1932

Abstract

Many important processes in the cell are mediated by stiff microtubule polymers and the active motor proteins moving on them. This includes the transport of subcellular structures (nuclei, chromosomes, organelles) and the self-assembly and positioning of the mitotic spindle. Little is understood of these processes, but they present fascinating problems in fluid-structure interactions. Microtubules and motor proteins are also the building blocks of new biosynthetic active suspensions driven by motor-protein activity. These reduced systems can be probed—and modeled—more easily than can the fully biological ones and demonstrate their own aspects of self-assembly and complex dynamics. I review recent work modeling such systems as fluid-structure interaction problems and as multiscale complex fluids.

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/content/journals/10.1146/annurev-fluid-010814-013639
2016-01-03
2024-04-28
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Literature Cited

  1. Allen MP, Tildesley DJ. 1987. Computer Simulation of Liquids Oxford: Clarendon
  2. Bendix P, Koenderink G, Cuvelier D, Dogic Z, Koeleman B. et al. 2008. A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys. J. 94:3126–36 [Google Scholar]
  3. Brugués J, Needleman DJ. 2014. Physical basis of spindle self-organization. PNAS 111:18496–500 [Google Scholar]
  4. Brugués J, Nuzzo V, Mazur E, Needleman DJ. 2012. Nucleation and transport organize microtubules in metaphase spindles. Cell 149:554–64 [Google Scholar]
  5. Cisneros LH, Kessler JO, Ganguly S, Goldstein RE. 2011. Dynamics of swimming bacteria: transition to directional order at high concentration. Phys. Rev. E 83:061907 [Google Scholar]
  6. Daniels BR, Masi BC, Wirtz D. 2006. Probing single-cell micromechanics in vivo: the microrheology of C. elegans developing embryos. Biophys. J. 90:4712–19 [Google Scholar]
  7. Desai A, Mitchison TJ. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83–117 [Google Scholar]
  8. Doi M, Edwards S. 1988. The Theory of Polymer Dynamics New York: Oxford Univ. Press
  9. Ezhilan B, Shelley MJ, Saintillan D. 2013. Instabilities and nonlinear dynamics of concentrated active suspensions. Phys. Fluids 25:070607 [Google Scholar]
  10. Forest M, Wang Q, Zhou R. 2013. Kinetic theory and simulations of active polar liquid crystalline polymers. Soft Matter 9:5207–22 [Google Scholar]
  11. Ganguly S, Williams LS, Palacios IM, Goldstein RE. 2012. Cytoplasmic streaming in Drosophila oocytes varies with kinesin activity and correlates with the microtubule cytoskeleton architecture. PNAS 109:15109–14 [Google Scholar]
  12. Gao T, Blackwell R, Glaser MA, Betterton M, Shelley MJ. 2015. Multiscale polar theory of microtubule and motor-protein assemblies. Phys. Rev. Lett. 114:048101 [Google Scholar]
  13. Giomi L, Bowick M, Ma X, Marchetti M. 2013. Defect annihilation and proliferation in active nematics. Phys. Rev. Lett. 110:228101 [Google Scholar]
  14. Giomi L, Bowick MJ, Mishra P, Sknepnek R, Marchetti MC. 2014. Defect dynamics in active nematics. Philos. Trans. R. Soc. A 372:20130365 [Google Scholar]
  15. Gittes F, Mickey B, Nettleton J, Howard J. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923–34 [Google Scholar]
  16. Glowinski R, Pan TW, Hesla TI, Joseph DD. 1999. A distributed Lagrange multiplier/fictitious domain method for particulate flows. Int. J. Multiphase Flow 25:755–94 [Google Scholar]
  17. Greengard L, Rokhlin V. 1987. A fast algorithm for particle simulations. J. Comput. Phys. 73:325–48 [Google Scholar]
  18. Grill SW, Gönczy P, Stelzer EH, Hyman AA. 2001. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630–33 [Google Scholar]
  19. Hämäläinen J, Lindström S, Hämäläinen T, Niskanen H. 2011. Papermaking fibre-suspension flow simulations at multiple scales. J. Eng. Math. 71:55–79 [Google Scholar]
  20. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P. et al. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420–25 [Google Scholar]
