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.
This chapter is part of Section IV: Tools for Exploring Mechanobiology
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Mohandas N and Gallagher P G (2008) Red cell membrane: past, present, and future. Blood 112:3939–3948
Cotran R, Kumar V, Collins T et al (2004) Robbins pathologic basis of disease. Philadelphia: WB Saunders
Bao G and Suresh S (2003) Cell and molecular mechanics of biological materials. Nature Mat 2:715–725
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 92:18102
Discher D E, Mohandas N, and Evans E A (1994) Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science 266:1032–1035
Engelhardt H, Gaub H, and Sackmann E (1984) Viscoelastic properties of erythrocyte membranes in high-frequency electric fields. Nature 307:378–380
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 293:597–605
Browicz T (1890) Further observation of motion phenomena on red blood cells in pathological states. Zbl med Wissen 28: 625–627
Gov N, Zilman A G, and Safran S (2003) Cytoskeleton confinement and tension of red blood cell membranes. Phys Rev Lett 90:228101
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 46:7998–8002
Popescu G, Ikeda T, Dasari R R et al (2006) Diffraction phase microscopy for quantifying cell structure and dynamics. Opt Lett 31:775–777
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 141:1551–1561
Gov N S and Safran S A (2005) Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J 88:1859
Lawrence C L L, Gov N, and Brown F L H (2006) Nonequilibrium membrane fluctuations driven by active proteins. J Chem Phys 124:074903
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 141:1551–1561
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 88:3707–3719
Brochard F and Lennon J F (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys 36:1035–1047
Kaizuka Y and Groves J T (2006) Hydrodynamic damping of membrane thermal fluctuations near surfaces imaged by fluorescence interference microscopy. Phys Rev Lett 96:118101
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 48:2139–2151
Zernike F (1942) Phase contrast, a new method for the microscopic observation of transparent objects part II. Physica 9:974–986
Zidovska A and Sackmann E (2006) Brownian motion of nucleated cell envelopes impedes adhesion. Phys Rev Lett 96:048103
Popescu G (2008) Quantitative phase imaging of nanoscale cell structure and dynamics. In: B. P. Jena, ed., Methods in Cell Biology. San Diego: Elsevier
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 26:1271–1273
Yang C H, Wax A, Georgakoudi I et al (2000) Interferometric phase-dispersion microscopy. Opt Lett 25:1526–1528
Choma M A, Ellerbee A K, Yang C H et al (2005) Spectral-domain phase microscopy. Opt Lett 30:1162–1164
Joo C, Akkin T, Cense B et al (2005) Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging. Opt Lett 30:2131–2133
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 29:2028–2030
Akkin T, Dave D P, Milner T E et al (2004) Detection of neural activity using phase-sensitive optical low-coherence reflectometry. Opt Express 12:2377–2386
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 29:1509–1511
Zicha D and Dunn G A (1995) An image-processing system for cell behavior studies in subconfluent cultures. J Microsc 179:11–21
Dunn G A, Zicha D, and Fraylich P E (1997) Rapid, microtubule-dependent fluctuations of the cell margin. J Cell Sci 110:3091–3098
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 112:447–454
Paganin D and Nugent K A (1998) Noninterferometric phase imaging with partially coherent light. Phys Rev Lett 80:2586–2589
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 17:1732–1743
Bajt S, Barty A, Nugent K A et al (2000) Quantitative phase-sensitive imaging in a transmission electron microscope. Ultramicroscopy 83:67–73
Mann C J, Yu L F, Lo C M et al (2005) High-resolution quantitative phase-contrast microscopy by digital holography. Opt Express 13:8693–8698
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 30:468–470
Iwai H, Fang-Yen C, Popescu G et al (2004) Quantitative phase imaging using actively stabilized phase-shifting low-coherence interferometry. Opt Lett 29:2399–2401
Popescu G, Deflores L P, Vaughan J C et al (2004) Fourier phase microscopy for investigation of biological structures and dynamics. Opt Lett 29:2503–2505
Ikeda T, Popescu G, Dasari R R et al (2005) Hilbert phase microscopy for investigating fast dynamics in transparent systems. Opt Lett 30:1165–1168
Popescu G, Ikeda T, Best C A et al (2005) Erythrocyte structure and dynamics quantified by Hilbert phase microscopy. J Biomed Opt Lett 10:060503
Huang D, Swanson E A, Lin C P et al (1991) Optical coherence tomography. Science 254:1178–1181
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 22:934–936
Hitzenberger C K and Fercher A F (1999) Differential phase contrast in optical coherence tomography. Gastrointest Endosc 24:622–624
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 55:55
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 28:2162–2164
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 56:56
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 8:8
Wojtkowski M (2010) High-speed optical coherence tomography: basics and applications. Appl Opt 49:30–61
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 press
Dunn G A and Zicha D (1995) Dynamics of fibroblast spreading. J Cell Sci 108:1239–1249
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 12:1932–1941
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 12:1942–1946
Goodman J W and Lawrence R W (1967) Digital image formation from electronically detected holograms. Appl Phys Lett 11:77
Gabor D (1948) A new microscopic principle. Nature 161:777
Goodman J (2005) Introduction to Fourier optics. Englewood Cliffs: Roberts & Company
Yamaguchi I and Zhang T (1997) Phase-shifting digital holography. Opt Lett 22:1268–1270
Carl D, Kemper B, Wernicke G et al (2004) Parameter-optimized digital holographic microscope for high-resolution living-cell analysis. Appl Opt 43:6536–6544
Lue N, Choi W, Popescu G et al (2007) Quantitative phase imaging of live cells using fast Fourier phase microscopy. Appl Opt 46:1836
Park Y K, Popescu G, Badizadegan K et al (2006) Diffraction phase and fluorescence microscopy. Opt Exp 14:8263
