Hostname: page-component-77c89778f8-5wvtr Total loading time: 0 Render date: 2024-07-19T00:38:31.090Z Has data issue: false hasContentIssue false

Erythrocyte responses in low-shear-rate flows: effects of non-biconcave stress-free state in the cytoskeleton

Published online by Cambridge University Press:  21 February 2014

Zhangli Peng
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
Adel Mashayekh
Affiliation:
Department of Structural Engineering, University of California San Diego, La Jolla, CA 92093, USA
Qiang Zhu*
Affiliation:
Department of Structural Engineering, University of California San Diego, La Jolla, CA 92093, USA
*
Email address for correspondence: qizhu@ucsd.edu

Abstract

Inspired by the recent experiment on erythrocytes (red blood cells, RBCs) in weak shear flows by Dupire et al. (Proc. Natl Acad. Sci. USA, vol. 109, 2012, pp. 20808–20813), we conduct a numerical investigation to study the dynamics of RBCs in low-shear-rate flows by applying a multiscale fluid–structure interaction model. By employing a spheroidal stress-free state in the cytoskeleton, we are able to numerically predict an important feature, namely that the cell maintains its biconcave shape during tank-treading motions. Furthermore, we numerically confirm the hypothesis that, as the stress-free state approaches a sphere, the threshold shear rates corresponding to the establishment of tank treading decrease. By comparing with the experimental measurements, our study suggests that the stress-free state of RBCs is a spheroid that is close to a sphere, rather than the biconcave shape applied in existing models (the implication is that the RBC skeleton is pre-stressed in its natural biconcave state). It also suggests that the response of RBCs in low-shear-rate flows may provide a measure to quantitatively determine the distribution of shear stress in the RBC cytoskeleton in the natural state.

Type
Papers
Copyright
© 2014 Cambridge University Press 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abkarian, M., Faivre, M. & Viallat, A. 2007 Swinging of red blood cells under shear flow. Phys. Rev. Lett. 98, 188302.Google Scholar
Bagchi, P. & Kalluri, R. 2009 Dynamics of nonspherical capsules in shear flow. Phys. Rev. E 80, 016307.Google Scholar
Barthès-Biesel, D. 1980 Motion of a spherical microcapsule freely suspended in a linear shear flow. J. Fluid Mech. 100, 831853.Google Scholar
Belytschko, T., Liu, W. & Moran, B. 2000 Nonlinear Finite Elements for Continua and Structures. John Wiley.Google Scholar
Bennett, V. & Baines, A. J. 2001 Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 13531392.Google Scholar
Bitbol, M. 1986 Red blood cell orientation in orbit $c=0$ . Biophys. J. 49, 10551068.CrossRefGoogle ScholarPubMed
Chien, S. 1987 Red cell deformability and its relevance to blood flow. Annu. Rev. Physiol. 49, 177192.Google Scholar
Dao, M., Li, J. & Suresh, S. 2006 Molecularly based analysis of deformation of spectrin network and human erythrocyte. Mater. Sci. Engng 26, 12321244.Google Scholar
Discher, D. E., Boal, D. H. & Boey, S. K. 1998 Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys. J. 75, 15841597.Google Scholar
Discher, D. E., Mohandas, N. & Evans, E. A. 1994 Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science 266, 10321035.Google Scholar
Doddi, S. & Bagchi, P. 2008 Lateral migration of a capsule in a plane Poiseuille flow in a channel. Intl J. Multiphase Flow 34, 966986.Google Scholar
Dodson, W. R. & Dimitrakopoulos, P. 2010 Tank-treading of erythrocytes in strong shear flows via a nonstiff cytoskeleton-based continuum computational modeling. Biophys. J. 99, 29062916.Google Scholar
Dupire, J., Socol, M. & Viallat, A. 2012 Full dynamics of a red blood cell in shear flow. Proc. Natl. Acad. Sci. USA 109, 2080820813.Google Scholar
Dupont, C., Salsac, A. & Barthès-Biesel, D. 2013 Off-plane motion of a prolate capsule in shear flow. J. Fluid Mech. 721, 180198.Google Scholar
Eggleton, C. D. & Popel, A. S. 1998 Large deformation of red blood cell ghosts in a simple shear flow. Phys. Fluids 10, 18341845.Google Scholar
Evans, E. & Hochmuth, R. 1976 Membrane viscoelasticity. Biophys. J. 16, 111.Google Scholar
Evans, E. A. & Skalak, P. 1980 Mechanics and Thermodynamics of Biomembranes. CRC Press.Google Scholar
Fedosov, D. A., Caswell, B. & Karniadakis, G. E. 2011 Wall shear stress-based model for adhesive dynamics of red blood cells in malaria. Biophys. J. 100, 20842093.CrossRefGoogle ScholarPubMed
Fischer, T. M. 2004 Shape memory of human red blood cells. Biophys. J. 86, 33043313.CrossRefGoogle ScholarPubMed
Fischer, T. M. & Korzeniewski, R. 2013 Threshold shear stress for the transition between tumbling and tank-treading of red blood cells in shear flow: dependence on the viscosity of the suspending medium. J. Fluid Mech. 736, 351365.CrossRefGoogle Scholar
Fischer, T. M., Stohr-Liesen, M. & Schmid-Schonbein, H. 1978 The red cell as a fluid droplet: tank tread-like motion of the human erythrocyte membrane in shear flow. Science 202, 894896.Google Scholar
Foessel, E., Walter, J., Salsac, A.-V. & Barthès-Biesel, D. 2011 Influence of internal viscosity on the large deformation and buckling of a spherical capsule in a simple shear flow. J. Fluid Mech. 672, 477486.Google Scholar
Henon, S., Lenormand, G., Richert, A. & Gallet, F. 1999 A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys. J. 76, 11451151.CrossRefGoogle ScholarPubMed
Hoffman, J. F. 2001 Questions for red blood cell physiologists to ponder in this millenium. Blood Cells Mol. Dis. 27, 5761.Google Scholar
Keller, S. & Skalak, R. 1982 Motion of a tank-treading ellipsoidal particle in a shear flow. J. Fluid Mech. 120, 2747.Google Scholar
Khairy, K. & Howard, J. 2011 Minimum-energy vesicle and cell shapes calculated using spherical harmonics parameterization. Soft Matt. 7, 21382143.Google Scholar
Law, R., Carl, P., Harper, S., Dalhaimer, P., Speicher, D. W. & Discher, D. E. 2003 Cooperativity in forced unfolding of tandem spectrin repeats. Biophys. J. 84, 533544.Google Scholar
Le, D. V. 2010 Effect of bending stiffness on the deformation of liquid capsules enclosed by thin shells in shear flow. Phys. Rev. E 82, 016318.CrossRefGoogle ScholarPubMed
Lim, G., Wortis, M. & 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. USA 99, 1676616769.Google Scholar
Mohandas, N. & Evans, E. A. 1994 Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Biophys. Biomol. Struct. 23, 787818.CrossRefGoogle ScholarPubMed
Noguchi, H. 2009 Swinging and synchronized rotations of red blood cells in simple shear flow. Phys. Rev. E 80, 021902.Google Scholar
Noguchi, H. 2010 Dynamic modes of microcapsules in steady shear flow: effects of bending and shear elasticities. Phys. Rev. E 81, 056319.CrossRefGoogle ScholarPubMed
