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Hydrodynamics and rheology of a vesicle doublet suspension
Phys. Rev. Fluids 4, 103601 – Published 10 October, 2019
DOI: https://doi.org/10.1103/PhysRevFluids.4.103601
Abstract
The dynamics of an adhesive two-dimensional vesicle doublet under various flow conditions is investigated numerically using a high-order, adaptive-in-time boundary integral method. In a quiescent flow, two nearby vesicles move slowly toward each other under the adhesive potential, pushing out fluid between them to form a vesicle doublet at equilibrium. A lubrication analysis on such draining of a thin film gives the dependencies of draining time on adhesion strength and separation distance, which are in good agreement with numerical results. In a planar extensional flow, we find that a stable vesicle doublet forms only when two vesicles collide head-on around the stagnation point. In a microfluid trap where the stagnation of an extensional flow is dynamically placed in the middle of a vesicle doublet through an active control loop, novel dynamics of a vesicle doublet are observed. Numerical simulations show that there exists a critical extensional flow rate above which adhesive interaction is overcome by the diverging stream, thus providing a simple method to measure the adhesion strength between two vesicle membranes. In a planar shear flow, numerical simulations reveal that a vesicle doublet may form provided that the adhesion strength is sufficiently large at a given vesicle reduced area. Once a doublet is formed, its oscillatory dynamics is found to depend on the adhesion strength and their reduced area. Furthermore the effective shear viscosity of a dilute suspension of vesicle doublets is found to be a function of the reduced area. Results from these numerical studies and analysis shed light on the hydrodynamic and rheological consequences of adhesive interactions between vesicles in a viscous fluid.
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References (86)
- E. Sackmann, Supported membranes: Scientific and practical applications, Science 271, 43 (1996).
- S. F. Fenz and K. Sengupta, Giant vesicles as cell models, Integr. Biol. 4, 982 (2012).
- D. Barthes-Biesel, Motion and deformation of elastic capsules and vesicles in flow, Annu. Rev. Fluid Mech. 48, 25 (2016).
- H.-G. Dobereiner, Properties of giant vesicles, Curr. Opin. Colloid Int. Sci. 5, 256 (2000).
- E. Evans, W. Rawicz, and B. A. Smith, Concluding remarks back to the future: Mechanics and thermodynamics of lipid biomembrane, Faraday Discuss. 161, 591 (2013).
- H. Sugiyama and T. Toyota, Toward experimental evolution with giant vesicles, Life 8, 53 (2018).
- D. Barthes-Biesel and J. M. Rallison, The time-dependent deformation of a capsule freely suspended in a linear shear flow, J. Fluid Mech. 113, 251 (1981).
- C. Misbah, Vascillating Breathing and Tumbling of Vesicles Under Shear Flow, Phys. Rev. Lett. 96, 028104 (2006).
- P. M. Vlahovska and R. S. Gracia, Dynamics of a viscous vesicle in linear flows, Phys. Rev. E 75, 016313 (2007).
- R. Finken, A. Lamura, U. Seifert, and G. Gompper, Two-dimensional fluctuating vesicles in linear shear flow, Eur. Phys. J. E 25, 309 (2008).
- J. Zhang, J. Zahn, W. Tan, and H. Lin, A transient solution for vesicle electrodeformation and relaxation, Phys. Fluids 25, 071903 (2013).
- H. Nganguia and Y.-N. Young, Equilibrium electrodeformation of a spheroidal vesicle in an ac electric field, Phys. Rev. E 88, 052718 (2013).
- P. Bagchi, P. C. Johnson, and A. S. Popel, Computational fluid dynamic simulation of aggregation of deformable cells in a shear flow, J. Biomech. Eng. 127, 1070 (2005).
- T. Biben, Phase-field models for free-boundary problems, Eur. J. Phys. 26, S47 (2005).
- S. K. Veerapaneni, D. Gueyffier, D. Zorin, and G. Biros, A boundary integral method for simulating the dynamics of inextensible vesicles suspended in a viscous fluid in 2D, J. Comput. Phys. 228, 2334 (2009).
- Y. Seol, W.-F. Hu, Y. Kim, and M.-C. Lai, An immersed boundary method for simulating vesicle dynamics in three dimensions, J. Comput. Phys. 322, 125 (2016).
- S. K. Veerapaneni, Y.-N. Young, P. M. Vlahovska, and J. Błazdzwicz, Dynamics of a Compound Vesicle in Shear Flow, Phys. Rev. Lett. 106, 158103 (2011).
- V. Vitkova, M. Mader, B. Polack, C. Misbah, and T. Podgorski, Micro-macro link in rheology of erythrocyte and vesicle suspensions, Biophys. J. 95, L33 (2008).
- G. Ghigliotti, T. Biben, and C. Misbah, Rheology of a dilute two-dimensional suspension of vesicles, J. Fluid Mech. 653, 489 (2010).
- J. Deschamps, V. Kantsler, E. Serge, and V. Steinberg, Dynamics of a vesicle in general flow, Proc. Natl. Acad. Sci. (USA) 106, 11444 (2009).
- V. Kantsler, E. Segre, and V. Steinberg, Dynamics of interacting vesicles and rheology of vesicle suspension in shear flow, Europhys. Lett. 82, 58005 (2008).
- N. Zabusky, E. Segre, J. Deschamps, V. Kantsler, and V. Steinberg, Dynamics of vesicles in shear and rotational flows: modal dynamics and phase diagram, Phys. Fluids 23, 041905 (2011).
- V. Kantsler, E. Segre, and V. Steinberg, Critical Dynamics of Vesicle Stretching Transition in Elongational Flow, Phys. Rev. Lett. 101, 048101 (2008).
- H. Zhao and E. S. G. Shaqfeh, The dynamics of a vesicle in simple shear flow, J. Fluid Mech. 674, 578 (2011).
- A. P. Spann, H. Zhao, and E. S. G. Shaqfeh, Loop subdivision surface boundary integral method simulations of vesicles at low reduced volume ratio in shear and extensional flow, Phys. Fluids 26, 031902 (2014).
- H. Zhao and E. S. G. Shaqfeh, The shape stability of a lipid vesicle in a uniaxial extensional flow, J. Fluid Mech. 719, 345 (2013).
- V. Narsimhan, A. P. Spann, and E. S. G. Shaqfeh, The mechanism of shape instability for a vesicle in extensional flow, J. Fluid Mech. 750, 144 (2014).
- J. B. Dahl, V. Narsimhan, B. Gouveia, S. Kumar, E. S. G. Shaqfeh, and S. J. Muller, Experimental observation of the asymmetric instability of intermediate-reduced-volume vesicles in extensional flow, Soft Matter 12, 3787 (2016).
- P. Ziherl, Aggregates of Two-Dimensional Vesicles: Rouleaux, Sheets, and Convergent Extension, Phys. Rev. Lett. 99, 128102 (2007).
- P. Ziherl and S. Svetina, Flat and sigmoidally curved contact zones in vesicle-vesicle adhesion, Proc. Natl. Acad. Sci. (USA) 104, 761 (2007).
- S. Svetina and P. Ziherl, Morphology of small aggregates of red blood cells, Bioelectrochemistry 73, 84 (2008).
- R. Gu, X. Wang, and M. Gunzburger, A two phase field model for tracking vesicle-vesicle adhesion, Math. Biol. 73, 1293 (2016).
- D. Flormann, O. Aouane, L. Kaestner, C. Ruloff, C. Misbah, T. Podgorski, and C. Wagner, The buckling instability of aggregating red blood cells, Sci. Rep. 7, 7928 (2017).
- M. Hoore, F. Yaya, T. Podgorski, C. Wagner, G. Gompper, and D. A. Fedosov, Effect of spectrin network elasticity on the shapes of erythrocyte doublets, Soft Matter 14, 6278 (2018).
- M. Brust, O. Aouane, M. Thiébaud, D. Flormann, C. Verdier, L. Kaestner, M. W. Laschke, H. Selmi, A. Benyoussef, T. Podgorski, G. Coupier, C. Misbah, and C. Wagner, The plasma protein fibrinogen stabilizes clusters of red blood cells in microcapillary flows, Sci. Rep. 4, 4348 (2014).
- V. Clavería, O. Aouane, M. Thiébaud, M. Abkarian, G. Coupier, C. Misbah, T. John, and C. Wagner, Clusters of red blood cells in microcapillary flow: hydrodynamic versus macromolecule induced interaction, Soft Matter 12, 8235 (2017).
- S. Chien, S. Usami, R. J. Dellenback, M. I. Gregersen, L. B. Nanninga, and M. Mason Guest, Blood viscosity: Influence of erythrocyte aggregation, Science 157, 829 (1967).