  21. Hird SN, White JG. 1993. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 121:1343–55 [Google Scholar]
  22. Hohenegger C, Cook S, Shinar T. 2014. Dimensional reduction of a multiscale continuum model of microtubule gliding assays. SIAM J. Appl. Math. 74:1338–53 [Google Scholar]
  23. Jeffery G. 1922. The motion of ellipsoidal particles immersed in a viscous fluid. Proc. R. Soc. Lond. A 102:161–79 [Google Scholar]
  24. Juelicher F, Kruse K, Prost J, Joanny JF. 2007. Active behavior of the cytoskeleton. Phys. Rep. 449:3–28 [Google Scholar]
  25. Keber FC, Loiseau E, Sanchez T, DeCamp SJ, Giomi L. et al. 2014. Topology and dynamics of active nematic vesicles. Science 345:1135–39 [Google Scholar]
  26. Keller J, Rubinow S. 1976. Slender-body theory for slow viscous flow. J. Fluid Mech. 75:705–14 [Google Scholar]
  27. Kimura A, Onami S. 2005. Computer simulations and image processing reveal length-dependent pulling force as the primary mechanism for C. elegans male pronuclear migration. Dev. Cell 8:765–75 [Google Scholar]
  28. Kimura A, Onami S. 2007. Local cortical pulling-force repression switches centrosomal centration and posterior displacement in C. elegans. J. Cell Biol. 179:1347–54 [Google Scholar]
  29. Kimura K, Kimura A. 2011. Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. PNAS 108:137–42 [Google Scholar]
  30. Koch D, Subramanian G. 2011. Collective hydrodynamics of swimming microorganisms: living fluids. Annu. Rev. Fluid Mech. 43:637–59 [Google Scholar]
  31. Lindner A, Shelley MJ. 2015. Elastic fibers in flows. Fluid-Structure Interactions in Low-Reynolds-Number Flows C Duprat, H Stone Cambridge, UK: R. Soc. Chem. In press [Google Scholar]
  32. Loughlin R, Heald R, Nédélec F. 2010. A computational model predicts Xenopus meiotic spindle organization. J. Cell Biol. 191:1239–49 [Google Scholar]
  33. Maier W, Saupe A. 1958. Eine einfache molekulare Theorie des nematischen kristallinflüssigen Zustandes. Z. Nat. A 13:564–66 [Google Scholar]
  34. Mardin BR, Schiebel E. 2012. Breaking the ties that bind: new advances in centrosome biology. J. Cell Biol. 197:11–18 [Google Scholar]
  35. McIntosh JR, Molodtsov MI, Ataullakhanov FI. 2012. Biophysics of mitosis. Q. Rev. Biophys. 45:147–207 [Google Scholar]
  36. Mickey B, Howard J. 1995. Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130:909–17 [Google Scholar]
  37. Mitchison T, Kirschner M. 1984. Dynamic instability of microtubule growth. Nature 312:237–42 [Google Scholar]
  38. Moeendarbary E, Valon L, Fritzsche M, Harris AR, Moulding DA. et al. 2013. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 12:253–61 [Google Scholar]
  39. Nakazawa H, Sekimoto K. 1996. Polarity sorting in a bundle of actin filaments by two-headed myosins. J. Phys. Soc. Jpn. 65:2404–7 [Google Scholar]
  40. Nédélec F, Foethke D. 2007. Collective Langevin dynamics of flexible cytoskeletal fibers. N. J. Phys. 9:427 [Google Scholar]
  41. Nédélec F, Surrey T, Maggs A, Leibler S. 1997. Self-organization of microtubules and motors. Nature 389:305–8 [Google Scholar]
  42. Nguyen H, Fauci L. 2014. Hydrodynamics of diatom chains and semiflexible fibres. J. R. Soc. Interface 11:20140314 [Google Scholar]
  43. Niwayama R, Shinohara K, Kimura A. 2011. Hydrodynamic property of the cytoplasm is sufficient to mediate cytoplasmic streaming in the Caenorhabiditis elegans embryo. PNAS 108:11900–5 [Google Scholar]
  44. Olson SD, Lim S, Cortez R. 2013. Modeling the dynamics of an elastic rod with intrinsic curvature and twist using a regularized stokes formulation. J. Comput. Phys. 238:169–87 [Google Scholar]
  45. Peskin C. 2002. The immersed boundary method. Acta Numer. 11:479–517 [Google Scholar]
  46. Power H, Miranda G. 1987. Second kind integral equation formulation of Stokes' flows past a particle of arbitrary shape. SIAM J. Appl. Math. 47:689–98 [Google Scholar]
  47. Pozrikidis C. 1992. Boundary Integral and Singularity Methods for Linearized Viscous Flow Cambridge, UK: Cambridge Univ. Press
  48. Prost J, Jülicher F, Joanny J. 2015. Active gel physics. Nat. Phys. 11:111–17 [Google Scholar]
