Hostname: page-component-5c6d5d7d68-wbk2r Total loading time: 0 Render date: 2024-08-29T22:57:52.191Z Has data issue: false hasContentIssue false

Assessment of coupled bilayer–cytoskeleton modelling strategy for red blood cell dynamics in flow

Published online by Cambridge University Press:  22 January 2024

V. Puthumana
Affiliation:
Aix Marseille Univ, CNRS, Centrale Marseille, M2P2, Turing Centre for Living Systems, 13013 Marseille, France
P.G. Chen
Affiliation:
Aix Marseille Univ, CNRS, Centrale Marseille, M2P2, Turing Centre for Living Systems, 13013 Marseille, France
M. Leonetti*
Affiliation:
Aix Marseille Univ, CNRS, CINaM, Turing Centre for Living Systems, 13009 Marseille, France
R. Lasserre*
Affiliation:
Aix Marseille Univ, CNRS, INSERM, CIML, Turing Centre for Living Systems, 13009 Marseille, France
M. Jaeger*
Affiliation:
Aix Marseille Univ, CNRS, Centrale Marseille, M2P2, Turing Centre for Living Systems, 13013 Marseille, France

Abstract

The red blood cell (RBC) membrane is composed of a lipid bilayer and a cytoskeleton interconnected by protein junction complexes, allowing for potential sliding between the lipid bilayer and the cytoskeleton. Despite this biological reality, it is most often modelled as a single-layer model, a hyperelastic capsule or a fluid vesicle. Another approach involves incorporating the membrane's composite structure using double layers, where one layer represents the lipid bilayer and the other represents the cytoskeleton. In this paper, we computationally assess the various modelling strategies by analysing RBC behaviour in extensional flow and four distinct regimes that simulate RBC dynamics in shear flow. The proposed double-layer strategies, such as the vesicle–capsule and capsule–capsule models, account for the fluidity and surface incompressibility of the lipid bilayer in different ways. Our findings demonstrate that introducing sliding between the layers offers the cytoskeleton a considerable degree of freedom to alleviate its elastic stresses, resulting in a significant increase in RBC elongation. Surprisingly, our study reveals that the membrane modelling strategy for RBCs holds greater importance than the choice of the cytoskeleton's reference shape. These results highlight the inadequacy of considering mechanical properties alone and emphasise the need for careful integration of these properties. Furthermore, our findings fortuitously uncover a novel indicator for determining the appropriate stress-free shape of the cytoskeleton.

Type
JFM Papers
Copyright
© The Author(s), 2024. Published by 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

