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Flows, self-organization, and transport in living cells
Phys. Rev. Fluids 9, 120501 – Published 11 December, 2024
DOI: https://doi.org/10.1103/PhysRevFluids.9.120501
Abstract
This paper briefly reprises, with added commentary, a talk I gave on transport and flows within living cells at an APS-DFD meeting. Directed transport is especially important in large cells, such as eggs where developmental factors need to be properly localized, and early embryos whose organelles and genetic material must be properly positioned before cell division. I discuss two cases—a nematode single-cell embryo and a fruit fly egg cell—where advances in mathematical modeling and large-scale simulation of fluid-structure interactions have helped us understand fundamental mechanisms of force transduction and self-organization within the cell.
Physics Subject Headings (PhySH)
Article Text
References (48)
- J. B. S. Haldane, On being the right size, Harper's Magazine 425 (1926).
- 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).
- K. Luby-Phelps, Cytoarchitecture and physical properties of cytoplasm: Volume, viscosity, diffusion, intracellular surface area, Int. Rev. Cytol. 192, 189 (1999).
- D. Needleman and M. Shelley, The stormy fluid dynamics of the living cell, Phys. Today 72(9), 32 (2019).
- B. Corti, Osservazioni Microscopiche Sulla Tremella E Sulla Circolazione Del Fluido in Una Pianta Acquajuola (Appresso Giuseppe Rocchi, Lucca, 1774).
- R. E. Goldstein and J.-W. van de Meent, A physical perspective on cytoplasmic streaming, Interface Focus. 5, 20150030 (2015).
- R. Brown, Observations on the Organs and Mode of Fecundation in Orchideae and Asclepiadeae (Taylor, London, 1833).
- L. Pickens, Organization of Cells and Other Organisms (Clarendon Press, London, 1960).
- A. Mogilner and A. Manhart, Intracellular fluid mechanics: Coupling cytoplasmic flow with active cytoskeletal gel, Annu. Rev. Fluid Mech. 50, 347 (2018).
- K. Yi, J. R. Unruh, M. Deng, B. D. Slaughter, B. Rubinstein, and R. Li, Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes, Nat. Cell Biol. 13, 1252 (2011).
- K. Kimura, A. Mamane, T. Sasaki, K. Sato, J. Takagi, R. Niwayama, L. Hufnagel, Y. Shimamoto, J.-F. Joanny, S. Uchida et al., Endoplasmic-reticulum-mediated microtubule alignment governs cytoplasmic streaming, Nature Cell Biology 19, 399 (2017).
- S. N. Hird and J. G. White, Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans, J. Cell Biol. 121, 1343 (1993).
- M. Mayer, M. Depken, J. S. Bois, F. Jülicher, and S. W. Grill, Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows, Nature (London) 467, 617 (2010).
- A. G. Gubieda, J. R. Packer, I. Squires, J. Martin, and J. Rodriguez, Going with the flow: Insights from Caenorhabditis elegans zygote polarization, Phil. Trans. R. Soc. B 375, 20190555 (2020).
- H.-Y. Wu, E. Nazockdast, M. J. Shelley, and D. J. Needleman, Forces positioning the mitotic spindle: Theories, and now experiments, BioEssays 39, 1600212 (2017).
- H.-Y. Wu, G. Kabacaoğlu, E. Nazockdast, H.-C. Chang, M. J. Shelley, and D. J. Needleman, Laser ablation and fluid flows reveal the mechanism behind spindle and centrosome positioning, Nat. Phys. 20, 157 (2024).
- S. Redemann, B. Weber, M. Möller, J.-M. Verbavatz, A. A. Hyman, D. Baum, S. Prohaska, and T. Müller-Reichert, The segmentation of microtubules in electron tomograms using amira, Mitosis: Methods Protoc. 1136, 261 (2014).
- R. C. Wilson and J. A. Doudna, Molecular mechanisms of RNA interference, Annu. Rev. Biophys. 42, 217 (2013).
- C. Garzon-Coral, H. A. Fantana, and J. Howard, A force-generating machinery maintains the spindle at the cell center during mitosis, Science 352, 1124 (2016).
- K. Kimura and A. Kimura, Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo, Proc. Natl. Acad. Sci. USA 108, 137 (2011).
- T. Shinar, M. Mana, F. Piano, and M. J. Shelley, A model of cytoplasmically driven microtubule-based motion in the single-celled Caenorhabditis elegans embryo, Proc. Natl. Acad. Sci. USA 108, 10508 (2011).
- M. J. Shelley, The dynamics of microtubule/motor-protein assemblies in biology and physics, Annu. Rev. Fluid Mech. 48, 487 (2016).
- A.-K. Tornberg and M. J. Shelley, Simulating the dynamics and interactions of flexible fibers in stokes flows, J. Comput. Phys. 196, 8 (2004).
- 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).