- A. Rahimian, S. K. Veerapaneni, and G. Biros, Dynamic simulation of locally inextensible vesicles suspended in an arbitrary two-dimensional domain, a boundary integral method, J. Comput. Phys. 229, 6466 (2010).
- B. Neu and H. J. Meiselman, Depletion-mediated red blood cell aggregation in polymer solutions, Biophys. J. 83, 2482 (2002).
- E. Evans and M. Metcalfe, Free energy potential for aggregation of giant, neutral lipid bilayer vesicles by Van der Waals attraction, Biophys. J. 46, 423 (1984).
- E. Evans, in Physical Basis of Cell-cell Adhesion, edited by P. Bongrand (CRC, Boca Raton, FL, 1988).
- J. Israelachvili, Intermolecular and Surface Forces (Academic, San Diego, 1991).
- S. Perutkova, M. Frank-Bertoncelj, B. Rozman, V. Kralj-Iglic, and A. Iglic, Influence of ionic strength and beta2-glycoprotein I concentration on agglutination of like-charged phospholipid membranes, Coll. Surf. B 111, 699 (2013).
- U. Seifert and R. Lipowsky, Adhesion of vesicles, Phys. Rev. A 42, 4768 (1990).
- A.-L. Bernard, M.-A. Guedeau-Boudeville, L. Jullien, and J.-M. di Meglio, Strong adhesion of giant vesicles on surface and permeability, Langmuir 16, 6809 (2000).
- W. Shi, X. Q. Feng, and H. Gao, Two-dimensional model of vesicle adhesion on curved substrates, Acta Mech. Sin. 22, 529 (2006).
- Y. Lin and L. B. Freund, Forced detachment of a vesicle in adhesive contact with a substrate, Int. J. Solids Struct. 44, 1927 (2007).
- T. Gruhn, T. Franke, R. Dimova, and R. Lipowsky, Novel method for measuring the adhesion energy of vesicles, Langmuir 23, 5423 (2007).
- S. Das and Q. Du, Adhesion of vesicles to curved substrates, Phys. Rev. E 77, 011907 (2008).
- M. P. Keh, J. Walter, and L. G. Leal, Hydrodynamic interaction between a capsule and a solid boundary in unbounded stokes flow, Phys. Fluids 26, 111903 (2014).
- J. Zhang, S. Das, and Q. Du, A phase field model for vesicle-substrate adhesion, J. Comput. Phys. 228, 7837 (2009).
- J. Agudo-Canalejo and R. Lipowsky, Critical particle sizes for the engulfment of nanoparticles by membranes and vesicles with bilayer asymmetry, ACS Nano Lett. 9, 3704 (2015).
- J. Agudo-Canalejo and R. Lipowsky, Adhesive nanoparticles as local probes of membrane curvature, Nano Lett. 15, 7168 (2015).
- J. Steinkuhler, J. Agudo-Canalejo, R. Lipowsky, and R. Dimova, Modulating vesicle adhesion by electric fields, Biophys. J. 111, 1454 (2016).
- M. P. Keh and L. G. Leal, Adhesion and detachment of a capsule in axisymmetric flow, Phys. Rev. Fluids 1, 013201 (2016).
- J. Agudo-Canalejo and R. Lipowsky, Uniform and Janus-like nanoparticles in contact with vesicles: energy landscapes and curvature-induced forces, Soft Matter 13, 2155 (2017).
- I. Cantat and C. Misbah, Lift Force and Dynamical Unbinding of Adhering Vesicles under Shear Flow, Phys. Rev. Lett. 83, 880 (1999).
- S. Sukumaran and U. Seifert, Influence of shear flow on vesicles near a wall: A numerical study, Phys. Rev. E 64, 011916 (2001).
- M. J. Blount, M. J. Miksis, and S. H. Davis, The equilibria of vesicles adhered to substrates by short-ranged potentials, Proc. R. Soc. A 469, 20120729 (2013).
- A. Ramachandran, T. H. Anderson, L. G. Leal, and J. N. Israelachvili, Adhesive interactions between vesicles in the strong adhesion limit, Langmuir 27, 59 (2010).
- T. Mares, M. Daniel, A. Iglic, V. Kralj-Iglic, and M. Fosnaric, Determination of the strength of adhesion between lipid vesicles, Sci. World J. 2012, 146804 (2012).
- J. M. Frostad, M. Seth, S. M. Bernasek, and L. G. Leal, Direct measurement of interaction forces between charged multilamellar vesicles, Soft Matter 10, 7769 (2014).
