Measurement of the nonlinear elasticity of red blood cell membranes.

The membranes of human red blood cells (RBCs) are a composite of a fluid lipid bilayer and a triangular network of semiflexible filaments (spectrin). We perform cellular microrheology using the dynamic membrane fluctuations of the RBCs to extract the elastic moduli of this composite membrane. By applying known osmotic stresses, we measure the changes in the elastic constants under imposed strain and thereby determine the nonlinear elastic properties of the membrane. We find that the elastic nonlinearities of the shear modulus in tensed RBC membranes can be well understood in terms of a simple wormlike chain model. Our results show that the elasticity of the spectrin network can mostly account for the area compression modulus at physiological osmolality, suggesting that the lipid bilayer has significant excess area. As the cell swells, the elastic contribution from the now tensed lipid membrane becomes dominant.

[1]  F. Brochard,et al.  Frequency spectrum of the flicker phenomenon in erythrocytes , 1975 .

[2]  Zhuo Wang,et al.  Fourier transform light scattering of inhomogeneous and dynamic structures. , 2008, Physical review letters.

[3]  Mason,et al.  Optical measurements of frequency-dependent linear viscoelastic moduli of complex fluids. , 1995, Physical review letters.

[4]  Martin Lenz,et al.  ATP-dependent mechanics of red blood cells , 2009, Proceedings of the National Academy of Sciences.

[5]  R. Wells,et al.  Influence of Deformability of Human Red Cells upon Blood Viscosity , 1969, Circulation research.

[6]  Michelle D. Wang,et al.  Estimating the persistence length of a worm-like chain molecule from force-extension measurements. , 1999, Biophysical journal.

[7]  Seifert,et al.  Dual network model for red blood cell membranes. , 1992, Physical review letters.

[8]  Shechao Feng,et al.  Percolation on Elastic Networks: New Exponent and Threshold , 1984 .

[9]  Gabriel Popescu,et al.  Measurement of red blood cell mechanics during morphological changes , 2010, Proceedings of the National Academy of Sciences.

[10]  M. Friebel,et al.  Model function to calculate the refractive index of native hemoglobin in the wavelength range of 250-1100 nm dependent on concentration. , 2006, Applied optics.

[11]  R M Hochmuth,et al.  Temperature dependence of the viscoelastic recovery of red cell membrane. , 1980, Biophysical journal.

[12]  A. Mikkelsen,et al.  Human erythrocyte spectrin dimer intrinsic viscosity: temperature dependence and implications for the molecular basis of the erythrocyte membrane free energy. , 1985, Biochimica et biophysica acta.

[13]  R. Dasari,et al.  Diffraction phase microscopy for quantifying cell structure and dynamics. , 2006, Optics letters.

[14]  Gabriel Popescu,et al.  Optical imaging of cell mass and growth dynamics. , 2008, American journal of physiology. Cell physiology.

[15]  Levine,et al.  One- and two-particle microrheology , 2000, Physical review letters.

[16]  Christoph F. Schmidt,et al.  Conformation and elasticity of the isolated red blood cell membrane skeleton. , 1992, Biophysical journal.

[17]  Pietro Cicuta,et al.  Flickering analysis of erythrocyte mechanical properties: dependence on oxygenation level, cell shape, and hydration level. , 2009, Biophysical journal.

[18]  Subra Suresh,et al.  Viscoelasticity of the human red blood cell , 2006, American journal of physiology. Cell physiology.

[19]  Milner,et al.  Dynamical fluctuations of droplet microemulsions and vesicles. , 1987, Physical review. A, General physics.

[20]  E. Evans,et al.  Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. , 1994, Science.

[21]  Andrew G. Glen,et al.  APPL , 2001 .

[22]  A. Zilman,et al.  Cytoskeleton confinement and tension of red blood cell membranes. , 2003, Physical review letters.

[23]  Y. C. Fung,et al.  Improved measurements of the erythrocyte geometry. , 1972, Microvascular research.

[24]  D. Discher,et al.  New insights into red cell network structure, elasticity, and spectrin unfolding--a current review. , 2001, Cellular & molecular biology letters.

[25]  R. Simmons,et al.  Elasticity of the red cell membrane and its relation to hemolytic disorders: an optical tweezers study. , 1999, Biophysical journal.

[26]  Zhuo Wang,et al.  Diffraction Phase Cytometry: blood on a CD-ROM. , 2009, Optics express.

[27]  E. Sackmann,et al.  Viscoelastic properties of erythrocyte membranes in high-frequency electric fields , 1984, Nature.

[28]  Pietro Cicuta,et al.  Diffusion of liquid domains in lipid bilayer membranes. , 2007, The journal of physical chemistry. B.

[29]  R. Wells,et al.  Red cell deformation and fluidity of concentrated cell suspensions. , 1969, Journal of applied physiology.

[30]  C. Lim,et al.  Mechanics of the human red blood cell deformed by optical tweezers , 2003 .

[31]  Sackmann,et al.  Spectral analysis of erythrocyte flickering in the 0.3-4- microm-1 regime by microinterferometry combined with fast image processing. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[32]  Nir S. Gov,et al.  Metabolic remodeling of the human red blood cell membrane , 2010, Proceedings of the National Academy of Sciences.

[33]  Suliana Manley,et al.  Optical measurement of cell membrane tension. , 2006, Physical review letters.

[34]  E. Evans.  Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. , 1983, Biophysical journal.

[35]  N. Mohandas,et al.  Analysis of factors regulating erythrocyte deformability. , 1980, The Journal of clinical investigation.

[36]  Yongkeun Park,et al.  Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum , 2008, Proceedings of the National Academy of Sciences.

[37]  A. Levine,et al.  Nanorheology of viscoelastic shells: applications to viral capsids. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.