  49. Reinsch S, Gonczy P. 1998. Mechanisms of nuclear positioning. J. Cell Sci. 111:2283–95 [Google Scholar]
  50. Saad Y, Schultz MH. 1986. GMRES: a generalized minimal residual algorithm for solving nonsymmetric linear systems. SIAM J. Sci. Stat. Comput. 7:856–69 [Google Scholar]
  51. Saintillan D, Shelley MJ. 2008a. Instabilities and pattern formation in active particle suspensions: kinetic theory and continuum simulations. Phys. Rev. Lett. 100:178103 [Google Scholar]
  52. Saintillan D, Shelley MJ. 2008b. Instabilities, pattern formation, and mixing in active suspensions. Phys. Fluids 20:123304 [Google Scholar]
  53. Saintillan D, Shelley MJ. 2013. Active suspensions and their nonlinear models. C. R. Phys. 14:497–517 [Google Scholar]
  54. Sanchez T, Chen D, DeCamp S, Heymann M, Dogic Z. 2012. Spontaneous motion in hierarchically assembled active matter. Nature 491:431–34 [Google Scholar]
  55. Sanchez T, Welch D, Nicastro D, Dogic Z. 2011. Cilia-like beating of active microtubule bundles. Science 333:456–59 [Google Scholar]
  56. Saunders WS, Hoyt MA. 1992. Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell 70:451–58 [Google Scholar]
  57. Schaller V, Weber C, Semmrich C, Frey E, Bausch A. 2010. Polar patterns of driven filaments. Nature 467:73–77 [Google Scholar]
  58. Shinar T, Mano M, Piano F, Shelley MJ. 2011. A model of cytoplasmically driven microtubule-based motion in the single-celled Caenorhabditis elegans embryo. PNAS 108:10508–13 [Google Scholar]
  59. Simha R, Ramaswamy S. 2002. Statistical hydrodynamics of ordered suspensions of self-propelled particles: waves, giant number fluctuations and instabilities. Physica A 306:262–69 [Google Scholar]
  60. Strychalski W, Copos CA, Lewis OL, Guy RD. 2015. A poroelastic immersed boundary method with applications to cell biology. J. Comput. Phys. 282:77–97 [Google Scholar]
  61. Subramanian G, Koch D. 2009. Critical bacterial concentration for the onset of collective swimming. J. Fluid Mech. 632:359–400 [Google Scholar]
  62. Sumino Y, Nagai KH, Shitaka Y, Tanaka D, Yoshikawa K. et al. 2012. Large-scale vortex lattice emerging from collectively moving microtubules. Nature 483:448–52 [Google Scholar]
  63. Surrey T, Nédélec F, Leibler S, Karsenti E. 2001. Physical properties determining self-organization of motors and microtubules. Science 292:1167–71 [Google Scholar]
  64. Thampi S, Golestanian R, Yeomans J. 2013. Velocity correlations in an active nematic. Phys. Rev. Lett. 111:118101 [Google Scholar]
  65. Thampi S, Golestanian R, Yeomans J. 2014. Instabilities and topological defects in active nematics. Europhys. Lett. 105:18001 [Google Scholar]
  66. Tornberg AK, Shelley MJ. 2004. Simulating the dynamics and interactions of elastic filaments in Stokes flows. J. Comput. Phys. 196:8–40 [Google Scholar]
  67. Verchot-Lubicz J, Goldstein RE. 2010. Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240:99–107 [Google Scholar]
  68. Verde F, Berrez JM, Antony C, Karsenti E. 1991. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112:1177–87 [Google Scholar]
  69. Vignaud T, Blanchoin L, Théry M. 2012. Directed cytoskeleton self-organization. Trends Cell Biol. 22:671–82 [Google Scholar]
  70. Visscher K, Schnitzer M, Block S. 1999. Single kinesin molecules studied with a molecular force clamp. Nature 400:184–89 [Google Scholar]
  71. Ward JJ, Roque H, Antony C, Nédélec F. 2015. Mechanical design principles of a mitotic spindle. eLife 3:e03398 [Google Scholar]
  72. Woodhouse FG, Goldstein RE. 2012. Spontaneous circulation of confined active suspensions. Phys. Rev. Lett. 109:168105 [Google Scholar]
  73. Woodhouse FG, Goldstein RE. 2013. Cytoplasmic streaming in plant cells emerges naturally by microfilament self-organization. PNAS 110:14132–37 [Google Scholar]
  74. Ying L, Biros G, Zorin D. 2004. A kernel-independent adaptive fast multipole algorithm in two and three dimensions. J. Comput. Phys. 196:591–626 [Google Scholar]
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