Abbasi, M., Farutin, A., Nait-Ouhra, A., Ez-Zahraouy, H., Benyoussef, A. & Misbah, C. 2022 Dynamics and rheology of a single two-dimensional multilobe vesicle in a confined geometry. Phys. Rev. Fluids 7 (9), 093603.CrossRefGoogle Scholar
Boedec, G., Leonetti, M. & Jaeger, M. 2011 3D vesicle dynamics simulations with a linearly triangulated surface. J. Comput. Phys. 230, 10201034.CrossRefGoogle Scholar
Boedec, G., Leonetti, M. & Jaeger, M. 2017 Isogeometric FEM-BEM simulations of drop, capsule and vesicle dynamics in Stokes flow. J. Comput. Phys. 342, 117138.CrossRefGoogle Scholar
Brust, M., et al. 2014 The plasma protein fibrinogen stabilizes clusters of red blood cells in microcapillary flows. Sci. Rep. 4 (1), 4348.CrossRefGoogle ScholarPubMed
Chang, H.-Y., Li, X. & Karniadakis, G.E. 2017 Modeling of biomechanics and biorheology of red blood cells in type 2 diabetes mellitus. Biophys. J. 113 (2), 481490.CrossRefGoogle ScholarPubMed
Chang, H.-Y., Li, X., Li, H. & 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), e1005173.CrossRefGoogle ScholarPubMed
Cirak, F. & Ortiz, M. 2001 Fully C1-conforming subdivision elements for finite deformation thin-shell analysis. Intl J. Numer. Meth. Engng 51 (7), 813833.CrossRefGoogle Scholar
Cirak, F., Ortiz, M. & Schröder, P. 2000 Subdivision surfaces: a new paradigm for thin-shell finite-element analysis. Intl J. Numer. Meth. Engng 47 (12), 20392072.3.0.CO;2-1>CrossRefGoogle Scholar
Cottrell, J.A., Hughes, T.J.R. & Bazilevs, Y. 2009 Isogeometric Analysis: Toward Integration of CAD and FEA. Wiley.CrossRefGoogle Scholar
Dahl, J.B., Narsimhan, V., Gouveia, B., Kumar, S., Shaqfeh, E.S.G. & Muller, S.J. 2016 Experimental observation of the asymmetric instability of intermediate-reduced-volume vesicles in extensional flow. Soft Matt. 12 (16), 37873796.CrossRefGoogle ScholarPubMed
Discher, D.E., Mohandas, N. & Evans, E.A. 1994 Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science 266 (5187), 10321035.CrossRefGoogle ScholarPubMed
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 (9), 29062916.CrossRefGoogle Scholar
Evans, E.A. & Skalak, R. 1980 Mechanics and Thermodynamics of Biomembranes, 1st edn. CRC.Google Scholar
Fedosov, D.A., Noguchi, H. & Gompper, G. 2014 Multiscale modeling of blood flow: from single cells to blood rheology. Biomech. Model. Mechanobiol. 13 (2), 239258.CrossRefGoogle ScholarPubMed
Fischer, T.M. 1992 Is the surface area of the red cell membrane skeleton locally conserved? Biophys. J. 61 (2), 298305.CrossRefGoogle ScholarPubMed
Fischer, T.M. 2007 Tank-tread frequency of the red cell membrane: dependence on the viscosity of the suspending medium. Biophys. J. 93 (7), 25532561.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
Freund, J.B. 2014 Numerical simulation of flowing blood cells. Annu. Rev. Fluid Mech. 46 (1), 6795.CrossRefGoogle Scholar
Gounley, J., Boedec, G., Jaeger, M. & Leonetti, M. 2016 Influence of surface viscosity on droplets in shear flow. J. Fluid Mech. 791, 464494.CrossRefGoogle Scholar
Gounley, J. & Peng, Y. 2015 Computational modeling of membrane viscosity of red blood cells. Commun. Comput. Phys. 17 (4), 10731087.CrossRefGoogle Scholar
Guglietta, F., Behr, M., Biferale, L., Falcucci, G. & Sbragaglia, M. 2020 On the effects of membrane viscosity on transient red blood cell dynamics. Soft Matt. 16 (26), 61916205.CrossRefGoogle ScholarPubMed
Hansen, J.C., Skalak, R., Chien, S. & Hoger, A. 1996 An elastic network model based on the structure of the red blood cell membrane skeleton. Biophys. J. 70 (1), 146166.CrossRefGoogle ScholarPubMed
Hoore, M., Yaya, F., Podgorski, T., Wagner, C., Gompper, G. & Fedosov, D.A. 2018 Effect of spectrin network elasticity on the shapes of erythrocyte doublets. Soft Matt. 14 (30), 62786289.CrossRefGoogle ScholarPubMed
Jeffery, G.B. 1922 The motion of ellipsoidal particles immersed in a viscous fluid. Proc. R. Soc. Lond. A 102 (715), 161179.Google Scholar
Kabacaoğlu, G. & Biros, G. 2019 Sorting same-size red blood cells in deep deterministic lateral displacement devices. J. Fluid Mech. 859, 433475.CrossRefGoogle Scholar
Kantsler, V., Segre, E. & Steinberg, V. 2007 Vesicle dynamics in time-dependent elongation flow: wrinkling instability. Phys. Rev. Lett. 99 (17), 178102.CrossRefGoogle ScholarPubMed