Omori, T., Ishikawa, T., Barthès-Biesel, D., Salsac, A., Imai, Y. & Yamaguchi, T. 2012 Tension of red blood cell membrane in simple shear flow. Phys. Rev. E 86, 056321.Google Scholar
Otter, W. K. & Shkulipa, S. A. 2007 Intermonolayer friction and surface shear viscosity of lipid bilayer membranes. Biophys. J. 93, 423433.Google Scholar
Peng, Z., Asaro, R. & Zhu, Q. 2010 Multiscale simulation of erythrocyte membranes. Phys. Rev. E 81, 031904.CrossRefGoogle ScholarPubMed
Peng, Z., Asaro, R. & Zhu, Q. 2011 Multiscale modeling of erythrocytes in Stokes flow. J. Fluid Mech. 686, 299337.Google Scholar
Peng, Z., Li, X., Pivkin, I. V., Dao, M., Karniadakis, G. E. & Suresh, S. 2013 Lipid bilayer and cytoskeletal interactions in a red blood cell. Proc. Natl. Acad. Sci. USA 110, 1335613361.Google Scholar
Peng, Z. & Zhu, Q. 2013 Deformation of the erythrocyte cytoskeleton in tank treading motions. Soft Matt. 9, 76177627.Google Scholar
Peterson, M. A., Strey, H. & Sackmann, E. 1992 Theoretical and phase contrast microscopic eigenmode analysis of erythrocyte flicker: amplitudes. J. Phys. II (Paris) 2, 12731285.Google Scholar
Pozrikidis, C. 1992 Boundary Integral and Singularity Methods for Linearized Viscous Flow. Cambridge University Press.Google Scholar
Pozrikidis, C. 2003 Numerical simulation of the flow-induced deformation of red blood cells. Ann. Biomed. Engng 31, 11941205.CrossRefGoogle ScholarPubMed
Pozrikidis, C. 2005 Axisymmetric motion of a file of red blood cells through capillaries. Phys. Fluids 17, 031503.Google Scholar
Ramanujan, S. & Pozrikidis, C. 1998 Deformation of liquid capsules enclosed by elastic membranes in simple shear flow: large deformations and the effect of fluid viscosities. J. Fluid Mech. 361, 117143.Google Scholar
Rief, M., Pascual, J., Saraste, M. & Gaub, H. E. 1999 Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J. Mol. Biol. 286, 553561.Google Scholar
Schenk, O. & Gartner, K. 2004 Solving unsymmetric sparse systems of linear equations with PARDISO. Future Gener. Comput. Syst. 20, 475487.Google Scholar
Schenk, O. & Gartner, K. 2006 On fast factorization pivoting methods for symmetric indefinite systems. Elec. Trans. Numer. Anal. 23, 158179.Google Scholar
Seifert, U., Berndl, K. & Lipowsky, R. 1991 Shape transformations of vesicles: phase diagram for spontaneous-curvature and bilayer-coupling models. Phys. Rev. A 44, 11821202.Google Scholar
Skotheim, J. & Secomb, T. 2007 Red blood cells and other nonspherical capsules in shear flow: oscillatory dynamics and the tank-treading-to-tumbling transition. Phys. Rev. Lett. 98, 078301.Google Scholar
Sui, Y., Chew, Y. T., Roy, P., Chen, X. B. & Low, H. T. 2007 Transient deformation of elastic capsules in shear flow: effect of membrane bending stiffness. Phys. Rev. E 75, 066301.Google Scholar
Sung, L. A. & Vera, C. 2003 Protofilament and hexagon: a three-dimensional mechanical model for the junctional complex in the RBC membrane skeleton. Ann. Biomed. Engng 31, 13141326.Google Scholar
Svelc, T. & Svetina, S. 2012 Stress-free state of the red blood cell membrane and the deformation of its skeleton. Cell. Mol. Biol. Lett. 17, 217227.Google Scholar
Svoboda, K., Schmidt, C. F., Branton, D. & Block, S. M. 1992 Conformation and elasticity of the isolated red blood cell membrane skeleton. Biophys. J. 63, 784793.Google Scholar
Telles, J. C. 1987 A self-adaptive co-ordinate transformation for efficient numerical evaluation of general boundary element integrals. Intl J. Numer. Meth. Engng 24, 959973.Google Scholar
Tran-Son-Tay, R., Sutera, S. & Rao, P. 1984 Determination of red blood cell membrane viscosity from rheoscopic observations of tank-treading motion. Biophys. J. 46, 6572.Google Scholar
Tsubota, K., Wada, S. & Liu, H. 2013 Elastic behavior of a red blood cell with the membranes nonuniform natural state: equilibrium shape, motion transition under shear flow, and elongation during tank-treading motion. Biomech. Model. Mechanobiol. doi:10.1007/s10237-013-0530-z.Google Scholar
Vlahovska, P., Young, Y. N., Danker, G. & Misbah, C. 2011 Dynamics of a non-spherical microcapsule with incompressible interface in shear flow. J. Fluid Mech. 678, 221247.Google Scholar
Walter, J., Salsac, A. V., Barthès-Biesel, D. & Le Tallec, P. 2010 Coupling of finite element and boundary integral methods for a capsule in a Stokes flow. Intl J. Numer. Meth. Engng 83, 829850.Google Scholar
Yazdani, A. & Bagchi, P. 2013 Influence of membrane viscosity on capsule dynamics in shear flow. J. Fluid Mech. 718, 569595.Google Scholar
Yazdani, A., Kalluri, R. & Bagchi, P. 2011 Tank-treading and tumbling frequencies of capsules and red blood cells. Phys. Rev. E 83, 046305.Google Scholar
Zhu, Q. & Asaro, R. 2008 Spectrin folding vs. unfolding reactions and RBC membrane stiffness. Biophys. J. 94, 25292545.Google Scholar
Zhu, Q., Vera, C., Asaro, R. J., Sche, P. & Sung, L. A. 2007 A hybrid model for erythrocyte membrane: a single unit of protein network coupled with lipid bilayer. Biophys. J. 93, 386400.Google Scholar