0
Research Papers

Computational Biomechanics of Human Red Blood Cells in Hematological Disorders

[+] Author and Article Information
Xuejin Li

Division of Applied Mathematics,
Brown University,
Providence, RI 02912
e-mail: Xuejin_Li@brown.edu

He Li, Hung-Yu Chang

Division of Applied Mathematics,
Brown University,
Providence, RI 02912

George Lykotrafitis

Department of Mechanical Engineering,
University of Connecticut,
Storrs, CT 06269;
Department of Biomedical Engineering,
University of Connecticut,
Storrs, CT 06269

George Em Karniadakis

Fellow ASME
Division of Applied Mathematics,
Brown University,
Providence, RI 02912
e-mail: George_Karniadakis@brown.edu

1Corresponding authors.

Manuscript received June 30, 2016; final manuscript received October 29, 2016; published online January 19, 2017. Assoc. Editor: Victor H. Barocas.

J Biomech Eng 139(2), 021008 (Jan 19, 2017) (13 pages) Paper No: BIO-16-1277; doi: 10.1115/1.4035120 History: Received June 30, 2016; Revised October 29, 2016

We review recent advances in multiscale modeling of the biomechanical characteristics of red blood cells (RBCs) in hematological diseases, and their relevance to the structure and dynamics of defective RBCs. We highlight examples of successful simulations of blood disorders including malaria and other hereditary disorders, such as sickle-cell anemia, spherocytosis, and elliptocytosis.

FIGURES IN THIS ARTICLE
<>
Copyright © 2017 by ASME
Your Session has timed out. Please sign back in to continue.

References

Popel, A. S. , and Johnson, P. C. , 2005, “ Microcirculation and Hemorheology,” Ann. Rev. Fluid Mech., 37(1), pp. 43–69. [CrossRef]
McLaren, C. E. , Brittenham, G. M. , and Hasselblad, V. , 1987, “ Statistical and Graphical Evaluation of Erythrocyte Volume Distributions,” Am. J. Physiol. Heart Circ. Physiol., 252(5), pp. H857–H866. http://ajpheart.physiology.org/content/252/4/H857
Chasis, J. A. , and Shohet, S. B. , 1987, “ Red Cell Biochemical Anatomy and Membrane Properties,” Ann. Rev. Physiol., 49(1), pp. 237–248. [CrossRef]
McCaughan, L. , and Krimm, S. , 1980, “ X-Ray and Neutron Scattering Density Profiles of the Intact Human Red Blood Cell Membrane,” Science, 207(4438), pp. 1481–1483. [CrossRef] [PubMed]
Hochmuth, R. , Evans, C. , Wiles, H. , and McCown, J. , 1983, “ Mechanical Measurement of Red Cell Membrane Thickness,” Science, 220(4592), pp. 101–102. [CrossRef] [PubMed]
Nguyen, Q. D. , and Boger, D. V. , 1987, “ Characterization of Yield Stress Fluids With Concentric Cylinder Viscometers,” Rheol. Acta, 26(6), pp. 508–515. [CrossRef]
Drochon, A. A. , Barthes-Biesel, D. D. , Lacombe, C. C. , and Lelievre, J. C. , 1990, “ Determination of the Red Blood Cell Apparent Membrane Elastic Modulus From Viscometric Measurements,” ASME J. Biomech. Eng., 112(3), pp. 241–249. [CrossRef]
Baskurt, O. K. , Hardeman, M. R. , Uyuklu, M. , Ulker, P. , Cengiz, M. , Nemeth, N. , Shin, S. , Alexy, T. , and Meiselman, H. J. , 2009, “ Comparison of Three Commercially Available Ektacytometers With Different Shearing Geometries,” Biorheology, 46(3), pp. 251–264. [PubMed]
Jandl, J. H. , Simmons, R. L. , and Castle, W. B. , 1961, “ Red Cell Filtration and the Pathogenesis of Certain Hemolytic Anemias,” Blood, 18(2), pp. 133–148. http://www.bloodjournal.org/content/18/2/133 [PubMed]
Artmann, G. M. , 1995, “ Microscopic Photometric Quantification of Stiffness and Relaxation Time of Red Blood Cells in a Flow Chamber,” Biorheology, 32(5), pp. 553–570. [CrossRef] [PubMed]
Binnig, G. , Quate, C. , and Gerber, C. , 1986, “ Atomic Force Microscope,” Phys. Rev. Lett., 56(9), pp. 930–933. [CrossRef] [PubMed]
Popescu, G. , Ikeda, T. , Dasari, R. R. , and Feld, M. S. , 2006, “ Diffraction Phase Microscopy for Quantifying Cell Structure and Dynamics,” Opt. Lett., 31(6), pp. 775–777. [CrossRef] [PubMed]
Laurent, V. M. , Hénon, S. , Planus, E. , Fodil, R. , Balland, M. , Isabey, D. , and Gallet, F. , 2002, “ Assessment of Mechanical Properties of Adherent Living Cells by Bead Micromanipulation: Comparison of Magnetic Twisting Cytometry vs Optical Tweezers,” ASME J. Biomech. Eng., 124(4), pp. 408–421. [CrossRef]
Puig-de Morales-Marinkovic, M. , Turner, K. T. , Butler, J. P. , Fredberg, J. J. , and Suresh, S. , 2007, “ Viscoelasticity of the Human Red Blood Cell,” Am. J. Physiol. Cell Physiol., 293(2), pp. C597–C605. [CrossRef] [PubMed]
Evans, E. , and La Celle, P. , 1975, “ Intrinsic Material Properties of the Erythrocyte Membrane Indicated by Mechanical Analysis of Deformation,” Blood, 45(1), pp. 29–43. http://www.bloodjournal.org/content/45/1/29 [PubMed]
Henon, S. , Lenormand, G. , Richert, A. , and Gallet, F. , 1999, “ A New Determination of the Shear Modulus of the Human Erythrocyte Membrane Using Optical Tweezers,” Biophys. J., 76(2), pp. 1145–1151. [CrossRef] [PubMed]
Dao, M. , Lim, C. , and Suresh, S. , 2003, “ Mechanics of the Human Red Blood Cell Deformed by Optical Tweezers,” J. Mech. Phys. Solids, 51(11–12), pp. 2259–2280. [CrossRef]
Boynard, M. , Lelievre, J. C. , and Guillet, R. , 1987, “ Aggregation of Red Blood Cells Studied by Ultrasound Backscattering,” Biorheology, 24(5), pp. 451–461. https://www.ncbi.nlm.nih.gov/pubmed/3446295 [PubMed]
Franceschini, E. , Yu, F. T. H. , Destrempes, F. , and Cloutier, G. , 2010, “ Ultrasound Characterization of Red Blood Cell Aggregation With Intervening Attenuating Tissue-Mimicking Phantoms,” J. Acoust. Soc. Am., 127(2), pp. 1104–1115. [CrossRef] [PubMed]
Dulinska, I. , Targosz, M. , Strojny, W. , Lekka, M. , Czuba, P. , Balwierz, W. , and Szymonski, M. , 2006, “ Stiffness of Normal and Pathological Erythrocytes Studied by Means of Atomic Force Microscopy,” J. Biochem. Biophys. Methods., 66(1–3), pp. 1–11. [CrossRef] [PubMed]
Maciaszek, J. L. , and Lykotrafitis, G. , 2011, “ Sickle Cell Trait Human Erythrocytes are Significantly Stiffer Than Normal,” J. Biomech., 44(4), pp. 657–661. [CrossRef] [PubMed]
Maciaszek, J. L. , Andemariam, B. , and Lykotrafitis, G. , 2011, “ Sickle Cell Trait Human Erythrocytes are Significantly Stiffer Than Normal,” J. Biomech., 46(4), pp. 368–379.
Waugh, R. , and Evans, E. , 1979, “ Thermoelasticity of Red Blood Cell Membrane,” Biophys. J., 26(1), pp. 115–131. [CrossRef] [PubMed]
Park, Y. , Best, C. A. , Auth, T. , Gov, N. S. , Safran, S. A. , Popescu, G. , Suresh, S. , and Feld, M. S. , 2010, “ Metabolic Remodeling of the Human Red Blood Cell Membrane,” Proc. Natl. Acad. Sci. U.S.A., 107(4), pp. 1289–1294. [CrossRef] [PubMed]
Evans, E. , 1973, “ New Membrane Concept Applied to the Analysis of Fluid Shear- and Micropipette-Deformed Red Blood Cells,” Biophys. J., 13(9), pp. 941–954. [CrossRef] [PubMed]
Betz, T. , Lenz, M. , Joanny, J.-F. , and Sykes, C. , 2009, “ ATP-Dependent Mechanics of Red Blood Cells,” Proc. Natl. Acad. Sci. U.S.A., 106(36), pp. 15320–15325. [CrossRef] [PubMed]
Miller, L. H. , Baruch, D. I. , Marsh, K. , and Doumbo, O. K. , 2002, “ The Pathogenic Basis of Malaria,” Nature, 415(6872), pp. 673–679. [CrossRef] [PubMed]
Suresh, S. , Spatz, J. , Mills, J. P. , Micoulet, A. , Dao, M. , Lim, C. T. , Beil, M. , and Seufferlein, T. , 2005, “ Connections Between Single-Cell Biomechanics and Human Disease States: Gastrointestinal Cancer and Malaria,” Acta Biomater., 1(1), pp. 15–30. [CrossRef] [PubMed]
Pauling, L. , Itano, H. A. , Singer, S. J. , and Wells, I. C. , 1949, “ Sickle Cell Anemia, a Molecular Disease,” Science, 110(2865), pp. 543–548. [CrossRef] [PubMed]
Barabino, G. A. , Platt, M. O. , and Kaul, D. K. , 2010, “ Sickle Cell Biomechanics,” Ann. Rev. Biomed. Eng., 12(1), pp. 345–367. [CrossRef]
Perrotta, S. , Gallagher, P. G. , and Mohandas, N. , 2008, “ Hereditary Spherocytosis,” Lancet, 372(9647), pp. 1411–1426. [CrossRef] [PubMed]
Bannerman, R. , and Renwick, J. , 1962, “ The Hereditary Elliptocytoses: Clinical and Linkage Data,” Ann. Hum. Genet., 26(1), pp. 23–38. [CrossRef] [PubMed]
McMillan, D. E. , Utterback, N. G. , and La Puma, J. , 1978, “ Reduced Erythrocyte Deformability in Diabetes,” Diabetes, 27(9), pp. 895–901. [CrossRef] [PubMed]
