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  • Open Access

Active mechanics of sea star oocytes

Peter J. Foster1,2,3,*, Alexandra Zampetaki4, Jinghui Liu1,†, Sebastian Fürthauer4,5,‡, and Nikta Fakhri1,§

  • 1Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA
  • 2Department of Physics, Brandeis University, Waltham, Massachusetts 02453, USA
  • 3Department of Physics and Astronomy, Department of Quantitative and Computational Biology, Bridge Institute, Michelson Center for Convergent Bioscience, University of Southern California, Los Angeles, California 90089, USA
  • 4Institute for Applied Physics, TU Wien, A-1040 Wien, Austria
  • 5Center for Computational Biology, Flatiron Institute, New York, New York 10010, USA

  • *Contact author: peterfos@usc.edu
  • †Present address: Max Planck Institute of Molecular Cell Biology and Genetics, SN 01307 Dresden, Germany.
  • ‡Contact author: fuerthauer@iap.tuwien.ac.at
  • §Contact author: fakhri@mit.edu
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Phys. Rev. Research 8, 043103 – Published 29 October, 2026

DOI: https://doi.org/10.1103/k71r-5zgm

Abstract

Cell shape changes, driven by the contractile actomyosin cortex, are essential for multicellular organisms. Yet, how contractility and cell shape changes emerge from molecular-scale interactions between proteins in the actomyosin cortex remains unclear. Oocytes of the bat star Patiria miniata exhibit a traveling wave of cellular deformation during meiosis, known as a surface contraction wave. Here, we exploit this highly stereotypical deformation to study how cortical properties are set by microscale processes. By pharmacologically modulating the levels of polymerized actin, we show that the wild-type composition maximizes the cellular deformation rate. To understand these results, we developed an active fluid model for shape changes that demonstrates that deformation rates are set by the ratio between cortical viscosity and active contractile stresses and provides a framework for deriving these two key material properties from coarse-grained molecular-scale interactions. In this model, the ratio of active stress to viscosity peaks at intermediate admixtures of passive cross-linkers. This explains the observations of the drug treatment experiments and makes additional predictions, namely, that overexpression of either myosin or passive cross-linkers would decrease deformation rates, which we verified experimentally. Together, this shows that the interplay between cortical active stress and viscosity relies on balancing the ratio of myosin to passive cross-linkers on each filament, which can be modulated by actin density. Our results argue that changing the relative molecular compositions of cortical cross-links and motors provides a mechanism that biological systems could exploit for robust and predictable control over both viscosity and active stresses.

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References (71)