Kantsler, V., Segre, E. & Steinberg, V. 2008 Critical dynamics of vesicle stretching transition in elongational flow. Phys. Rev. Lett. 101 (4), 048101.CrossRefGoogle ScholarPubMed
Késmárky, G., Kenyeres, P., Rábai, M. & Tóth, K. 2008 Plasma viscosity: a forgotten variable. Clin. Hemorheol. Microcirc. 39, 243246.CrossRefGoogle ScholarPubMed
Kim, Y., Kim, K. & Park, Y. 2012 Measurement techniques for red blood cell deformability: recent advances. In Blood Cell – An Overview of Studies in Hematology (ed. T. Moschandreou). InTech.CrossRefGoogle Scholar
Krapf, D. 2015 Mechanisms underlying anomalous diffusion in the plasma membrane. In Lipid Domains (ed. A.K. Kenworthy), Current Topics in Membranes, vol. 75, pp. 167–207. Academic.CrossRefGoogle Scholar
Krishnaswamy, S. 1996 A cosserat-type model for the red blood cell wall. Intl J. Engng Sci. 34 (8), 873899.CrossRefGoogle Scholar
Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R.S., Kondo, J. & Fujiwara, T. 2005 Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. 34 (1), 351378.CrossRefGoogle Scholar
Lenormand, G., Hénon, S., Richert, A., Siméon, J. & Gallet, F. 2001 Direct measurement of the area expansion and shear moduli of the human red blood cell membrane skeleton. Biophys. J. 81 (1), 4356.CrossRefGoogle ScholarPubMed
Lenormand, G., Hénon, S., Richert, A., Siméon, J. & Gallet, F. 2003 Elasticity of the human red blood cell skeleton. J. Biorheol. 40, 247251.Google ScholarPubMed
Levant, M. & Steinberg, V. 2016 Intermediate regime and a phase diagram of red blood cell dynamics in a linear flow. Phys. Rev. E 94 (6), 062412.CrossRefGoogle Scholar
Li, X., Lu, H. & Peng, Z. 2018 Continuum- and particle-based modeling of human red blood cells. In Handbook of Materials Modeling (ed. W. Andreoni & S. Yip), pp. 1–17. Springer International Publishing.CrossRefGoogle Scholar
Li, X, Peng, Z., Lei, H., Dao, M. & Karniadakis, G.E. 2014 Probing red blood cell mechanics, rheology and dynamics with a two-component multi-scale model. Phil. Trans. A Math. Phys. Engng Sci. 372 (2021), 20130389.Google ScholarPubMed
Li, X., Vlahovska, P.M. & Karniadakis, G.E. 2013 Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease. Soft Matt. 9 (1), 2837.CrossRefGoogle ScholarPubMed
Loop, C.T. 1987 Smooth subdivision surfaces based on triangles. Master's thesis, The University of Utah.Google Scholar
Lu, H. & Peng, Z. 2019 Boundary integral simulations of a red blood cell squeezing through a submicron slit under prescribed inlet and outlet pressures. Phys. Fluids 31 (3), 031902.CrossRefGoogle Scholar
Lu, L., Morse, M.J., Rahimian, A., Stadler, G. & Zorin, D. 2019 Scalable simulation of realistic volume fraction red blood cell flows through vascular networks. In Proceedings of the International Conference for High Performance Computing, Networking, Storage and Analysis, pp. 1–30. ACM.CrossRefGoogle Scholar
Lyu, J., Chen, P.G., Boedec, G., Leonetti, M. & Jaeger, M. 2018 Hybrid continuum–coarse-grained modeling of erythrocytes. C. R. Méc 346 (6), 439448.CrossRefGoogle Scholar
Lyu, J.M., Chen, P.G., Boedec, G., Leonetti, M. & Jaeger, M. 2021 An isogeometric boundary element method for soft particles flowing in microfluidic channels. Comput. Fluids 214, 104786.CrossRefGoogle Scholar
Mauer, J., Mendez, S., Lanotte, L., Nicoud, F., Abkarian, M., Gompper, G. & Fedosov, D.A. 2018 Flow-induced transitions of red blood cell shapes under shear. Phys. Rev. Lett. 121 (11), 118103.CrossRefGoogle ScholarPubMed
McWhirter, J.L., Noguchi, H. & Gompper, G. 2011 Deformation and clustering of red blood cells in microcapillary flows. Soft Matt. 7 (22), 10967.CrossRefGoogle Scholar
Mendez, S. & Abkarian, M. 2018 In-plane elasticity controls the full dynamics of red blood cells in shear flow. Phys. Rev. Fluids 3 (10), 101101.CrossRefGoogle Scholar
Minetti, C., Audemar, V., Podgorski, T. & Coupier, G. 2019 Dynamics of a large population of red blood cells under shear flow. J. Fluid Mech. 864, 408448.CrossRefGoogle Scholar
Mohandas, N. & Evans, E. 1994 Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Biophys. Biomol. 23 (1), 787818.CrossRefGoogle ScholarPubMed
Mohandas, N. & Gallagher, P.G. 2008 Red cell membrane: past, present, and future. Blood 112 (10), 39393948.CrossRefGoogle ScholarPubMed
Narsimhan, V., Spann, A.P. & Shaqfeh, E.S.G. 2014 The mechanism of shape instability for a vesicle in extensional flow. J. Fluid Mech. 750, 144190.CrossRefGoogle Scholar
Noguchi, H. & Gompper, G. 2005 Shape transitions of fluid vesicles and red blood cells in capillary flows. Proc. Natl Acad. Sci. USA 102 (40), 1415914164.CrossRefGoogle ScholarPubMed
Omori, T., Ishikawa, T., Barthès-Biesel, D., Salsac, A.-V., Walter, J., Imai, Y. & Yamaguchi, T. 2011 Comparison between spring network models and continuum constitutive laws: application to the large deformation of a capsule in shear flow. Phys. Rev. E 83 (4), 041918.CrossRefGoogle Scholar
Peng, Z., Asaro, R.J. & Zhu, Q. 2010 Multiscale simulation of erythrocyte membranes. Phys. Rev. E 81 (3), 031904.CrossRefGoogle ScholarPubMed
Peng, Z., Asaro, R.J. & Zhu, Q. 2011 Multiscale modelling of erythrocytes in Stokes flow. J. Fluid Mech. 686, 299337.CrossRefGoogle Scholar
Peng, Z., Chen, Y.-L., Lu, H., Pan, Z. & Chang, H.-C. 2015 a Mesoscale simulations of two model systems in biophysics: from red blood cells to DNAs. Comput. Part. Mech. 2 (4), 339357.CrossRefGoogle 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 (33), 1335613361.CrossRefGoogle Scholar
Peng, Z., Mashayekh, A. & Zhu, Q. 2014 Erythrocyte responses in low-shear-rate flows: effects of non-biconcave stress-free state in the cytoskeleton. J. Fluid Mech. 742, 96118.CrossRefGoogle Scholar
Peng, Z., Salehyar, S. & Zhu, Q. 2015 b Stability of the tank treading modes of erythrocytes and its dependence on cytoskeleton reference states. J. Fluid Mech. 771, 449467.CrossRefGoogle Scholar
Peng, Z. & Zhu, Q. 2013 Deformation of the erythrocyte cytoskeleton in tank treading motions. Soft Matt. 9 (31), 7617.CrossRefGoogle Scholar
Pivkin, I.V., Peng, Z., Karniadakis, G.E., Buffet, P.A., Dao, M. & Suresh, S. 2016 Biomechanics of red blood cells in human spleen and consequences for physiology and disease. Proc. Natl Acad. Sci. USA 113 (28), 78047809.CrossRefGoogle ScholarPubMed
Pozrikidis, C. 1992 Boundary Integral and Singularity Methods for Linearized Viscous Flow. Cambridge Texts in Applied Mathematics, vol. 7. Cambridge University Press.CrossRefGoogle Scholar
Pozrikidis, C. 2002 A Practical Guide to Boundary Element Methods with the Software Library BEMLIB. Chapman & Hall/CRC.CrossRefGoogle Scholar
Prado, G., Farutin, A., Misbah, C. & Bureau, L. 2015 Viscoelastic transient of confined red blood cells. Biophys. J. 108 (9), 21262136.CrossRefGoogle ScholarPubMed
Salehyar, S. & Zhu, Q. 2016 Deformation and internal stress in a red blood cell as it is driven through a slit by an incoming flow. Soft Matt. 12 (13), 31563164.CrossRefGoogle Scholar
Sigüenza, J., Mendez, S. & Nicoud, F. 2017 How should the optical tweezers experiment be used to characterize the red blood cell membrane mechanics? Biomech. Model. Mechanobiol. 16 (5), 16451657.CrossRefGoogle ScholarPubMed
Skalak, R., Tozeren, A., Zarda, R.P. & Chien, S. 1973 Strain energy function of red blood cell membranes. Biophys. J. 13 (3), 245264.CrossRefGoogle ScholarPubMed
Tsubota, K. 2014 Short note on the bending models for a membrane in capsule mechanics: comparison between continuum and discrete models. J. Comput. Phys. 277, 320328.CrossRefGoogle Scholar
Tsubota, K. 2021 Elongation deformation of a red blood cell under shear flow as stretch testing. J. Mech. Phys. Solids 152, 104345.CrossRefGoogle Scholar
Vlahovska, P.M., Barthes-Biesel, D. & Misbah, C. 2013 Flow dynamics of red blood cells and their biomimetic counterparts. C. R. Phys. 14 (6), 451458.CrossRefGoogle Scholar
Williams, A.R. & Morris, D.R. 2009 The internal viscosity of the human erythrocyte may determine its lifespan in vivo. Scand. J. Haematol. 24 (1), 5762.CrossRefGoogle Scholar
Yazdani, A. & Bagchi, P. 2013 Influence of membrane viscosity on capsule dynamics in shear flow. J. Fluid Mech. 718, 569595.CrossRefGoogle Scholar
Zhang, Y., Huang, C., Kim, S., Golkaram, M., Dixon, M.W.A., Tilley, L., Li, J., Zhang, S. & Suresh, S. 2015 Multiple stiffening effects of nanoscale knobs on human red blood cells infected with Plasmodium falciparum malaria parasite. Proc. Natl Acad. Sci. USA 112 (19), 60686073.CrossRefGoogle ScholarPubMed
Zhao, H. & Shaqfeh, E.S.G. 2013 The shape stability of a lipid vesicle in a uniaxial extensional flow. J. Fluid Mech. 719, 345361.CrossRefGoogle Scholar
Zhu, Q., Salehyar, S., Cabrales, P. & Asaro, R.J. 2017 Prospects for human erythrocyte skeleton-bilayer dissociation during splenic flow. Biophys. J. 113 (4), 900912.CrossRefGoogle ScholarPubMed