- O. du Roure, A. Lindner, E. N. Nazockdast, and M. J. Shelley, Dynamics of flexible fibers in viscous flows and fluids, Annu. Rev. Fluid Mech. 51, 539 (2019).
- E. Nazockdast, A. Rahimian, D. Needleman, and M. Shelley, Cytoplasmic flows as signatures for the mechanics of mitotic positioning, Mol. Biol. Cell 28, 3261 (2017).
- SkellySim cellular dynamics package, https://github.com/flatironinstitute/SkellySim (2022).
- D. B. Stein and M. J. Shelley, Computational tools for cellular scale biophysics, Curr. Opin. Cell Biol. 89, 102379 (2024).
- Y.-N. Young, V. G. Herrera, H. Zhang, R. Farhadifar, and M. J. Shelley, A first-principles geometric model for dynamics of motor-driven centrosomal asters, bioRxiv (2024) [Phys. Rev. Res. (to be published)].
- M. E. Quinlan, Cytoplasmic streaming in the drosophila oocyte, Annu. Rev. Cell Dev. Biol. 32, 173 (2016).
- J. Imran Alsous, N. Romeo, J. A. Jackson, F. M. Mason, J. Dunkel, and A. C. Martin, Dynamics of hydraulic and contractile wave-mediated fluid transport during Drosophila oogenesis, Proc. Natl. Acad. Sci. USA 118, e2019749118 (2021).
- H. O. Gutzeit and R. Koppa, Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila, Development 67, 101 (1982).
- J. B. Glotzer, R. Saffrich, M. Glotzer, and A. Ephrussi, Cytoplasmic flows localize injected Oskar RNA in Drosophila oocytes, Curr. Biol. 7, 326 (1997).
- S. Ganguly, L. S. Williams, I. M. Palacios, and R. E. Goldstein, Cytoplasmic streaming in Drosophila oocytes varies with kinesin activity and correlates with the microtubule cytoskeleton architecture, Proc. Natl. Acad. Sci. USA 109, 15109 (2012).
- P. Khuc Trong, H. Doerflinger, J. Dunkel, D. St Johnston, and R. E. Goldstein, Cortical microtubule nucleation can organise the cytoskeleton of Drosophila oocytes to define the anteroposterior axis, Elife 4, e06088 (2015).
- A. N. Becalska and E. R. Gavis, Lighting up mRNA localization in Drosophila oogenesis, Development 136, 2493 (2009).
- W. Lu, M. Lakonishok, A. S. Serpinskaya, D. Kirchenbüechler, S.-C. Ling, and V. I. Gelfand, Ooplasmic flow cooperates with transport and anchorage in Drosophila oocyte posterior determination, J. Cell Biol. 217, 3497 (2018).
- W. Lu, M. Winding, M. Lakonishok, J. Wildonger, and V. I. Gelfand, Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes, Proc. Natl. Acad. Sci. USA 113, E4995 (2016).
- C. E. Monteith, M. E. Brunner, I. Djagaeva, A. M. Bielecki, J. M. Deutsch, and W. M. Saxton, A mechanism for cytoplasmic streaming: Kinesin-driven alignment of microtubules and fast fluid flows, Biophys. J. 110, 2053 (2016).
- S. Dutta, R. Farhadifar, W. Lu, G. Kabacaoğlu, R. Blackwell, D. B. Stein, M. Lakonishok, V. I. Gelfand, S. Y. Shvartsman, and M. J. Shelley, Self-organized intracellular twisters, Nat. Phys. 20, 666 (2024).
- 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).
- J. B. Keller and S. I. Rubinow, Slender-body theory for slow viscous flow, J. Fluid Mech. 75, 705 (1976).
- D. B. Stein and M. J. Shelley, Coarse graining the dynamics of immersed and driven fiber assemblies, Phys. Rev. Fluids 4, 073302 (2019).
- T. A. Westwood and E. E. Keaveny, Coordinated motion of active filaments on spherical surfaces, Phys. Rev. Fluids 6, L121101 (2021).
- O. Jain, B. Chakrabarti, R. Farhadifar, E. R. Gavis, M. J. Shelley, and S. Y. Shvartsman, Geometric effects in large scale intracellular flows, arXiv:2409.06763.
- B. Chakrabarti, M. Rachh, S. Y. Shvartsman, and M. J. Shelley, Cytoplasmic stirring by active carpets, Proc. Natl. Acad. Sci. USA 121, e2405114121 (2024).
- D. Saintillan and M. J. Shelley, Active suspensions and their nonlinear models, C. R. Phys. 14, 497 (2013).
- C. Hernández-López, A. Puliafito, Y. Xu, Z. Lu, S. Di Talia, and M. Vergassola, Two-fluid dynamics and micron-thin boundary layers shape cytoplasmic flows in early Drosophila embryos, Proc. Natl. Acad. Sci. USA 120, e2302879120 (2023).