Schwartz, R. S. , Madsen, J. W. , Rybicki, A. C. , and Nagel, R. L. , 1991, “ Oxidation of Spectrin and Deformability Defects in Diabetic Erythrocytes,” Diabetes, 40(6), pp. 701–708. [CrossRef] [PubMed]
Mohandas, N. , Clark, M. R. , Jacobs, M. S. , and Shohet, S. B. , 1980, “ Analysis of Factors Regulating Erythrocyte Deformability,” J. Clin. Invest., 66(3), pp. 563–573. [CrossRef] [PubMed]
Delaunay, J. , Alloisio, N. , Morle, L. , Baklouti, F. , DallaVenezia, N. , Maillet, P. , and Wilmotte, R. , 1996, “ Molecular Genetics of Hereditary Elliptocytosis and Hereditary Spherocytosis,” Ann. Genet., 39(4), pp. 209–221. https://www.ncbi.nlm.nih.gov/pubmed/9037349 [PubMed]
Wan, J. , Ristenpart, W. D. , and Stone, H. A. , 2008, “ Dynamics of Shear-Induced ATP Release From Red Blood Cells,” Proc. Natl. Acad. Sci. U.S.A., 105(43), pp. 16432–16437. [CrossRef] [PubMed]
Arciero, J. C. , Carlson, B. E. , and Secomb, T. W. , 2008, “ Theoretical Model of Metabolic Blood Flow Regulation: Roles of ATP Release by Red Blood Cells and Conducted Responses,” Am. J. Physiol. Heart Circ. Physiol., 295(4), pp. H1562–H1571. [CrossRef] [PubMed]
Forsyth, A. M. , Wan, J. , Owrutsky, P. D. , Abkarian, M. , and Stone, H. A. , 2011, “ Multiscale Approach to Link Red Blood Cell Dynamics, Shear Viscosity, and ATP Release,” Proc. Natl. Acad. Sci. U.S.A., 108(27), pp. 10986–10991. [CrossRef] [PubMed]
Hines, P. C. , Zen, Q. , Burney, S. N. , Shea, D. A. , Ataga, K. I. , Orringer, E. P. , Telen, M. J. , and Parise, L. V. , 2003, “ Novel Epinephrine and Cyclic Amp-Mediated Activation of BCAM/Lu-Dependent Sickle RBC Adhesion,” Blood, 101(8), pp. 3281–3287. [CrossRef] [PubMed]
Telen, M. J. , 2005, “ Erythrocyte Adhesion Receptors: Blood Group Antigens and Related Molecules,” Transfus. Med. Rev., 19(1), pp. 32–44. [CrossRef] [PubMed]
Maciaszek, J. L. , Andemariam, B. , Abiraman, K. , and Lykotrafitis, G. , 2014, “ Akap-Dependent Modulation of BCAM/Lu Adhesion on Normal and Sickle Cell Disease RBCs Revealed by Force Nanoscopy,” Biophys. J., 106(6), pp. 1258–1267. [CrossRef] [PubMed]
Park, Y. , Diez-Silva, M. , Popescu, G. , Lykotrafitis, G. , Choi, W. , Feld, M. S. , and Suresh, S. , 2008, “ Refractive Index Maps and Membrane Dynamics of Human Red Blood Cells Parasitized by Plasmodium Falciparum,” Proc. Natl. Acad. Sci. U.S.A., 105(37), pp. 13730–13735. [CrossRef] [PubMed]
An, X. , and Mohandas, N. , 2008, “ Disorders of Red Cell Membrane,” Brit. J. Haematol., 141(3), pp. 367–375.
Cristini, V. , and Kassab, G. S. , 2005. “ Computer Modeling of Red Blood Cell Rheology in the Microcirculation: A Brief Overview,” Ann. Biomed. Eng., 33(12), pp. 1724–1727. [CrossRef] [PubMed]
Wan, J. , Forsyth, A. M. , and Stone, H. A. , 2011, “ Red Blood Cell Dynamics: From Cell Deformation to ATP Release,” Integr. Biol., 3(10), pp. 972–981. [CrossRef]
Li, X. J. , Vlahovska, P. V. , and Karniadakis, G. E. , 2013, “ Continuum- and Particle-Based Modeling of Shapes and Dynamics of Red Blood Cells in Health and Disease,” Soft Matter, 9(1), pp. 28–37. [CrossRef] [PubMed]
Fedosov, D. A. , Dao, M. , Karniadakis, G. E. , and Suresh, S. , 2014, “ Computational Biorheology of Human Blood Flow in Health and Disease,” Ann. Biomed. Eng., 42(2), pp. 368–387. [CrossRef] [PubMed]
Freund, J. B. , 2014, “ Numerical Simulation of Flowing Blood Cells,” Ann. Rev. Fluid Mech., 46(1), pp. 67–95. [CrossRef]
Yazdani, A. , Li, X. J. , and Karniadakis, G. E. , 2016, “ Dynamic and Rheological Properties of Soft Biological Cell Suspensions,” Rheol. Acta, 55(6), pp. 433–447. [CrossRef] [PubMed]
Gompper, G. , and Fedosov, D. A. , 2016, “ Modeling Microcirculatory Blood Flow: Current State and Future Perspectives,” Wiley Interdiscip. Rev. Syst. Biol. Med., 8(2), pp. 157–168. [CrossRef] [PubMed]
Peskin, C. S. , 2002, “ The Immersed Boundary Method,” Acta Numer., 11, pp. 479–517. [CrossRef]
Doddi, S. K. , and Bagchi, P. , 2009, “ Three-Dimensional Computational Modeling of Multiple Deformable Cells Flowing in Microvessels,” Phys. Rev. E, 79(4), p. 046318. [CrossRef]
Zhao, H. , Isfahani, A. H. , Olson, L. N. , and Freund, J. B. , 2010, “ A Spectral Boundary Integral Method for Flowing Blood Cells,” J. Comput. Phys., 229(10), pp. 3726–3744. [CrossRef]
Veerapaneni, S. K. , Rahimian, A. , Biros, G. , and Zorin, D. , 2011, “ A Fast Algorithm for Simulating Vesicle Flows in Three Dimensions,” J. Comput. Phys., 230(14), pp. 5610–5634. [CrossRef]
Kumar, A. , and Graham, M. D. , 2012, “ Accelerated Boundary Integral Method for Multiphase Flow in Non-Periodic Geometries,” J. Comput. Phys., 231(20), pp. 6682–6713. [CrossRef]
Boal, D. H. , Seifert, U. , and Zilker, A. , 1992, “ Dual Network Model for Red Blood Cell Membranes,” Phys. Rev. Lett., 69(23), pp. 3405–3408. [CrossRef] [PubMed]
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(3), pp. 1584–1597. [CrossRef] [PubMed]
Noguchi, H. , and Gompper, G. , 2005, “ Shape Transitions of Fluid Vesicles and Red Blood Cells in Capillary Flows,” Proc. Natl. Acad. Sci. U.S.A., 102(40), pp. 14159–14164. [CrossRef] [PubMed]
Li, J. , Dao, M. , Lim, C. T. , and Suresh, S. , 2005, “ Spectrin-Level Modeling of the Cytoskeleton and Optical Tweezers Stretching of the Erythrocyte,” Biophys. J., 88(5), pp. 3707–3719. [CrossRef] [PubMed]
Li, J. , Lykotrafitis, G. , Dao, M. , and Suresh, S. , 2007, “ Cytoskeletal Dynamics of Human Erythrocyte,” Proc. Natl. Acad. Sci. U.S.A., 104(12), pp. 4937–4942. [CrossRef] [PubMed]
Pivkin, I. V. , and Karniadakis, G. E. , 2008, “ Accurate Coarse-Grained Modeling of Red Blood Cells,” Phys. Rev. Lett., 101(11), p. 118105. [CrossRef] [PubMed]
Fedosov, D. A. , Caswell, B. , and Karniadakis, G. E. , 2010, “ A Multiscale Red Blood Cell Model With Accurate Mechanics, Rheology, and Dynamics,” Biophys. J., 98(10), pp. 2215–2225. [CrossRef] [PubMed]
Pan, W. , Caswell, B. , and Karniadakis, G. E. , 2010, “ A Low-Dimensional Model for the Red Blood Cell,” Soft Matter, 6(18), pp. 4366–4376. [CrossRef]
Peng, Z. , Li, X. J. , Pivkin, I. V. , Dao, M. , Karniadakis, G. E. , and Suresh, S. , 2013, “ Lipid–Bilayer and Cytoskeletal Interactions in a Red Blood Cell,” Proc. Natl. Acad. Sci. U.S.A., 110(33), pp. 13356–13361. [CrossRef] [PubMed]
Tran-Son-Tay, R. , Sutera, S. , and Rao, P. , 1984, “ Determination of Red Blood Cell Membrane Viscosity From Rheoscopic Observations of Tank-Treading Motion,” Biophys. J., 46(1), pp. 65–72. [CrossRef] [PubMed]
Fischer, T. M. , 2004, “ Shape Memory of Human Red Blood Cells,” Biophys. J., 86(5), pp. 3304–3313. [CrossRef] [PubMed]
Fischer, T. M. , 2007, “ Tank-Tread Frequency of the Red Cell Membrane: Dependence on the Viscosity of the Suspending Medium,” Biophys. J., 93(7), pp. 2553–2561. [CrossRef] [PubMed]
