) Membrane rigidity of red blood cells parasitized by different strains of Plasmodium falciparum. J Lab Clin Med 122:581–589Google Scholar
  96. 96.
    Miller L H, Baruch D I, Marsh K et al (2002) The pathogenic basis of malaria. Nature 415:673–679CrossRefGoogle Scholar
  97. 97.
    Suresh S, Spatz J, Mills J P et al (2005) Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomater 1:15–30CrossRefGoogle Scholar
  98. 98.
    Mills J P, Diez-Silva M, Quinn D J et al (2007) Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Proc Natl Acad Sci U S A 104:9213–9217CrossRefGoogle Scholar
  99. 99.
    Glenister F K, Coppel R L, Cowman A F et al (2002) Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 99:1060–1063CrossRefGoogle Scholar
  100. 100.
    Pei X, Guo X, Coppel R et al (2007) The ring-infected erythrocyte surface antigen (RESA) of plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110:1036–1042CrossRefGoogle Scholar
  101. 101.
    Lee J C M and Discher D E (2001) Deformation-enhanced fluctuations in the red cell skeleton with theoretical relations to elasticity, connectivity, and spectrin unfolding. Biophys J 81:3178–3192CrossRefGoogle Scholar
  102. 102.
    Parpart A and Hoffman J (1956) Flicker in erythrocytes. Vibratory movements in the cytoplasm? J Cell Comp Physiol 47:295–303CrossRefGoogle Scholar
  103. 103.
    Evans J, Gratzer W, Mohandas N et al (2008) Fluctuations of the red blood cell membrane: relation to mechanical properties and lack of ATP dependence. Biophys J 94:4134CrossRefGoogle Scholar
  104. 104.
    Szekely D, Yau T, and Kuchel P (2009) Human erythrocyte flickering: temperature, ATP concentration, water transport, and cell aging, plus a computer simulation. Eur Biophys J 38:923–939CrossRefGoogle Scholar
  105. 105.
    Gov N S (2007) Active elastic network: cytoskeleton of the red blood cell. Phys Rev E 75:11921CrossRefGoogle Scholar
  106. 106.
    Li J, Lykotrafitis G, Dao M et al (2007) Cytoskeletal dynamics of human erythrocyte. Proc Natl Acad Sci U S A 104:4937CrossRefGoogle Scholar
  107. 107.
    Zhang R and Brown F (2008) Cytoskeleton mediated effective elastic properties of model red blood cell membranes. J Chem Phys 129:065101CrossRefGoogle Scholar
  108. 108.
    Park Y, Best C, Auth T et al (2010) Metabolic remodeling of the human red blood cell membrane. Proc Natl Acad Sci U S A 107:1289CrossRefGoogle Scholar
  109. 109.
    Sheetz M and Singer S (1977) On the mechanism of ATP-induced shape changes in human erythrocyte membranes. I. The role of the spectrin complex. J Cell Biol 73:638–646CrossRefGoogle Scholar
  110. 110.
    Auth T, Safran S, and Gov N (2007) Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E 76:51910CrossRefGoogle Scholar
  111. 111.
    Tuvia S, Almagor A, Bitler A et al (1997) Cell membrane fluctuations are regulated by medium macroviscosity: evidence for a metabolic driving force. Proc Natl Acad Sci U S A 94:5045–5049CrossRefGoogle Scholar
  112. 112.
    Mizuno D, Tardin C, Schmidt C et al (2007) Nonequilibrium mechanics of active cytoskeletal networks. Science 315:370CrossRefGoogle Scholar
  113. 113.
    Liu F, Mizukami H, Sarnaik S et al (2005) Calcium-dependent human erythrocyte cytoskeleton stability analysis through atomic force microscopy. J Struct Biol 150:200–210CrossRefGoogle Scholar
  114. 114.
    Muller E, Hegewald H, Jaroszewicz K et al (1986) Turnover of phosphomonoester groups and compartmentation of polyphosphoinositides in human erythrocytes. Biochem J 235:775Google Scholar
  115. 115.
    Patel V and Fairbanks G (1981) Spectrin phosphorylation and shape change of human erythrocyte ghosts. J Cell Biol 88:430–440CrossRefGoogle Scholar
  116. 116.
    Agre P and Parker J (1989) Red blood cell membranes: structure, function, clinical implications. New York: CRC PressGoogle Scholar
  117. 117.
    Tchernia G, Mohandas N, and Shohet S (1981) Deficiency of skeletal membrane protein band 4.1 in homozygous hereditary elliptocytosis. Implications for erythrocyte membrane stability. J Clin Invest 68:454CrossRefGoogle Scholar
  118. 118.
    Suresh S (2006) Mechanical response of human red blood cells in health and disease: some structure-property-function relationships. J Mater Res 21:1872MathSciNetCrossRefGoogle Scholar
  119. 119.
    Fred M and Pickens M (1969) Metabolic dependence of red cell deformability. J Clin Invest 48:795CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • YongKeun Park
  • Catherine A. Best
  • Gabriel Popescu
    • 1
  1. 1.Department of Electrical and Computer Engineering, Quantitative Light Imaging Laboratory, Beckman Institute for Advanced Science and TechnologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations