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Active matter at the interface between materials science and cell biology

Abstract

The remarkable processes that characterize living organisms, such as motility, self-healing and reproduction, are fuelled by a continuous injection of energy at the microscale. The field of active matter focuses on understanding how the collective behaviours of internally driven components can give rise to these biological phenomena, while also striving to produce synthetic materials composed of active energy-consuming components. The synergistic approach of studying active matter in both living cells and reconstituted systems assembled from biochemical building blocks has the potential to transform our understanding of both cell biology and materials science. This methodology can provide insight into the fundamental principles that govern the dynamical behaviours of self-organizing subcellular structures, and can lead to the design of artificial materials and machines that operate away from equilibrium and can thus attain life-like properties. In this Review, we focus on active materials made of cytoskeletal components, highlighting the role of active stresses and how they drive self-organization of both cellular structures and macroscale materials, which are machines powered by nanomachines.

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Figure 1: Organisms are machines made from machines.
Figure 2: Properties of mitotic spindles.
Figure 3: Symmetries of filament assemblies and topological defects.
Figure 4: Active stresses in active materials.
Figure 5: Synthetic active matter systems assembled from cytoskeletal components.
Figure 6: Machines built from machines: surface-confined active nematics drive cell-like protrusions and deformations.
Figure 7: Theory and experiments on subcellular structures.

References

  1. 1

    Riskin, J. The Restless Clock: A History of the Centuries-long Argument over What Makes Living Things Tick (Univ. of Chicago Press, 2016).

    Google Scholar 

  2. 2

    Cross, M. C. & Hohenberg, P. C. Pattern formation outside of equilibrium. Rev. Mod. Phys. 65, 851–1112 (1993).

    CAS  Article  Google Scholar 

  3. 3

    Vale, R. D. The molecular motor toolbox for intracellular transport. Cell 112, 467–480 (2003).

    CAS  Article  Google Scholar 

  4. 4

    Jülicher, F., Ajdari, A. & Prost, J. Modeling molecular motors. Rev. Mod. Phys. 69, 1269–1281 (1997).

    Article  Google Scholar 

  5. 5

    Nedelec, F., Surrey, T., Maggs, A. C. & Leibler, S. Self-organization of microtubules and motors. Nature 389, 305–308 (1997).

    CAS  Article  Google Scholar 

  6. 6

    Surrey, T., Nédélec, F., Leibler, S. & Karsenti, E. Physical properties determining self-organization of motors and microtubules. Science 292, 1167–1171 (2001).

    CAS  Article  Google Scholar 

  7. 7

    Vicsek, T., Czirók, A., Ben-Jacob, E., Cohen, I. & Shochet, O. Novel type of phase transition in a system of self-driven particles. Phys. Rev. Lett. 75, 1226–1229 (1995).

    CAS  Article  Google Scholar 

  8. 8

    Toner, J. & Tu, Y. Flocks, herds, and schools: a quantitative theory of flocking. Phys. Rev. E 58, 4828–4858 (1998).

    CAS  Article  Google Scholar 

  9. 9

    Simha, R. A. & Ramaswamy, S. Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles. Phys. Rev. Lett. 89, 058101 (2002).

    Article  CAS  Google Scholar 

  10. 10

    Saintillan, D. & Shelley, M. J. Active suspensions and their nonlinear models. C. R. Phys. 14, 497–517 (2013).

    CAS  Article  Google Scholar 

  11. 11

    Ramaswamy, S. The mechanics and statistics of active matter. Annu. Rev. Condens. Matter Phys. 1, 323–345 (2010).

    Article  Google Scholar 

  12. 12

    Toner, J., Tu, Y. & Ramaswamy, S. Hydrodynamics and phases of flocks. Ann. Phys. 318, 170–244 (2005).

    CAS  Article  Google Scholar 

  13. 13

    Prost, J., Jülicher, F. & Joanny, J. Active gel physics. Nat. Phys. 11, 111–117 (2015).

    CAS  Article  Google Scholar 

  14. 14

    Shelley, M. J. The dynamics of microtubule/motor-protein assemblies in biology and physics. Annu. Rev. Fluid Mechan. 48, 487–506 (2016).

    Article  Google Scholar 

  15. 15

    Hagan, M. F. & Baskaran, A. Emergent self-organization in active materials. Curr. Opin. Cell Biol. 38, 74–80 (2016).

    CAS  Article  Google Scholar 

  16. 16

    Marchetti, M. et al. Hydrodynamics of soft active matter. Rev. Modern Phys. 85, 1143–1189 (2013).

    CAS  Article  Google Scholar 

  17. 17

    Fletcher, D. A. & Geissler, P. L. Active biological materials. Annu. Rev. Phys. Chem. 60, 469–486 (2009).

    CAS  Article  Google Scholar 

  18. 18

    Schrader, F. Mitosis (Columbia Univ. Press, 1944).

    Google Scholar 

  19. 19

    Rappaport, R. Cytokinesis in Animal Cells (Cambridge Univ. Press, 1996).

    Book  Google Scholar 

  20. 20

    Bechtel, W. Discovering Cell Mechanisms: The Creation of Modern Cell Biology (Cambridge Univ. Press, 2006).

    Google Scholar 

  21. 21

    Inoue, S., Fuseler, J., Salmon, E. D. & Ellis, G. W. Functional organization of mitotic microtubules — physical chemistry of in vivo equilibrium system. Biophys. J. 15, 725–744 (1975).

    CAS  Article  Google Scholar 

  22. 22

    Oosawa, F. & Asakura, S. Thermodynamics of the Polymerization of Protein (Academic, 1975).

    Google Scholar 

  23. 23

    Harold, F. M. The Vital Force: A Study of Bioenergetics (W. H. Freeman, 1986).

    Google Scholar 

  24. 24

    Schrödinger, E. What is Life? With Mind and Matter and Autobiographical Sketches (Cambridge Univ. Press, 1992).

    Book  Google Scholar 

  25. 25

    Kirschner, M. W. Implications of treadmilling for the stability and polarity of actin and tubulin polymers in vivo. J. Cell Biol. 86, 330–334 (1980).

    CAS  Article  Google Scholar 

  26. 26

    Verde, F., Berrez, J. M., Antony, C. & Karsenti, E. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs — requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112, 1177–1187 (1991).

    CAS  Article  Google Scholar 

  27. 27

    Mitchison, T. J. Self-organization of polymer-motor systems in the cytoskeleton. Phil. Trans. R. Soc. Lond. B Biol. Sci. 336, 99–106 (1992).

    CAS  Article  Google Scholar 

  28. 28

    Sawin, K. E. & Scholey, J. M. Motor proteins in cell division. Trends Cell Biol. 1, 122–129 (1991).

    CAS  Article  Google Scholar 

  29. 29

    Subramanian, R. & Kapoor, T. M. Building complexity: insights into self-organized assembly of microtubule-based architectures. Dev. Cell 23, 874–885 (2012).

    CAS  Article  Google Scholar 

  30. 30

    Vignaud, T., Blanchoin, L. & Thery, M. Directed cytoskeleton self-organization. Trends Cell Biol. 22, 671–682 (2012).

    CAS  Article  Google Scholar 

  31. 31

    Glick, B. S. Integrated self-organization of transitional ER and early Golgi compartments. Bioessays 36, 129–133 (2014).

    CAS  Article  Google Scholar 

  32. 32

    Kirschner, M., Gerhart, J. & Mitchison, T. Molecular ‘vitalism’. Cell 100, 79–88 (2000).

    CAS  Article  Google Scholar 

  33. 33

    Misteli, T. Beyond the sequence: cellular organization of genome function. Cell 128, 787–800 (2007).

    CAS  Article  Google Scholar 

  34. 34

    Howard, J. Molecular motors: structural adaptations to cellular functions. Nature 389, 561–567 (1997).

    CAS  Article  Google Scholar 

  35. 35

    Leibler, S. & Huse, D. A. Porters versus rowers: a unified stochastic model of motor proteins. J. Cell Biol. 121, 1357–1368 (1993).

    CAS  Article  Google Scholar 

  36. 36

    Vale, R. D. & Milligan, R. A. The way things move: looking under the hood of molecular motor proteins. Science 288, 88–95 (2000).

    CAS  Article  Google Scholar 

  37. 37

    Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721–727 (1993).

    CAS  Article  Google Scholar 

  38. 38

    Finer, J. T., Simmons, R. M. & Spudich, J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113–119 (1994).

    CAS  Article  Google Scholar 

  39. 39

    Vale, R. D. et al. Direct observation of single kinesin molecules moving along microtubules. Nature 380, 451–453 (1996).

    CAS  Article  Google Scholar 

  40. 40

    Chen, L., Nakamura, M., Schindler, T. D., Parker, D. & Bryant, Z. Engineering controllable bidirectional molecular motors based on myosin. Nat. Nanotechnol. 7, 252–256 (2012).

    CAS  Article  Google Scholar 

  41. 41

    Nakamura, M. et al. Remote control of myosin and kinesin motors using light-activated gearshifting. Nat. Nanotechnol. 9, 693–697 (2014).

    CAS  Article  Google Scholar 

  42. 42

    Schindler, T. D., Chen, L., Lebel, P., Nakamura, M. & Bryant, Z. Engineering myosins for long-range transport on actin filaments. Nat. Nanotechnol. 9, 33–38 (2014).

    CAS  Article  Google Scholar 

  43. 43

    Nédélec, F., Surrey, T. & Maggs, A. Dynamic concentration of motors in microtubule arrays. Phys. Rev. Lett. 86, 3192–3195 (2001).

    Article  CAS  Google Scholar 

  44. 44

    Liverpool, T. B. & Marchetti, M. C. Bridging the microscopic and the hydrodynamic in active filament solutions. EPL 69, 846–852 (2005).

    CAS  Article  Google Scholar 

  45. 45

    Chaikin, P. M. & Lubensky, T. C. Principles of Condensed Matter Physics (Cambridge Univ. Press, 2000).

    Google Scholar 

  46. 46

    Needleman, D. J. et al. Synchrotron X-ray diffraction study of microtubules buckling and bundling under osmotic stress: a probe of interprotofilament interactions. Phys. Rev. Lett. 93, 198104 (2004).

    Article  CAS  Google Scholar 

  47. 47

    Hilitski, F. et al. Measuring cohesion between macromolecular filaments one pair at a time: depletion-induced microtubule bundling. Phys. Rev. Lett. 114, 138102 (2015).

    Article  CAS  Google Scholar 

  48. 48

    Henkin, G., DeCamp, S. J., Chen, D. T., Sanchez, T. & Dogic, Z. Tunable dynamics of microtubule-based active isotropic gels. Phil. Trans. A. Math. Phys. Eng. Sci. 372, 20140142 (2014).

    Article  CAS  Google Scholar 

  49. 49

    Sanchez, T., Chen, D. T., DeCamp, S. J., Heymann, M. & Dogic, Z. Spontaneous motion in hierarchically assembled active matter. Nature 491, 431–434 (2012).

    CAS  Article  Google Scholar 

  50. 50

    Visscher, K., Schnitzer, M. J. & Block, S. M. Single kinesin molecules studied with a molecular force clamp. Nature 400, 184–189 (1999).

    CAS  Article  Google Scholar 

  51. 51

    Szent-Györgyi, A. G. The early history of the biochemistry of muscle contraction. J. Gen. Physiol. 123, 631–641 (2004).

    Article  Google Scholar 

  52. 52

    Szent-Györgyi, A. The contraction of myosin threads. Stud. Inst. Med. Chem. Univ. Szeged 1, 17–26 (1942).

    Google Scholar 

  53. 53

    Murrell, M., Oakes, P. W., Lenz, M. & Gardel, M. L. Forcing cells into shape: the mechanics of actomyosin contractility. Nat. Rev. Mol. Cell Biol. 16, 486–498 (2015).

    CAS  Article  Google Scholar 

  54. 54

    Bendix, P. M. et al. A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys. J. 94, 3126–3136 (2008).

    CAS  Article  Google Scholar 

  55. 55

    Köhler, S., Schaller, V. & Bausch, A. R. Structure formation in active networks. Nat. Mater. 10, 462–468 (2011).

    Article  CAS  Google Scholar 

  56. 56

    e Silva, M. S. et al. Active multistage coarsening of actin networks driven by myosin motors. Proc. Natl Acad. Sci. USA 108, 9408–9413 (2011).

    Article  CAS  Google Scholar 

  57. 57

    Alvarado, J., Sheinman, M., Sharma, A., MacKintosh, F. C. & Koenderink, G. H. Molecular motors robustly drive active gels to a critically connected state. Nat. Phys. 9, 591–597 (2013).

    CAS  Article  Google Scholar 

  58. 58

    Foster, P. J., Furthauer, S., Shelley, M. J. & Needleman, D. J. Active contraction of microtubule networks. eLife 4, e10837 (2015).

    Article  Google Scholar 

  59. 59

    Martin, A. C., Kaschube, M. & Wieschaus, E. F. Pulsed contractions of an actin–myosin network drive apical constriction. Nature 457, 495–499 (2009).

    CAS  Article  Google Scholar 

  60. 60

    Mayer, M., Depken, M., Bois, J. S., Jülicher, F. & Grill, S. W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617–621 (2010).

    CAS  Article  Google Scholar 

  61. 61

    Rauzi, M., Lenne, P.-F. & Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110–1114 (2010).

    CAS  Article  Google Scholar 

  62. 62

    He, L., Wang, X., Tang, H. L. & Montell, D. J. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat. Cell Biol. 12, 1133–1142 (2010).

    CAS  Article  Google Scholar 

  63. 63

    Shah, E. A. & Keren, K. Symmetry breaking in reconstituted actin cortices. eLife 3, e01433 (2014).

    Article  Google Scholar 

  64. 64

    Kruse, K. & Jülicher, F. Actively contracting bundles of polar filaments. Phys. Rev. Lett. 85, 1778–1781 (2000).

    CAS  Article  Google Scholar 

  65. 65

    Nédélec, F. & Surrey, T. Dynamics of microtubule aster formation by motor complexes. C. R. Acad. Sci. Ser. IV Phys. Astrophys. 2, 841–847 (2001).

    Google Scholar 

  66. 66

    Liverpool, T. B., Marchetti, M. C., Joanny, J.-F. & Prost, J. Mechanical response of active gels. EPL 85, 18007 (2009).

    Article  CAS  Google Scholar 

  67. 67

    Lenz, M., Thoresen, T., Gardel, M. L. & Dinner, A. R. Contractile units in disordered actomyosin bundles arise from F-actin buckling. Phys. Rev. Lett. 108, 238107 (2012).

    Article  CAS  Google Scholar 

  68. 68

    Murrell, M. P. & Gardel, M. L. F-Actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex. Proc. Natl Acad. Sci. USA 109, 20820–20825 (2012).

    CAS  Article  Google Scholar 

  69. 69

    Thoresen, T., Lenz, M. & Gardel, M. L. Reconstitution of contractile actomyosin bundles. Biophys. J. 100, 2698–2705 (2011).

    CAS  Article  Google Scholar 

  70. 70

    Giomi, L., Bowick, M. J., Ma, X. & Marchetti, M. C. Defect annihilation and proliferation in active nematics. Phys. Rev. Lett. 110, 228101 (2013).

    Article  CAS  Google Scholar 

  71. 71

    Giomi, L. Geometry and topology of turbulence in active nematics. Phys. Rev. X 5, 031003 (2015).

    Google Scholar 

  72. 72

    Thampi, S. P., Golestanian, R. & Yeomans, J. M. Velocity correlations in an active nematic. Phys. Rev. Lett. 111, 118101 (2013).

    Article  CAS  Google Scholar 

  73. 73

    Gao, T., Blackwell, R., Glaser, M. A., Betterton, M. & Shelley, M. J. Multiscale polar theory of microtubule and motor-protein assemblies. Phys. Rev. Lett. 114, 048101 (2015).

    Article  CAS  Google Scholar 

  74. 74

    Giomi, L., Bowick, M. J., Mishra, P., Sknepnek, R. & Marchetti, M. C. Defect dynamics in active nematics. Phil. Trans. A Math. Phys. Eng. Sci. 372, 20130365 (2014).

    Article  CAS  Google Scholar 

  75. 75

    DeCamp, S. J., Redner, G. S., Baskaran, A., Hagan, M. F. & Dogic, Z. Orientational order of motile defects in active nematics. Nat. Mater. 14, 1110–1115 (2015).

    CAS  Article  Google Scholar 

  76. 76

    Oza, A. U. & Dunkel, J. Antipolar ordering of topological defects in active liquid crystals. New J. Phys. 18, 093006 (2015).

    Article  Google Scholar 

  77. 77

    Putzig, E., Redner, G. S., Baskaran, A. & Baskaran, A. Instabilities, defects, and defect ordering in an overdamped active nematic. Soft Matter 12, 3854–3859 (2016).

    CAS  Article  Google Scholar 

  78. 78

    Doostmohammadi, A., Adamer, M. F., Thampi, S. P. & Yeomans, J. M. Stabilization of active matter by flow-vortex lattices and defect ordering. Nat. Commun. 7, 10557 (2016).

    CAS  Article  Google Scholar 

  79. 79

    Narayan, V., Ramaswamy, S. & Menon, N. Long-lived giant number fluctuations in a swarming granular nematic. Science 317, 105–108 (2007).

    CAS  Article  Google Scholar 

  80. 80

    Duclos, G., Garcia, S., Yevick, H. & Silberzan, P. Perfect nematic order in confined monolayers of spindle-shaped cells. Soft Matter 10, 2346–2353 (2014).

    CAS  Article  Google Scholar 

  81. 81

    Zhou, S., Sokolov, A., Lavrentovich, O. D. & Aranson, I. S. Living liquid crystals. Proc. Natl Acad. Sci. USA 111, 1265–1270 (2014).

    CAS  Article  Google Scholar 

  82. 82

    Bieling, P., Telley, I. A., Piehler, J. & Surrey, T. Processive kinesins require loose mechanical coupling for efficient collective motility. EMBO Rep. 9, 1121–1127 (2008).

    CAS  Article  Google Scholar 

  83. 83

    Blackwell, R. et al. Microscopic origins of anisotropic active stress in motor-driven nematic liquid crystals. Soft Matter 12, 2676–2687 (2016).

    CAS  Article  Google Scholar 

  84. 84

    Gao, T., Blackwell, R., Glaser, M. A., Betterton, M. & Shelley, M. J. Multiscale modeling and simulation of microtubule–motor-protein assemblies. Phys. Rev. E 92, 062709 (2015).

    Article  CAS  Google Scholar 

  85. 85

    Guillamat, P., Ignés-Mullol, J. & Sagués, F. Control of active liquid crystals with a magnetic field. Proc. Natl Acad. Sci. USA 113, 5498–5502 (2016).

    CAS  Article  Google Scholar 

  86. 86

    Howard, J., Hudspeth, A. & Vale, R. Movement of microtubules by single kinesin molecules. Nature 342, 154–158 (1989).

    CAS  Article  Google Scholar 

  87. 87

    Kron, S. J. & Spudich, J. A. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl Acad. Sci. USA 83, 6272–6276 (1986).

    CAS  Article  Google Scholar 

  88. 88

    Schaller, V., Weber, C., Semmrich, C., Frey, E. & Bausch, A. R. Polar patterns of driven filaments. Nature 467, 73–77 (2010).

    CAS  Article  Google Scholar 

  89. 89

    Suzuki, R., Weber, C. A., Frey, E. & Bausch, A. R. Polar pattern formation in driven filament systems requires non-binary particle collisions. Nat. Phys. 11, 839–849 (2015).

    CAS  Article  Google Scholar 

  90. 90

    Sumino, Y. et al. Large-scale vortex lattice emerging from collectively moving microtubules. Nature 483, 448–452 (2012).

    CAS  Article  Google Scholar 

  91. 91

    Kumar, N., Soni, H., Ramaswamy, S. & Sood, A. K. Flocking at a distance in active granular matter. Nat. Commun. 5, 4688 (2014).

    CAS  Article  Google Scholar 

  92. 92

    Bricard, A., Caussin, J.-B., Desreumaux, N., Dauchot, O. & Bartolo, D. Emergence of macroscopic directed motion in populations of motile colloids. Nature 503, 95–98 (2013).

    CAS  Article  Google Scholar 

  93. 93

    Deseigne, J., Dauchot, O. & Chaté, H. Collective motion of vibrated polar disks. Phys. Rev. Lett. 105, 098001 (2010).

    Article  CAS  Google Scholar 

  94. 94

    Buhl, J. et al. From disorder to order in marching locusts. Science 312, 1402–1406 (2006).

    CAS  Article  Google Scholar 

  95. 95

    Wioland, H., Woodhouse, F. G., Dunkel, J., Kessler, J. O. & Goldstein, R. E. Confinement stabilizes a bacterial suspension into a spiral vortex. Phys. Rev. Lett. 110, 268102 (2013).

    Article  CAS  Google Scholar 

  96. 96

    Riedel, I. H., Kruse, K. & Howard, J. A self-organized vortex array of hydrodynamically entrained sperm cells. Science 309, 300–303 (2005).

    CAS  Article  Google Scholar 

  97. 97

    Doxzen, K. et al. Guidance of collective cell migration by substrate geometry. Integr. Biol. (Camb.) 5, 1026–1035 (2013).

    CAS  Article  Google Scholar 

  98. 98

    Wu, K.-T. et al. Transition from turbulent to coherent flows in confined three-dimensional active fluids. Science 355, eaal1979 (2017).

    Article  CAS  Google Scholar 

  99. 99

    Brugués, J. & Needleman, D. Physical basis of spindle self-organization. Proc. Natl Acad. Sci. USA 111, 18496–18500 (2014).

    Article  CAS  Google Scholar 

  100. 100

    Keber, F. C. et al. Topology and dynamics of active nematic vesicles. Science 345, 1135–1139 (2014).

    CAS  Article  Google Scholar 

  101. 101

    Nelson, D. R. Toward a tetravalent chemistry of colloids. Nano Lett. 2, 1125–1129 (2002).

    CAS  Article  Google Scholar 

  102. 102

    Hatwalne, Y., Ramaswamy, S., Rao, M. & Simha, R. A. Rheology of active-particle suspensions. Phys. Rev. Lett. 92, 118101 (2004).

    Article  CAS  Google Scholar 

  103. 103

    Gardel, M. L., Valentine, M. T. & Weitz, D. A. in Microscale Diagnostic Techniques 1–49 (Springer, 2005).

    Book  Google Scholar 

  104. 104

    Lau, A. W. C., Hoffman, B. D., Davies, A., Crocker, J. C. & Lubensky, T. C. Microrheology stress fluctuations and active behavior of living cells. Phys. Rev. Lett. 91, 198101 (2003).

    CAS  Article  Google Scholar 

  105. 105

    Mizuno, D., Tardin, C., Schmidt, C. F. & MacKintosh, F. C. Nonequilibrium mechanics of active cytoskeletal networks. Science 315, 370–373 (2007).

    CAS  Article  Google Scholar 

  106. 106

    Chen, D. T. N. et al. Fluctuations and rheology in active bacterial suspensions. Phys. Rev. Lett. 99, 148302 (2007).

    CAS  Article  Google Scholar 

  107. 107

    Schlosser, F., Rehfeldt, F. & Schmidt, C. F. Force fluctuations in three-dimensional suspended fibroblasts. Phil. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140028 (2015).

    Article  CAS  Google Scholar 

  108. 108

    Mizuno, D., Bacabac, R., Tardin, C., Head, D. & Schmidt, C. F. High-resolution probing of cellular force transmission. Phys. Rev. Lett. 102, 168102 (2009).

    Article  CAS  Google Scholar 

  109. 109

    Bursac, P. et al. Cytoskeletal remodelling and slow dynamics in the living cell. Nat. Mater. 4, 557–561 (2005).

    CAS  Article  Google Scholar 

  110. 110

    Guo, M. et al. Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy. Cell 158, 822–832 (2014).

    CAS  Article  Google Scholar 

  111. 111

    Wilhelm, C. Out-of-equilibrium microrheology inside living cells. Phys. Rev. Lett. 101, 028101 (2008).

    Article  CAS  Google Scholar 

  112. 112

    Robert, D., Nguyen, T. H., Gallet, F. & Wilhelm, C. In vivo determination of fluctuating forces during endosome trafficking using a combination of active and passive microrheology. PLoS One 5, e10046 (2010).

    Article  CAS  Google Scholar 

  113. 113

    MacKintosh, F. C. & Levine, A. J. Nonequilibrium mechanics and dynamics of motor-activated gels. Phys. Rev. Lett. 100, 018104 (2008).

    CAS  Article  Google Scholar 

  114. 114

    Almonacid, M. et al. Active diffusion positions the nucleus in mouse oocytes. Nat. Cell Biol. 17, 470–479 (2015).

    CAS  Article  Google Scholar 

  115. 115

    López, H. M., Gachelin, J., Douarche, C., Auradou, H. & Clément, E. Turning bacteria suspensions into superfluids. Phys. Rev. Lett. 115, 028301 (2015).

    Article  CAS  Google Scholar 

  116. 116

    Naganathan, S. R., Furthauer, S., Nishikawa, M., Julicher, F. & Grill, S. W. Active torque generation by the actomyosin cell cortex drives left-right symmetry breaking. eLife 3, e04165 (2014).

    Article  Google Scholar 

  117. 117

    Tinevez, J. Y. et al. Role of cortical tension in bleb growth. Proc. Natl Acad. Sci. USA 106, 18581–18586 (2009).

    CAS  Article  Google Scholar 

  118. 118

    Sedzinski, J. et al. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476, 462–466 (2011).

    CAS  Article  Google Scholar 

  119. 119

    Turlier, H., Audoly, B., Prost, J. & Joanny, J. F. Furrow constriction in animal cell cytokinesis. Biophys. J. 106, 114–123 (2014).

    CAS  Article  Google Scholar 

  120. 120

    Sain, A., Inamdar, M. M. & Jülicher, F. Dynamic force balances and cell shape changes during cytokinesis. Phys. Rev. Lett. 114, 048102 (2015).

    Article  CAS  Google Scholar 

  121. 121

    Ruprecht, V. et al. Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell 160, 673–685 (2015).

    CAS  Article  Google Scholar 

  122. 122

    Bergert, M. et al. Force transmission during adhesion-independent migration. Nat. Cell Biol. 17, 524–529 (2015).

    CAS  Article  Google Scholar 

  123. 123

    Aranson, I. S. Physical Models of Cell Motility (Springer, 2016).

    Book  Google Scholar 

  124. 124

    Löber, J., Ziebert, F. & Aranson, I. S. Modeling crawling cell movement on soft engineered substrates. Soft Matter 10, 1365–1373 (2014).

    Article  Google Scholar 

  125. 125

    Tjhung, E., Tiribocchi, A., Marenduzzo, D. & Cates, M. E. A minimal physical model captures the shapes of crawling cells. Nat. Commun. 6, 5420 (2015).

    CAS  Article  Google Scholar 

  126. 126

    Saha, A. et al. Determining physical properties of the cell cortex. Biophys. J. 110, 1421–1429 (2016).

    CAS  Article  Google Scholar 

  127. 127

    Oh, D., Yu, C.-H. & Needleman, D. J. Spatial organization of the Ran pathway by microtubules in mitosis. Proc. Natl Acad. Sci. USA 113, 8729–8734 (2016).

    CAS  Article  Google Scholar 

  128. 128

    Gowrishankar, K. et al. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149, 1353–1367 (2012).

    CAS  Article  Google Scholar 

  129. 129

    Moseley, J. B. & Goode, B. L. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70, 605–645 (2006).

    CAS  Article  Google Scholar 

  130. 130

    Loisel, T. P., Boujemaa, R., Pantaloni, D. & Carlier, M.-F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613–616 (1999).

    CAS  Article  Google Scholar 

  131. 131

    Dogterom, M. & Yurke, B. Measurement of the force–velocity relation for growing microtubules. Science 278, 856–860 (1997).

    CAS  Article  Google Scholar 

  132. 132

    Howard, J., Grill, S. W. & Bois, J. S. Turing's next steps: the mechanochemical basis of morphogenesis. Nat. Rev. Mol. Cell Biol. 12, 392–398 (2011).

    Article  CAS  Google Scholar 

  133. 133

    Bois, J. S., Jülicher, F. & Grill, S. W. Pattern formation in active fluids. Phys. Rev. Lett. 106, 028103 (2011).

    Article  CAS  Google Scholar 

  134. 134

    Kumar, K. V., Bois, J. S., Jülicher, F. & Grill, S. W. Pulsatory patterns in active fluids. Phys. Rev. Lett. 112, 208101 (2014).

    Article  CAS  Google Scholar 

  135. 135

    Bruinsma, R., Grosberg, A. Y., Rabin, Y. & Zidovska, A. Chromatin hydrodynamics. Biophys. J. 106, 1871–1881 (2014).

    CAS  Article  Google Scholar 

  136. 136

    Zidovska, A., Weitz, D. A. & Mitchison, T. J. Micron-scale coherence in interphase chromatin dynamics. Proc. Natl Acad. Sci. USA 110, 15555–15560 (2013).

    CAS  Article  Google Scholar 

  137. 137

    Weber, S. C., Spakowitz, A. J. & Theriot, J. A. Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm. Phys. Rev. Lett. 104, 238102 (2010).

    Article  CAS  Google Scholar 

  138. 138

    Fudenberg, G. et al. Formation of chromosomal domains by loop extrusion. Cell Rep. 15, 2038–2049 (2016).

    CAS  Article  Google Scholar 

  139. 139

    Goloborodko, A., Imakaev, M. V., Marko, J. F. & Mirny, L. Compaction and segregation of sister chromatids via active loop extrusion. eLife 5, e14864 (2016).

    Article  Google Scholar 

  140. 140

    Naumova, N. et al. Organization of the mitotic chromosome. Science 342, 948–953 (2013).

    CAS  Article  Google Scholar 

  141. 141

    Alipour, E. & Marko, J. F. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 40, 11202–11212 (2012).

    CAS  Article  Google Scholar 

  142. 142

    Bertrand, O. J., Fygenson, D. K. & Saleh, O. A. Active, motor-driven mechanics in a DNA gel. Proc. Natl Acad. Sci. USA 109, 17342–17347 (2012).

    CAS  Article  Google Scholar 

  143. 143

    Smith, K., Griffin, B., Byrd, H., MacKintosh, F. & Kilfoil, M. L. Nonthermal fluctuations of the mitotic spindle. Soft Matter 11, 4396–4401 (2015).

    CAS  Article  Google Scholar 

  144. 144

    Dmitrieff, S., Rao, M. & Sens, P. Quantitative analysis of intra-Golgi transport shows intercisternal exchange for all cargo. Proc. Natl Acad. Sci. USA 110, 15692–15697 (2013).

    CAS  Article  Google Scholar 

  145. 145

    Foret, L. et al. A general theoretical framework to infer endosomal network dynamics from quantitative image analysis. Curr. Biol. 22, 1381–1390 (2012).

    CAS  Article  Google Scholar 

  146. 146

    Ramakrishnan, N., Ipsen, J. H., Rao, M. & Kumar, P. B. S. Organelle morphogenesis by active membrane remodeling. Soft Matter 11, 2387–2393 (2015).

    CAS  Article  Google Scholar 

  147. 147

    Girard, P., Prost, J. & Bassereau, P. Passive or active fluctuations in membranes containing proteins. Phys. Rev. Lett. 94, 088102 (2005).

    CAS  Article  Google Scholar 

  148. 148

    Faris, M. E. A. et al. Membrane tension lowering induced by protein activity. Phys. Rev. Lett. 102, 038102 (2009).

    Article  CAS  Google Scholar 

  149. 149

    Manneville, J.-B., Bassereau, P., Levy, D. & Prost, J. Activity of transmembrane proteins induces magnification of shape fluctuations of lipid membranes. Phys. Rev. Lett. 82, 4356 (1999).

    CAS  Article  Google Scholar 

  150. 150

    Ramaswamy, S. & Rao, M. The physics of active membranes. C. R. Acad. Sci. Ser. IV Phys. Astrophys. 2, 817–839 (2001).

    CAS  Google Scholar 

  151. 151

    He, B., Doubrovinski, K., Polyakov, O. & Wieschaus, E. Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation. Nature 508, 392–396 (2014).

    CAS  Article  Google Scholar 

  152. 152

    Farhadifar, R., Röper, J.-C., Aigouy, B., Eaton, S. & Jülicher, F. The influence of cell mechanics, cell–cell interactions, and proliferation on epithelial packing. Curr. Biol. 17, 2095–2104 (2007).

    CAS  Article  Google Scholar 

  153. 153

    Aigouy, B. et al. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773–786 (2010).

    CAS  Article  Google Scholar 

  154. 154

    Hannezo, E., Prost, J. & Joanny, J.-F. Theory of epithelial sheet morphology in three dimensions. Proc. Natl Acad. Sci. USA 111, 27–32 (2014).

    CAS  Article  Google Scholar 

  155. 155

    Zitterbart, D. P., Wienecke, B., Butler, J. P. & Fabry, B. Coordinated movements prevent jamming in an emperor penguin huddle. PLoS ONE 6, e20260 (2011).

    CAS  Article  Google Scholar 

  156. 156

    Schwarz-Linek, J. et al. Escherichia coli as a model active colloid: a practical introduction. Colloids Surf. B 137, 2–16 (2016).

    CAS  Article  Google Scholar 

  157. 157

    Wu, X.-L. & Libchaber, A. Particle diffusion in a quasi-two-dimensional bacterial bath. Phys. Rev. Lett. 84, 3017–3020 (2000).

    CAS  Article  Google Scholar 

  158. 158

    Wensink, H. H. et al. Meso-scale turbulence in living fluids. Proc. Natl Acad. Sci. USA 109, 14308–14313 (2012).

    CAS  Article  Google Scholar 

  159. 159

    Dunkel, J. et al. Fluid dynamics of bacterial turbulence. Phys. Rev. Lett. 110, 228102 (2013).

    Article  CAS  Google Scholar 

  160. 160

    Wioland, H., Woodhouse, F. G., Dunkel, J. & Goldstein, R. E. Ferromagnetic and antiferromagnetic order in bacterial vortex lattices. Nat. Phys. 12, 341–345 (2016).

    CAS  Article  Google Scholar 

  161. 161

    Paxton, W. F. et al. Catalytic nanomotors: autonomous movement of striped nanorods. J. Am. Chem. Soc. 126, 13424–13431 (2004).

    CAS  Article  Google Scholar 

  162. 162

    Theurkauff, I., Cottin-Bizonne, C., Palacci, J., Ybert, C. & Bocquet, L. Dynamic clustering in active colloidal suspensions with chemical signaling. Phys. Rev. Lett. 108, 268303 (2012).

    CAS  Article  Google Scholar 

  163. 163

    Palacci, J., Sacanna, S., Steinberg, A. P., Pine, D. J. & Chaikin, P. M. Living crystals of light-activated colloidal surfers. Science 339, 936–940 (2013).

    CAS  Article  Google Scholar 

  164. 164

    Buttinoni, I. et al. Dynamical clustering and phase separation in suspensions of self-propelled colloidal particles. Phys. Rev. Lett. 110, 238301 (2013).

    Article  CAS  Google Scholar 

  165. 165

    Wang, W., Chiang, T.-Y., Velegol, D. & Mallouk, T. E. Understanding the efficiency of autonomous nano- and microscale motors. J. Am. Chem. Soc. 135, 10557–10565 (2013).

    CAS  Article  Google Scholar 

  166. 166

    Tirnauer, J. S., Salmon, E. D. & Mitchison, T. J. Microtubule plus-end dynamics in Xenopus egg extract spindles. Mol. Biol. Cell 15, 1776–1784 (2004).

    CAS  Article  Google Scholar 

  167. 167

    Gatlin, J. C. et al. Spindle fusion requires dynein-mediated sliding of oppositely oriented microtubules. Curr. Biol. 19, 287–296 (2009).

    CAS  Article  Google Scholar 

  168. 168

    Mitchison, T. J. et al. Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol. Biol. Cell 16, 3064–3076 (2005).

    CAS  Article  Google Scholar 

  169. 169

    Schaller, V., Weber, C. A., Hammerich, B., Frey, E. & Bausch, A. R. Frozen steady states in active systems. Proc. Natl Acad. Sci. USA 108, 19183–19188 (2011).

    CAS  Article  Google Scholar 

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Acknowledgements

Z.D. acknowledges primary support from Department of Energy Office of Basic Energy Science (Grant No. DE-SC0010432TDD) for supporting research on cytoskeletal active matter. Additional support from John F. Templeton Foundation (Grant Nos 57392 and NSF-MRSEC-1420382) is acknowledged. D.N. acknowledges support from the National Science Foundation (Grant Nos PHY-0847188, PHY-1305254 and DMR-0820484).

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Correspondence to Daniel Needleman or Zvonimir Dogic.

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Needleman, D., Dogic, Z. Active matter at the interface between materials science and cell biology. Nat Rev Mater 2, 17048 (2017). https://doi.org/10.1038/natrevmats.2017.48

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