Abkarian, M. , Faivre, M. , and Viallat, A. , 2007, “ Swinging of Red Blood Cells Under Shear Flow,” Phys. Rev. Lett., 98(18), p. 188302. [CrossRef] [PubMed]
Skotheim, J. M. , and Secomb, T. W. , 2007, “ Red Blood Cells and Other Nonspherical Capsules in Shear Flow: Oscillatory Dynamics and the Tank-Treading-to-Tumbling Transition,” Phys. Rev. Lett., 98(7), p. 078301. [CrossRef] [PubMed]
Fedosov, D. A. , Noguchi, H. , and Gompper, G. , 2014, “ Multiscale Modeling of Blood Flow: From Single Cells to Blood Rheology,” Biomech. Model Mechanobiol., 13(2), pp. 239–258. [CrossRef] [PubMed]
Zhang, Y. , Huang, C. , Kim, S. , Golkaram, M. , Dixon, M. W. A. , Tilley, L. , Li, J. , Zhang, S. , and Suresh, S. , 2015, “ Multiple Stiffening Effects of Nanoscale Knobs on Human Red Blood Cells Infected With Plasmodium Falciparum Malaria Parasite,” Proc. Natl. Acad. Sci. U.S.A., 112(19), pp. 6068–6073. [CrossRef] [PubMed]
Ramanujan, S. , and 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, pp. 117–143. [CrossRef]
Lac, E. , Barthes-Biesel, D. , Pelekasis, N. , and Tsamopoulos, J. , 2004, “ Spherical Capsules in Three-Dimensional Unbounded Stokes Flows: Effect of the Membrane Constitutive Law and Onset of Buckling,” J. Fluid Mech., 516, pp. 303–334. [CrossRef]
Yazdani, A. Z. , and Bagchi, P. , 2011, “ Phase Diagram and Breathing Dynamics of a Single Red Blood Cell and a Biconcave Capsule in Dilute Shear Flow,” Phys, Rev, E, 84(2), p. 026314. [CrossRef]
Fai, T. G. , Griffith, B. E. , Mori, Y. , and Peskin, C. S. , 2013, “ Immersed Boundary Method for Variable Viscosity and Variable Density Problems Using Fast Constant-Coefficient Linear Solvers—I: Numerical Method and Results,” SIAM J. Sci. Comput., 35(5), pp. B1132–B1161. [CrossRef]
Shi, L. , Pan, T.-W. , and Glowinski, R. , 2014, “ Three-Dimensional Numerical Simulation of Red Blood Cell Motion in Poiseuille Flows,” Int. J. Numer. Methods Fluids, 76(7), pp. 397–415. [CrossRef]
Hao, W. , Xu, Z. , Liu, C. , and Lin, G. , 2015, “ A Fictitious Domain Method With a Hybrid Cell Model for Simulating Motion of Cells in Fluid Flow,” J. Comput. Phys., 280, pp. 345–362. [CrossRef]
Pozrikidis, C. , 1992, Boundary Integral and Singularity Methods for Linearized Viscous Flow, Cambridge University Press, Cambridge, UK.
Sui, Y. , Low, H. , Chew, Y. , and Roy, P. , 2008, “ Tank-Treading, Swinging, and Tumbling of Liquid-Filled Elastic Capsules in Shear Flow,” Phys. Rev. E, 77(1), p. 016310. [CrossRef]
Clausen, J. R. , Reasor, D. A. , and Aidun, C. K. , 2011, “ The Rheology and Microstructure of Concentrated Non-Colloidal Suspensions of Deformable Capsules,” J. Fluid Mech., 685, pp. 202–234. [CrossRef]
Zhang, J. , Johnson, P. C. , and Popel, A. S. , 2007, “ An Immersed Boundary-Lattice Boltzmann Approach to Simulate Deformable Liquid Capsules and Its Application to Microscopic Blood Flows,” Phys. Biol., 4(4), pp. 285–295. [CrossRef] [PubMed]
Zhang, J. , Johnson, P. C. , and Popel, A. S. , 2008, “ Red Blood Cell Aggregation and Dissociation in Shear Flows Simulated by Lattice Boltzmann Method,” J. Biomech., 41(1), pp. 47–55. [CrossRef] [PubMed]
Krüger, T. , Varnik, F. , and Raabe, D. , 2011, “ Efficient and Accurate Simulations of Deformable Particles Immersed in a Fluid Using a Combined Immersed Boundary Lattice Boltzmann Finite Element Method,” Comput. Math. Appl., 61(12), pp. 3485–3505. [CrossRef]
Reasor, D. A. , Clausen, J. R. , and Aidun, C. K. , 2012, “ Coupling the Lattice-Boltzmann and Spectrin-Link Methods for the Direct Numerical Simulation of Cellular Blood Flow,” Int. J. Numer. Methods Fluids, 68(6), pp. 767–781. [CrossRef]
Reasor, D. A. , Clausen, J. R. , and Aidun, C. K. , 2013, “ Rheological Characterization of Cellular Blood in Shear,” J. Fluid Mech., 726, pp. 497–516. [CrossRef]
Li, H. , and Lykotrafitis, G. , 2012, “ Two-Component Coarse-Grained Molecular-Dynamics Model for the Human Erythrocyte Membrane,” Biophys. J., 102(1), pp. 75–84. [CrossRef] [PubMed]
Li, H. , and Lykotrafitis, G. , 2014, “ Erythrocyte Membrane Model With Explicit Description of the Lipid Bilayer and the Spectrin Network,” Biophys. J., 107(3), pp. 642–653. [CrossRef] [PubMed]
Fedosov, D. A. , Peltomäki, M. , and Gompper, G. , 2014, “ Deformation and Dynamics of Red Blood Cells in Flow Through Cylindrical Microchannels,” Soft Matter, 10(24), pp. 4258–4267. [CrossRef] [PubMed]
Hosseini, S. M. , and Feng, J. J. , 2012, “ How Malaria Parasites Reduce the Deformability of Infected Red Blood Cells,” Biophys. J., 103(1), pp. 1–10. [CrossRef] [PubMed]
Wu, T. H. , and Feng, J. J. , 2013, “ Simulation of Malaria-Infected Red Blood Cells in Microfluidic Channels: Passage and Blockage,” Biomicrofluidics, 7(4), p. 044115. [CrossRef]
McWhirter, J. L. , Noguchi, H. , and Gompper, G. , 2009, “ Flow-Induced Clustering and Alignment of Vesicles and Red Blood Cells in Microcapillaries,” Proc. Natl. Acad. Sci. U.S.A., 106(15), pp. 6039–6043. [CrossRef] [PubMed]
Fedosov, D. A. , Caswell, B. , Suresh, S. , and Karniadakis, G. E. , 2011, “ Quantifying the Biophysical Characteristics of Plasmodium-Falciparum-Parasitized Red Blood Cells in Microcirculation,” Proc. Natl. Acad. Sci. U.S.A., 108(1), pp. 35–39. [CrossRef] [PubMed]
Li, X. J. , Popel, A. S. , and Karniadakis, G. E. , 2012, “ Blood-Plasma Separation in Y-Shaped Bifurcating Microfluidic Channels: A Dissipative Particle Dynamics Simulation Study,” Phys. Biol., 9(2), p. 026010. [CrossRef] [PubMed]
Lei, H. , and Karniadakis, G. E. , 2013, “ Probing Vasoocclusion Phenomena in Sickle Cell Anemia Via Mesoscopic Simulations,” Proc. Natl. Acad. Sci. U.S.A., 110(28), pp. 11326–11330. [CrossRef] [PubMed]
Lykov, K. , Li, X. J. , Pivkin, I. V. , and Karniadakis, G. E. , 2015, “ Inflow/Outflow Boundary Conditions for Particle-Based Blood Flow Simulations: Application to Arterial Bifurcations and Trees,” PLOS Comput. Biol., 11(8), p. e1004410. [CrossRef] [PubMed]
Yazdani, A. , and Karniadakis, G. E. , 2016, “ Sub-Cellular Modeling of Platelet Transport in Blood Flow Through Microchannels With Constriction,” Soft Matter, 12(19), pp. 4339–4351. [CrossRef] [PubMed]
Li, H. , Zhang, Y. H. , Ha, V. , and Lykotrafitis, G. , 2016, “ Modeling of Band-3 Protein Diffusion in the Normal and Defective Red Blood Cell Membrane,” Soft Matter, 12(15), pp. 3643–3653. [CrossRef] [PubMed]
Helfrich, W. , 1973, “ Elastic Properties of Lipid Bilayers: Theory and Possible Experiments,” Z. Naturforsch. C, 28(11–12), pp. 693–703. [CrossRef] [PubMed]