Park Y K, Popescu G, Badizadegan K et al (2006) Diffraction phase and fluorescence microscopy. Opt Express 14:8263–8268
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 72:156–160
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 105:13730
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: 3668–3670
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 89:122
Popescu G, Ikeda T, Goda K et al (2006) Optical measurement of cell membrane tension. Phys Rev Lett 97:218101
Evans E and Rawicz W (1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett 64:2094–2097
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 44:612–620
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 99:16766–16769
Gov N, Zilman A, and Safran S (2003) Cytoskeleton confinement of red blood cell membrane fluctuations. Biophys J 84:486A
Discher D E, Boal D H, and Boey S K (1998) Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys J 75:1584–1597
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 107:6731
Kuriabova T and Levine A J (2008) Nanorheology of viscoelastic shells: applications to viral capsids. Phys Rev E 77:031921
Chaikin P M and Lubensky T C (1995) Principles of condensed matter physics. Cambridge: Cambridge University Press
Kuriabova T and Levine A (2008) Nanorheology of viscoelastic shells: applications to viral capsids. Phys Rev E 77:31921
Waugh R and Evans E A (1979) Thermoelasticity of red blood cell membrane. Biophys J 26:115–131
Dao M, Lim C T, and Suresh S (2003) Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 51:2259–2280
Tang W and Thorpe M F (1988) Percolation of elastic networks under tension. Phys Rev B 37:5539
Bursac P, Lenormand G, Fabry B et al (2005) Cytoskeletal remodelling and slow dynamics in the living cell. Nat Mater 4:557–561
Siegel D (1985) Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J Cell Biol 100:775–785
Marko J F and Siggia E D (1995) Stretching DNA. Macromolecules 28:8759–8770
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)
Popescu G, Park Y, Lue N et al (2008) Optical imaging of cell mass and growth dynamics. Am J Physiol Cell Physiol 295:C538
Evans E and Fung Y C (1972) Improved measurements of the erythrocyte geometry. Microvasc Res 4:335–347
Savitz D, Sidel V W, and Solomon A K (1964) Osmotic Properties of human red cells. J Gen Physiol 48:79–94
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 45:2838–2842
Schmid-SchoNbein H, Wells R O E, and Goldstone J (1969) Influence of deformability of human red cells upon blood viscosity. Circ Res 25:131–143
Mohandas N, Clark M R, Jacobs M S et al (1980) Analysis of factors regulating erythrocyte deformability. J Clin Invest 66:563
Wells R and Schmid-Schonbein H (1969) Red cell deformation and fluidity of concentrated cell suspensions. J Appl Physiol 27:213–217
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 76:4650–4653
Sherman I W (1979) Biochemistry of Plasmodium (malarial parasites). Microbiol Rev 43:453
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 87:2931–2935
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 74:855–861
Cranston H A, Boylan C W, Carroll G L et al (1984) Plasmodium falciparum maturation abolishes physiologic red cell deformability. Science 223:400–403
Paulitschke M and Nash G B (1993) Membrane rigidity of red blood cells parasitized by different strains of Plasmodium falciparum. J Lab Clin Med 122:581–589
Miller L H, Baruch D I, Marsh K et al (2002) The pathogenic basis of malaria. Nature 415:673–679
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 1:15–30
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 104:9213–9217
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 99:1060–1063
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 110:1036–1042
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 81:3178–3192
Parpart A and Hoffman J (1956) Flicker in erythrocytes. Vibratory movements in the cytoplasm? J Cell Comp Physiol 47:295–303
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 94:4134
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 38:923–939
Gov N S (2007) Active elastic network: cytoskeleton of the red blood cell. Phys Rev E 75:11921
Li J, Lykotrafitis G, Dao M et al (2007) Cytoskeletal dynamics of human erythrocyte. Proc Natl Acad Sci U S A 104:4937
Zhang R and Brown F (2008) Cytoskeleton mediated effective elastic properties of model red blood cell membranes. J Chem Phys 129:065101
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 107:1289
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 73:638–646
Auth T, Safran S, and Gov N (2007) Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E 76:51910
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 94:5045–5049
Mizuno D, Tardin C, Schmidt C et al (2007) Nonequilibrium mechanics of active cytoskeletal networks. Science 315:370
Liu F, Mizukami H, Sarnaik S et al (2005) Calcium-dependent human erythrocyte cytoskeleton stability analysis through atomic force microscopy. J Struct Biol 150:200–210
Muller E, Hegewald H, Jaroszewicz K et al (1986) Turnover of phosphomonoester groups and compartmentation of polyphosphoinositides in human erythrocytes. Biochem J 235:775
Patel V and Fairbanks G (1981) Spectrin phosphorylation and shape change of human erythrocyte ghosts. J Cell Biol 88:430–440
Agre P and Parker J (1989) Red blood cell membranes: structure, function, clinical implications. New York: CRC Press
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 68:454
Suresh S (2006) Mechanical response of human red blood cells in health and disease: some structure-property-function relationships. J Mater Res 21:1872
Fred M and Pickens M (1969) Metabolic dependence of red cell deformability. J Clin Invest 48:795
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Park, Y., Best, C.A., Popescu, G. (2011). Optical Sensing of Red Blood Cell Dynamics. In: Wagoner Johnson, A., Harley, B. (eds) Mechanobiology of Cell-Cell and Cell-Matrix Interactions. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-8083-0_13
Download citation
DOI: https://doi.org/10.1007/978-1-4419-8083-0_13
Published:
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4419-8082-3
Online ISBN: 978-1-4419-8083-0
eBook Packages: EngineeringEngineering (R0)