- A. Agrawal, Mechanics of membrane-membrane adhesion, Math. Mech. Solids 16, 872 (2011).
- P. Y. Gires, G. Danker, and C. Misbah, Hydrodynamic interaction between two vesicles in a linear shear flow, Phys. Rev. E 86, 011408 (2012).
- P.-Y. Gires, A. Srivastav, C. Misbah, T. Podgorski, and G. Coupier, Pairwise hydrodynamic interactions and diffusion in a vesicle suspension, Phys. Fluids 26, 013304 (2014).
- B. Quaife and G. Biros, High-volume fraction simulations of two-dimensional vesicle suspensions, J. Comput. Phys. 274, 245 (2014).
- B. Quaife and G. Biros, Adaptive time stepping for vesicle suspensions, J. Comput. Phys. 306, 478 (2016).
- Y.-N. Young and H. A. Stone, Long-wave dynamics of an elastic sheet lubricated by a thin liquid film on a wetting substrate, Phys. Rev. Fluids 2, 064001 (2017).
- A. Ramachandran and G. Leal, A scaling theory for the hydrodynamic interaction between a pair of vesicles or capsules, Phys. Fluids 22, 091702 (2010).
- V. Kantsler, E. Segre, and V. Steinberg, Vesicle Dynamics in Time-Dependent Elongation Flow: Wrinkling Instability, Phys. Rev. Lett. 99, 178102 (2007).
- J. J. M. Jansen, A. Boon, and W. G. M. Agterof, Influence of dynamic interfacial properties on droplet breakup in plane hyperbolic flow, AIChE J. 43, 1436 (1997).
- Y. T. Hu, D. J. Pine, and L. Gary Leal, Drop deformation, breakup, and coalescence with compatibilizer, Phys. Fluids 12, 484 (2000).
- J. M. Frostad, J. Walter, and L. G. Leal, A scaling relation for the capillary-pressure driven drainage of thin films, Phys. Fluids 25, 052108 (2013).
- J. E. Spjut, Trapping, deformation, and dynamics of phospholipid vesicles, Master's thesis, University of California, Berkeley, 2010.
- B. J. Bentley and L. G. Leal, A computer-controlled four-roll mill for investigations of particle and drop dynamics in two-dimensional linear shear flows, J. Fluid Mech. 167, 219 (1986).
- E. M. Johnson-Chavarria, M. Tanyeri, and C. M. Schroeder, A microfluidic-based hydrodynamic trap for single particles, J. Vis. Exp. 47, e2517 (2011).
- G. Breyiannis and C. Pozrikidis, Simple shear flow of suspensions of elastic capsules, Theor. Comput. Fluid Dyn. 13, 327 (2000).
- E. Lac, A. Morel, and D. Barthes-Biesel, Hydrodynamic interaction between two identical capsules in simple shear flow, J. Fluid Mech. 573, 149 (2007).
- E. Lac and D. Barthes-Biesel, Pairwise interaction of capsules in simple shear flow: Three-dimensional effects, Phys. Fluids 20, 040801 (2008).
- T. Omori, T. Ishikawa, Y. Imai, and T. Yamaguchi, Membrane tension of red blood cells pairwisely interacting in simple shear flow, J. Biomech. 46, 548 (2013).
- A. Rahimian, S. K. Veerapaneni, D. Zorin, and G. Biros, Boundary integral method for the flow of vesicles with viscosity contrast in three dimensions, J. Comput. Phys. 298, 766 (2015).
- G. B. Jeffery, The motion of ellipsoidal particles immersed in a viscous fluid, Proc. R. Soc. A 102, 161 (1922).
- S. F. Fenz, T. Bihr, D. Schmidt, R. Merkel, U. Seifert, K. Sengupta, and A.-S. Smith, Membrane fluctuations mediate lateral interactions between cadherin bonds, Nat. Phys. 13, 906 (2017).
- K. Liu, B. Chu, J. Newby, E. L. Read, J. Lowengrub, and J. Allard, Hydrodynamics of transient cell-cell contact: The role of membrane permeability and active protrusion length, PLoS Comput. Biol. 15, e1006352 (2019).
- B. K. Alpert, Hybrid Gauss-trapezoidal quadrature rules, SIAM J. Sci. Comput. 20, 1551 (1999).
- L. N. Trefethen and J. A. C. Weideman, The exponentially convergent trapezoidal rule, SIAM Rev. 56, 385 (2014).