Seifert, U. , Berndl, K. , and Lipowsky, R. , 1991, “ Shape Transformations of Vesicles: Phase Diagram for Spontaneous- Curvature and Bilayer-Coupling Models,” Phys. Rev. A, 44(2), pp. 1182–1202. [CrossRef] [PubMed]
Svetina, S. , and Zeks, B. , 1989, “ Membrane Bending Energy and Shape Determination of Phospholipid Vesicles and Red Blood Cells,” Eur. Biophys. J., 17(2), pp. 101–111. [CrossRef] [PubMed]
Heinrich, V. , Svetina, S. , and Žekš, B. , 1993, “ Nonaxisymmetric Vesicle Shapes in a Generalized Bilayer-Couple Model and the Transition Between Oblate and Prolate Axisymmetric Shapes,” Phys. Rev. E, 48(4), pp. 3112–3123. [CrossRef]
Miao, L. , Seifert, U. , Wortis, M. , and Dobereiner, H. G. , 1994, “ Budding Transitions of Fluid-Bilayer Vesicles: The Effect of Area-Difference Elasticity,” Phys. Rev. E, 49(6), pp. 5389–5407. [CrossRef]
Li, X. J. , Pivkin, I. V. , Liang, H. J. , and Karniadakis, G. E. , 2009, “ Shape Transformations of Membrane Vesicles From Amphiphilic Triblock Copolymers: A Dissipative Particle Dynamics Simulation Study,” Macromolecules, 42(8), pp. 3195–3200. [CrossRef]
Khairy, K. , and Howard, J. , 2011, “ Minimum-Energy Vesicle and Cell Shapes Calculated Using Spherical Harmonics Parameterization,” Soft Matter, 7(5), pp. 2138–2143. [CrossRef]
Paessler, M. , and Hartung, H. , 2015, “ Dehydrated Hereditary Stomatocytosis Masquerading as MDS,” Blood, 125(11), pp. 1841–1841. [CrossRef] [PubMed]
Bain, B. J. , 2005, “ Diagnosis From the Blood Smear,” N. Engl. J. Med., 353(5), pp. 498–507. [CrossRef] [PubMed]
Hernandez, J. D. H. , Villasenor, O. R. , Alvarado, J. D. R. , Lucach, R. O. , Zarate, A. , Saucedo, R. , and Hernandez-Valencia, M. , 2015, “ Morphological Changes of Red Blood Cells in Peripheral Blood Smear of Patients With Pregnancy-Related Hypertensive Disorders,” Arch. Med. Res., 46(6), pp. 479–483. [CrossRef] [PubMed]
Young, L. E. , Izzo, M. J. , and Platzer, R. F. , 1951, “ Hereditary Spherocytosis,” Blood, 6(11), pp. 1073–1098. http://www.bloodjournal.org/content/6/11/1073 [PubMed]
Agre, P. , Casella, J. F. , Zinkham, W. H. , McMillan, C. , and Bennett, V. , 1985, “ Partial Deficiency of Erythrocyte Spectrin in Hereditary Spherocytosis,” Nature, 314(6009), pp. 380–383. [CrossRef] [PubMed]
Tomaselli, M. B. , John, K. M. , and Lux, S. E. , 1981, “ Elliptical Erythrocyte Membrane Skeletons and Heat-Sensitive Spectrin in Hereditary Elliptocytosis,” Proc. Natl. Acad. Sci. U.S.A., 78(3), pp. 1911–1915. [CrossRef] [PubMed]
Marchesi, S. L. , Letsinger, J. T. , Speicher, D. W. , Marchesi, V. T. , Agre, P. , Hyun, B. , and Gulati, G. , 1987, “ Mutant Forms of Spectrin Alpha-Subunits in Hereditary Elliptocytosis,” J. Clin. Invest., 80(1), pp. 191–198. [CrossRef] [PubMed]
Liu, S. C. , Palek, J. , Prchal, J. , and Castleberry, R. P. , 1981, “ Altered Spectrin Dimer-Dimer Association and Instability of Erythrocyte Membrane Skeletons in Hereditary Pyropoikilocytosis,” J. Clin. Invest., 68(3), pp. 597–605. [CrossRef] [PubMed]
Knowles, W. J. , Morrow, J. S. , Speicher, D. W. , Zarkowsky, H. S. , Mohandas, N. , Mentzer, W. C. , Shohet, S. B. , and Marchesi, V. T. , 1983, “ Molecular and Functional Changes in Spectrin From Patients With Hereditary Pyropoikilocytosis,” J. Clin. Invest., 71(6), pp. 1867–1877. [CrossRef] [PubMed]
Hsu, R. , Kanofsky, J. , and Yachnin, S. , 1980, “ The Formation of Echinocytes by the Insertion of Oxygenated Sterol Compounds Into Red Cell Membranes,” Blood, 56(1), pp. 109–117. http://www.bloodjournal.org/content/56/1/109 [PubMed]
Harlan, W. R. , Shaw, W. A. , and Zelkowitz, M. , 1976, “ Echinocytes and Acquired Deficiency of Plasma Lipoproteins in Burned Patients,” Arch. Intern. Med., 136(1), pp. 71–76. [CrossRef] [PubMed]
Smith, J. A. , Lonergan, E. T. , and Sterling, K. , 1964, “ Spur-Cell Anemia,” N. Engl. J. Med., 271(8), pp. 396–398. [CrossRef] [PubMed]
McBride, J. A. , and Jacob, H. S. , 1970, “ Abnormal Kinetics of Red Cell Membrane Cholesterol in Acanthocytes: Studies in Genetic and Experimental Abetalipoproteinaemia and in Spur Cell Anaemia,” Br. J. Haematol., 18(4), pp. 383–398. [CrossRef] [PubMed]
Reinhart, W. , and Chien, S. , 1986, “ Red Cell Rheology in Stomatocyte-Echinocyte Transformation: Roles of Cell Geometry and Cell Shape,” Blood, 67(4), pp. 1110–1118. http://www.bloodjournal.org/content/67/4/1110 [PubMed]
Fischer, T. , Haest, C. W. , Stöhr-Liesen, M. , Schmid-Schönbein, H. , and Skalak, R. , 1981, “ The Stress-Free Shape of the Red Blood Cell Membrane,” Biophys. J., 34(3), pp. 409–422. [CrossRef] [PubMed]
Bull, B. S. , and Kuhn, I. N. , 1970, “ The Production of Schistocytes by Fibrin Strands (A Scanning Electron Microscope Study),” Blood, 35(1), pp. 104–111. http://www.bloodjournal.org/content/35/1/104 [PubMed]
Heyes, H. , Köhle, W. , and Slijepcevic, B. , 1976, “ The Appearance of Schistocytes in the Peripheral Blood in Correlation to the Degree of Disseminated Intravascular Coagulation,” Pathophysiol. Haemostasis Thromb., 5(2), pp. 66–73. [CrossRef]
Kaul, D. K. , Fabry, M. E. , Windisch, P. , Baez, S. , and Nagel, R. L. , 1983, “ Erythrocytes in Sickle Cell Anemia are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest., 72(1), pp. 22–31. [CrossRef] [PubMed]
Evans, E. , Mohandas, N. , and Leung, A. , 1984, “ Static and Dynamics Rigidities of Normal and Sickle Erythrocytes: Major Influence of Cell Hemoglobin Concentration,” J. Clin. Invest., 73(2), pp. 477–488. [CrossRef] [PubMed]
Gallagher, P. G. , 2005, “ Red Cell Membrane Disorders,” Hematol. Am. Soc. Hematol. Educ. Program, 2005(1), pp. 13–18.
Seifert, U. , 1997, “ Configurations of Fluid Membranes and Vesicles,” Adv. Phys., 46(1), pp. 13–137. [CrossRef]
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(26), pp. 16766–16769. [CrossRef] [PubMed]
Spangler, E. J. , Harvey, C. W. , Revalee, J. D. , Kumar, P. B. S. , and Laradji, M. , 2011, “ Computer Simulation of Cytoskeleton-Induced Blebbing in Lipid Membranes,” Phys. Rev. E, 84(5), p. 051906. [CrossRef]
Gov, N. , Cluitmans, J. , Sens, P. , and Bosman, G. , 2009, “ Cytoskeletal Control of Red Blood Cell Shape: Theory and Practice of Vesicle Formation,” Advances in Planar Lipid Bilayers and Liposomes, Vol. 10, Academic Press, San Diego, California, pp. 95–119.
Li, H. , and Lykotrafitis, G. , 2015, “ Vesiculation of Healthy and Defective Red Blood Cells,” Phys. Rev. E, 92(1), p. 012715. [CrossRef]
Sens, P. , and Gov, N. , 2007, “ Force Balance and Membrane Shedding at the Red-Blood-Cell Surface,” Phys. Rev. Lett., 98(1), p. 018102. [CrossRef] [PubMed]
Hess, J. R. , 2014, “ Measures of Stored Red Blood Cell Quality,” Vox Sang., 107(1), pp. 1–9. [CrossRef] [PubMed]
Greenwalt, T. J. , 2006, “ The How and Why of Exocytic Vesicles,” Transfusion, 46(1), pp. 143–152. [CrossRef] [PubMed]
Alaarg, A. , Schiffelers, R. , van Solinge, W. W. , and Van Wijk, R. , 2013, “ Red Blood Cell Vesiculation in Hereditary Hemolytic Anemia,” Front. Physiol., 4, p. 365. [CrossRef] [PubMed]
Lei, H. , and Karniadakis, G. E. , 2012, “ Predicting the Morphology of Sickle Red Blood Cells Using Coarse-Grained Models of Intracellular Aligned Hemoglobin Polymers,” Soft Matter, 8(16), pp. 4507–4516. [CrossRef]
Quinn, D. J. , Pivkin, I. V. , Wong, S. K. , Chiam, K. H. , Dao, M. , Karniadakis, G. E. , and Suresh, S. , 2011, “ Combined Simulation and Experimental Study of Large Deformation of Red Blood Cells in Microfluidic Systems,” Ann. Biomed. Eng., 39(3), pp. 1041–1050. [CrossRef] [PubMed]
Imai, Y. , Kondo, H. , Ishikawa, T. , Lim, C. T. , and Yamaguchi, T. , 2010, “ Modeling of Hemodynamics Arising From Malaria Infection,” J. Biomech., 43(7), pp. 1386–1393. [CrossRef] [PubMed]
Fedosov, D. A. , Lei, H. , Caswell, B. , Suresh, S. , and Karniadakis, G. E. , 2011, “ Multiscale Modeling of Red Blood Cell Mechanics and Blood Flow in Malaria,” PLOS Comput. Biol., 7(12), p. e1002270. [CrossRef] [PubMed]
Ye, T. , Phan-Thien, N. , Khoo, B. C. , and Lim, C. T. , 2013, “ Stretching and Relaxation of Malaria-Infected Red Blood Cells,” Biophys. J., 105(5), pp. 1103–1109. [CrossRef] [PubMed]
Imai, Y. , Nakaaki, K. , Kondo, H. , Ishikawa, T. , Lim, C. T. , and Yamaguchi, T. , 2011, “ Margination of Red Blood Cells Infected by Plasmodium Falciparum in a Microvessel,” J. Biomech., 44(8), pp. 1553–1558. [CrossRef] [PubMed]
Aingaran, M. , Zhang, R. , Law, S. K. Y. , Peng, Z. L. , Undisz, A. , Meyer, E. , Diez-Silva, M. , Burke, T. A. , Spielmann, T. , Lim, C. T. , Suresh, S. , Dao, M. , and Marti, M. , 2012, “ Host Cell Deformability is Linked to Transmission in the Human Malaria Parasite Plasmodium Falciparum,” Cell Microbiol., 14(7), pp. 983–993. [CrossRef] [PubMed]
Bow, H. , Pivkin, I. V. , Diez-Silva, M. , Goldfless, S. J. , Dao, M. , Niles, J. C. , Suresh, S. , and Han, J. , 2011, “ A Microfabricated Deformability-Based Flow Cytometer With Application to Malaria,” Lab Chip, 11(6), pp. 1065–1073. [CrossRef] [PubMed]
Ye, T. , Phan-Thien, N. , Khoo, B. C. , and Lim, C. T. , 2014, “ Numerical Modelling of a Healthy/Malaria-Infected Erythrocyte in Shear Flow Using Dissipative Particle Dynamics Method,” J. Appl. Phys., 115(22), p. 224701. [CrossRef]
Fedosov, D. A. , Caswell, B. , and Karniadakis, G. E. , 2011, “ Wall Shear Stress-Based Model for Adhesive Dynamics of Red Blood Cells in Malaria,” Biophys. J., 100(9), pp. 2084–2093. [CrossRef] [PubMed]
Hou, H. W. , Bhagat, A. A. S. , Lee, W. C. , Huang, S. , Han, J. , and Lim, C. T. , 2011, “ Microfluidic Devices for Blood Fractionation,” Micromachines, 2(4), p. 319. [CrossRef]
Chien, S. , Usami, S. , and Bertles, J. F. , 1970, “ Abnormal Rheology of Oxygenated Blood in Sickle Cell Anemia,” J. Clin. Invest., 49(4), pp. 623–634. [CrossRef] [PubMed]
Kaul, D. K. , and Xue, H. , 1991, “ Rate of Deoxygenation and Rheologic Behavior of Blood in Sickle Cell Anemia,” Blood, 77(6), pp. 1353–1361. http://www.bloodjournal.org/content/77/6/1353 [PubMed]
Ferrone, F. A. , Hofrichter, J. , and Eaton, W. A. , 1985, “ Kinetics of Sickle Hemoglobin Polymerization II: A Double Nucleation Mechanism,” J. Mol. Biol., 183(4), pp. 611–631. [CrossRef] [PubMed]
Vekilov, P. G. , 2007, “ Sickle-Cell Haemoglobin Polymerization: Is It the Primary Pathogenic Event of Sickle-Cell Anaemia?,” Br. J. Haematol., 139(2), pp. 173–184. [CrossRef] [PubMed]
Lu, L. , Li, X. J. , Vekilov, P. G. , and Karniadakis, G. E. , 2016, “ Probing the Twisted Structure of Sickle Hemoglobin Fibers Via Particle Simulations,” Biophys. J., 110(9), pp. 2085–2093. [CrossRef] [PubMed]
Li, X. J. , Caswell, B. , and Karniadakis, G. E. , 2012, “ Effect of Chain Chirality on the Self-Assembly of Sickle Hemoglobin,” Biophys. J., 103(6), pp. 1130–1140. [CrossRef] [PubMed]
Li, H. , and Lykotrafitis, G. , 2011, “ A Coarse-Grain Molecular Dynamics Model for Sickle Hemoglobin Fibers,” J. Mech. Behav. Biomed. Mater., 4(2), pp. 162–173. [CrossRef] [PubMed]
Li, H. , Ha, V. , and Lykotrafitis, G. , 2012, “ Modeling Sickle Hemoglobin Fibers as One Chain of Coarse-Grained Particles,” J. Biomech., 45(11), pp. 1947–1951. [CrossRef] [PubMed]
Liu, S. C. , Derick, L. H. , Zhai, S. , and Palek, J. , 1991, “ Uncoupling of the Spectrin-Based Skeleton From the Lipid Bilayer in Sickled Red Cells,” Science, 252(5005), pp. 574–576. [CrossRef] [PubMed]
Odiévre, M.-H. , Verger, E. , Silva-Pinto, A. C. , and Elion, J. , 2011, “ Pathophysiological Insights in Sickle Cell Disease,” Indian J. Med. Res., 134(4), pp. 532–537. http://www.ijmr.org.in/text.asp?2011/134/4/532/89895 [PubMed]
Dupin, M. , Halliday, I. , Care, C. M. , and Munn, L. L. , 2008, “ Lattice Boltzmann Modeling of Blood Cell Dynamics,” Int. J. Comput. Fluid Dyn., 22(7), pp. 481–492. [CrossRef]
Chang, H.-Y. , Li, X. J. , Li, H. , and Karniadakis, G. E. , 2016, “ MD/DPD Multiscale Framework for Predicting Morphology and Stresses of Red Blood Cells in Health and Disease,” PLOS Comput. Biol., 12(10), p. e1005173. [CrossRef] [PubMed]
Kodippili, G. C. , Spector, J. , Sullivan, C. , Kuypers, F. A. , Labotka, R. , Gallagher, P. G. , Ritchie, K. , and Low, P. S. , 2009, “ Imaging of the Diffusion of Single Band 3 Molecules on Normal and Mutant Erythrocytes,” Blood, 113(24), pp. 6237–6245. [CrossRef] [PubMed]
Cho, M. R. , Eber, S. W. , Liu, S.-C. , Lux, S. E. , and Golan, D. E. , 1998, “ Regulation of Band 3 Rotational Mobility by Ankyrin in Intact Human Red Cells,” Biochemistry, 37(51), pp. 17828–17835. [CrossRef] [PubMed]
Tsuji, A. , and Ohnishi, S. , 1986, “ Restriction of the Lateral Motion of Band 3 in the Erythrocyte Membrane by the Cytoskeletal Network: Dependence on Spectrin Association State,” Biochemistry, 25(20), pp. 6133–6139. [CrossRef] [PubMed]
Schindler, M. , Koppel, D. E. , and Sheetz, M. P. , 1980, “ Modulation of Membrane Protein Lateral Mobility by Polyphosphates and Polyamines,” Proc. Natl. Acad. Sci. U.S.A., 77(3), pp. 1457–1461. [CrossRef] [PubMed]
Sheetz, M. P. , Febbroriello, P. , and Koppel, D. E. , 1982, “ Triphosphoinositide Increases Glycoprotein Lateral Mobility in Erythrocyte Membranes,” Nature, 296(5852), pp. 91–93. [CrossRef] [PubMed]
Smith, D. K. , and Palek, J. , 1982, “ Modulation of Lateral Mobility of Band 3 in the Red Cell Membrane by Oxidative Cross-Linking of Spectrin,” Nature, 297(5865), pp. 424–425. [CrossRef] [PubMed]
Saxton, M. J. , 1995, “ Single-Particle Tracking: Effects of Corrals,” Biophys. J., 69(2), pp. 389–398. [CrossRef] [PubMed]
Saxton, M. J. , 1989, “ The Spectrin Network as a Barrier to Lateral Diffusion in Erythrocytes: A Percolation Analysis,” Biophys. J., 55(1), pp. 21–28. [CrossRef] [PubMed]
Saxton, M. J. , 1990, “ The Membrane Skeleton of Erythrocytes: A Percolation Model,” Biophys. J., 57(6), pp. 1167–1177. [CrossRef] [PubMed]
Saxton, M. J. , 1990, “ The Membrane Skeleton of Erythrocytes: Models of Its Effect on Lateral Diffusion,” Int. J. Biochem. Cell Biol., 22(8), pp. 801–809.
Brown, F. L. , Leitner, D. M. , McCammon, J. A. , and Wilson, K. R. , 2000, “ Lateral Diffusion of Membrane Proteins in the Presence of Static and Dynamic Corrals: Suggestions for Appropriate Observables,” Biophys. J., 78(5), pp. 2257–2269. [CrossRef] [PubMed]
Kenkre, V. M. , Giuggioli, L. , and Kalay, Z. , 2008, “ Molecular Motion in Cell Membranes: Analytic Study of Fence-Hindered Random Walks,” Phys. Rev. E, 77(5), p. 051907. [CrossRef]
Auth, T. , and Gov, N. S. , 2009, “ Diffusion in a Fluid Membrane With a Flexible Cortical Cytoskeleton,” Biophys. J., 96(3), pp. 818–830. [CrossRef] [PubMed]
Bouchaud, J.-P. , and Georges, A. , 1990, “ Anomalous Diffusion in Disordered Media: Statistical Mechanisms, Models and Physical Applications,” Phys. Rep., 195(4–5), pp. 127–293. [CrossRef]
Saxton, M. J. , 2007, “ A Biological Interpretation of Transient Anomalous Subdiffusion—I: Qualitative Model,” Biophys. J., 92(4), pp. 1178–1191. [CrossRef] [PubMed]
Powles, J. G. , Mallett, M. J. D. , Rickayzen, G. , and Evans, W. A. B. , 1992, “ Exact Analytic Solutions for Diffusion Impeded by an Infinite Array of Partially Permeable Barriers,” Proc. R. Soc. London A Math. Phys. Sci., 436(1897), pp. 391–403. [CrossRef]
Daumas, F. , Destainville, N. , Millot, C. , Lopez, A. , Dean, D. , and Salome, L. , 2003, “ Confined Diffusion Without Fences of a G-Protein-Coupled Receptor as Revealed by Single Particle Tracking,” Biophys. J., 84(1), pp. 356–366. [CrossRef] [PubMed]
Brown, C. D. , Ghali, H. S. , Zhao, Z. , Thomas, L. L. , and Friedman, E. A. , 2005, “ Association of Reduced Red Blood Cell Deformability and Diabetic Nephropathy,” Kidney Int., 67(1), pp. 295–300. [CrossRef] [PubMed]
Agrawal, R. , Smart, T. , Nobre-Cardoso, J. , Richards, C. , Bhatnagar, R. , Tufail, A. , Shima, D. , Jones, P. H. , and Pavesio, C. , 2016, “ Assessment of Red Blood Cell Deformability in Type 2 Diabetes Mellitus and Diabetic Retinopathy by Dual Optical Tweezers Stretching Technique,” Sci. Rep., 6, p. 15873. [CrossRef] [PubMed]
Shin, S. , Ku, Y.-H. , Ho, J.-X. , Kim, Y.-K. , Suh, J.-S. , and Singh, M. , 2007, “ Progressive Impairment of Erythrocyte Deformability as Indicator of Microangiopathy in Type 2 Diabetes Mellitus,” Clin. Hemorheol. Micro., 36(1), pp. 253–261. http://content.iospress.com/articles/clinical-hemorheology-and-microcirculation/ch977
Chien, S. , 1987, “ Red Cell Deformability and Its Relevance to Blood Flow,” Ann. Rev. Physiol., 49(1), pp. 177–192. [CrossRef]
Tsukada, K. , Sekizuka, E. , Oshio, C. , and Minamitani, H. , 2001, “ Direct Measurement of Erythrocyte Deformability in Diabetes Mellitus With a Transparent Microchannel Capillary Model and High-Speed Video Camera System,” Microvasc. Res., 61(3), pp. 231–239. [CrossRef] [PubMed]
Singh, M. , and Shin, S. , 2009, “ Changes in Erythrocyte Aggregation and Deformability in Diabetes Mellitus: A Brief Review,” Indian J. Exp. Biol., 47(1), pp. 7–15. http://www.niscair.res.in/sciencecommunication/researchjournals/rejour/ijeb/ijeb2k9/ijeb_jan09.asp#7 [PubMed]
Tomaiuolo, G. , 2014, “ Biomechanical Properties of Red Blood Cells in Health and Disease Towards Microfluidics,” Biomicrofluidics, 8(5), p. 051501. [CrossRef] [PubMed]
Kim, J. , Lee, H. , and Shin, S. , 2015, “ Advances in the Measurement of Red Blood Cell Deformability: A Brief Review,” J. Cell. Biotechnol., 1(1), pp. 63–79. [CrossRef]
Buys, A. V. , Van Rooy, M.-J. , Soma, P. , Van Papendorp, D. , Lipinski, B. , and Pretorius, E. , 2013, “ Changes in Red Blood Cell Membrane Structure in Type 2 Diabetes: A Scanning Electron and Atomic Force Microscopy Study,” Cardiovasc. Diabetol., 12(1), p. 25. [CrossRef] [PubMed]
Singh, R. , Barden, A. , Mori, T. , and Beilin, L. , 2001, “ Advanced Glycation End-Products: A Review,” Diabetologia, 44(2), pp. 129–146. [CrossRef] [PubMed]
Ahmed, N. , 2005, “ Advanced Glycation Endproducts–Role in Pathology of Diabetic Complications,” Diabetes Res. Clin. Pract., 67(1), pp. 3–21. [CrossRef] [PubMed]
Takakuwa, Y. , and Mohandas, N. , 1988, “ Modulation of Erythrocyte Membrane Material Properties by Ca2+ and Calmodulin: Implications for Their Role in Regulation of Skeletal Protein Interactions,” J. Clin. Invest., 82(2), p. 394. [CrossRef] [PubMed]
Kunt, T. , Schneider, S. , Pfützner, A. , Goitum, K. , Engelbach, M. , Schauf, B. , Beyer, J. , and Forst, T. , 1999, “ The Effect of Human Proinsulin C-Peptide on Erythrocyte Deformability in Patients With Type 1 Diabetes Mellitus,” Diabetologia, 42(4), pp. 465–471. [CrossRef] [PubMed]
Hashemi, Z. Z. , Rahnama, M. M. , and Jafari, S. S. , 2016, “ Lattice Boltzmann Simulation of Healthy and Defective Red Blood Cell Settling in Blood Plasma,” ASME J. Biomech. Eng., 138(5), p. 051002. [CrossRef]
Schubert, C. , 2011, “ Single-Cell Analysis: The Deepest Differences,” Nature, 480(7375), pp. 133–137. [CrossRef] [PubMed]
Itoh, T. , Chien, S. , and Usami, S. , 1995, “ Effects of Hemoglobin Concentration on Deformability of Individual Sickle Cells After Deoxygenation,” Blood, 85(8), pp. 2245–2253. http://www.bloodjournal.org/content/85/8/2245 [PubMed]
Kaul, D. , Chen, D. , and Zhan, J. , 1994, “ Adhesion of Sickle Cells to Vascular Endothelium is Critically Dependent on Changes in Density and Shape of the Cells,” Blood, 83(10), pp. 3006–3017. http://www.bloodjournal.org/content/83/10/3006 [PubMed]
Alapan, Y. , Little, J. A. , and Gurkan, U. A. , 2014, “ Heterogeneous Red Blood Cell Adhesion and Deformability in Sickle Cell Disease,” Sci. Rep., 4, p. 7173. [CrossRef] [PubMed]
Li, X. J. , Du, E. , Lei, H. , Tang, Y.-H. , Dao, M. , Suresh, S. , and Karniadakis, G. E. , 2016, “ Patient-Specific Blood Rheology in Sickle-Cell Anaemia,” Interface Focus, 6(1), p. 20150065. [CrossRef] [PubMed]
Padilla, F. , Bromberg, P. A. , and Jensen, W. N. , 1973, “ The Sickle-Unsickle Cycle: A Cause of Cell Fragmentation Leading to Permanently Deformed Cells,” Blood, 41(5), pp. 653–660. http://www.bloodjournal.org/content/41/5/653 [PubMed]

Figures

Grahic Jump Location
Fig. 1

(a and b) Schematic representation of a healthy human RBC (a) and its complex membrane structure (b). The cell membrane is made of a lipid bilayer reinforced on its inner face by a flexible two-dimensional spectrin network. (c and d) Schematic view of the particle-based whole-cell model (c) and composite membrane model (d). For the whole-cell model (c), the lipid bilayer and cytoskeleton are rendered in dark gray and black triangular networks. For the coarse-grained composite membrane model (d), the dark gray, black, and light gray particles represent clusters of lipid molecules, actin junctions, and spectrin filaments of cytoskeleton, respectively; the black particles signify band-3 complexes.

Grahic Jump Location
Fig. 2

Shape transformation pathways of membrane vesicles (a) and RBCs (b) obtained from experimental investigations (upper) and model predictions (lower). Reproduced from Refs. [47,105].

Grahic Jump Location
Fig. 3

(a–c) Snapshot of a vesicle undergoing blebbing as a result of a localized ablation of the RBC cytoskeleton. (d–f) Sequences of coalescence of two blebs on vesicle during a uniform contraction of RBC cytoskeleton (Reproduced from Ref. [128]). CGMD modeling of one-component (g–i) and two-component (j–l) RBC membrane under uniform compression at compression ratio of (g) 2%, (h) 5%, and (i) 15%. Gray color highlights the lipid bilayer component with spontaneous curvature. The compression ratio is defined as the ratio of the decrease in the horizontally projected area due to compression, to the projected area of the membrane at equilibrium (Reproduced with permission from Li and Lykotrafitis [130]. Copyright 2015 by American Physical Society.

Grahic Jump Location
Fig. 4

(a) Illustration of the flow cytometer device. (b) Experimental images of ring-stage infected (dark gray arrows) and uninfected (light gray arrows) RBCs in the channels. (c) The computational RBC model consists of 5000 particles connected with links. The parasite is modeled as a rigid sphere inside the cell. (d) DPD simulation images of Pf-RBCs traveling in channels of converging (left) and diverging (right) pore geometries. (Reproduced with permission from Bow et al. [142]. Copyright 2011 by Royal Society of Chemistry).

Grahic Jump Location
Fig. 5

The twisted structure of HbS fiber (a) and its pitch length s (b) and persistence length lp (c) properties obtained from CGMD simulations. (Reproduced with permission from Lu et al. [150]. Copyright 2016 by Elsevier).

Grahic Jump Location
Fig. 6

Sickle cells in shear flow: (a) Successive snapshots of SS-RBCs in shear flow. Labels I, II, and III correspond to a deformable SS2 cell, rigid SS3 cell, and ISC, respectively. The arrow indicates the flow direction; (b-c) Instantaneous contact area and velocity for sickle RBC in shear flow conditions. (Reproduced from Ref. [95]).

Grahic Jump Location
Fig. 7

MSDs of band-3 particles against time and corresponding diffusion coefficients of the mobile band-3 in the membrane with various vertical (a) and horizontal (b) connectivities. (Reproduced from Ref. [98].).

Tables

Errata

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In