  1. S. Banerjee, M. L. Gardel, and U. S. Schwarz, The actin cytoskeleton as an active adaptive material, Annu. Rev. Condens. Matter Phys. 11, 421 (2020).
  2. P. J. Foster, S. Fürthauer, M. J. Shelley, and D. J. Needleman, From cytoskeletal assemblies to living materials, Curr. Opin. Cell Biol. 56, 109 (2019).
  3. M. C. Marchetti, J. F. Joanny, S. Ramaswamy, T. B. Liverpool, J. Prost, M. Rao, and R. A. Simha, Hydrodynamics of soft active matter, Rev. Mod. Phys. 85, 1143 (2013).
  4. D. Needleman and Z. Dogic, Active matter at the interface between materials science and cell biology, Nat. Rev. Mater. 2, 17048 (2017).
  5. M. J. Bowick, N. Fakhri, M. C. Marchetti, and S. Ramaswamy, Symmetry, thermodynamics, and topology in active matter, Phys. Rev. X 12, 010501 (2022).
  6. M. Lenz, Reversal of contractility as a signature of self-organization in cytoskeletal bundles, eLife 9, e51751 (2020).
  7. V. Wollrab, J. M. Belmonte, L. Baldauf, M. Leptin, F. Nédeléc, and G. H. Koenderink, Polarity sorting drives remodeling of actin-myosin networks, J. Cell Sci. 132, jcs219717 (2019).
  8. G. H. Koenderink and E. K. Paluch, Architecture shapes contractility in actomyosin networks, Curr. Opin. Cell Biol. 50, 79 (2018).
  9. P. Chugh, A. G. Clark, M. B. Smith, D. A. D. Cassani, K. Dierkes, A. Ragab, P. P. Roux, G. Charras, G. Salbreux, and E. K. Paluch, Actin cortex architecture regulates cell surface tension, Nat. Cell Biol. 19, 689 (2017).
  10. L. Feld, L. Kellerman, A. Mukherjee, A. Livne, E. Bouchbinder, and H. Wolfenson, Cellular contractile forces are nonmechanosensitive, Sci. Adv. 6, eaaz6997 (2020).
  11. F. Backouche, L. Haviv, D. Groswasser, and A. Bernheim-Groswasser, Active gels: Dynamics of patterning and self-organization, Phys. Biol. 3, 264 (2006).
  12. P. M. Bendix, G. H. Koenderink, D. Cuvelier, Z. Dogic, B. N. Koeleman, W. M. Brieher, C. M. Field, L. Mahadevan, and D. A. Weitz, A quantitative analysis of contractility in active cytoskeletal protein networks, Biophys. J. 94, 3126 (2008).
  13. H. Ennomani, G. Letort, C. Guérin, J.-L. Martiel, W. Cao, F. Nédélec, E. M. De La Cruz, M. Théry, and L. Blanchoin, Architecture and connectivity govern actin network contractility, Curr. Biol. 26, 616 (2016).
  14. T. H. Tan, M. Malik-Garbi, E. Abu-Shah, J. Li, A. Sharma, F. C. MacKintosh, K. Keren, C. F. Schmidt, and N. Fakhri, Self-organized stress patterns drive state transitions in actin cortices, Sci. Adv. 4, eaar2847 (2018).
  15. J. Alvarado, M. Sheinman, A. Sharma, F. C. MacKintosh, and G. H. Koenderink, Molecular motors robustly drive active gels to a critically connected state, Nat. Phys. 9, 591 (2013).
  16. M. P. Murrell and M. L. Gardel, F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex, Proc. Natl. Acad. Sci. USA 109, 20820 (2012).
  17. S. Köhler, K. M. Schmoller, A. H. Crevenna, and A. R. Bausch, Regulating contractility of the actomyosin cytoskeleton by pH, Cell Rep. 2, 433 (2012).
  18. M. Murrell, P. W. Oakes, M. Lenz, and M. L. Gardel, Forcing cells into shape: The mechanics of actomyosin contractility, Nat. Rev. Mol. Cell Biol. 16, 486 (2015).
  19. M. Lenz, Geometrical origins of contractility in disordered actomyosin networks, Phys. Rev. X 4, 041002 (2014).
  20. K. Kruse and F. Jülicher, Actively contracting bundles of polar filaments, Phys. Rev. Lett. 85, 1778 (2000).
  21. P. J. Foster, S. Fürthauer, M. J. Shelley, and D. J. Needleman, Active contraction of microtubule networks, eLife 4, e10837 (2015).
  22. T. Torisawa, D. Taniguchi, S. Ishihara, and K. Oiwa, Spontaneous formation of a globally connected contractile network in a microtubule-motor system, Biophys. J. 111, 373 (2016).
  23. R. Tan, P. J. Foster, D. J. Needleman, and R. J. McKenney, Cooperative accumulation of dynein-dynactin at microtubule minus-ends drives microtubule network reorganization, Dev. Cell 44, 233 (2018).
  24. M. Lenz, T. Thoresen, M. L. Gardel, and A. R. Dinner, Contractile units in disordered actomyosin bundles arise from F-actin buckling, Phys. Rev. Lett. 108, 238107 (2012).
  25. S. Chen, T. Markovich, and F. C. MacKintosh, Motor-free contractility in active gels, Phys. Rev. Lett. 125, 208101 (2020).
  26. S. Chen, T. Markovich, and F. C. MacKintosh, Motor-free contractility of active biopolymer networks, Phys. Rev. E 108, 044405 (2023).
  27. P. Lénárt, C. P. Bacher, N. Daigle, A. R. Hand, R. Eils, M. Terasaki, and J. Ellenberg, A contractile nuclear actin network drives chromosome congression in oocytes, Nature (London) 436, 812 (2005).
  28. P. Bun, S. Dmitrieff, J. M. Belmonte, F. J. Nédélec, and P. Lénárt, A disassembly-driven mechanism explains F-actin-mediated chromosome transport in starfish oocytes, eLife 7, e31469 (2018).
  29. O. Kučera, V. Siahaan, D. Janda, S. H. Dijkstra, E. Pilátová, E. Zatecka, S. Diez, M. Braun, and Z. Lansky, Anillin propels myosin-independent constriction of actin rings, Nat. Commun. 12, 4595 (2021).
  30. W. M. Bement, M. Leda, A. M. Moe, A. M. Kita, M. E. Larson, A. E. Golding, C. Pfeuti, K.-C. Su, A. L. Miller, A. B. Goryachev, and G. von Dassow, Activator–inhibitor coupling between Rho signalling and actin assembly makes the cell cortex an excitable medium, Nat. Cell Biol. 17, 1471 (2015).
  31. J. Bischof, C. A. Brand, K. Somogyi, I. Májer, S. Thome, M. Mori, U. S. Schwarz, and P. Lénárt, A cdk1 gradient guides surface contraction waves in oocytes, Nat. Commun. 8, 849 (2017).
  32. S. Fürthauer, D. J. Needleman, and M. J. Shelley, A design framework for actively crosslinked filament networks, New J. Phys. 23, 013012 (2021).
  33. S. Fürthauer, B. Lemma, P. J. Foster, S. C. Ems-McClung, C.-H. Yu, C. E. Walczak, Z. Dogic, D. J. Needleman, and M. J. Shelley, Self-straining of actively crosslinked microtubule networks, Nat. Phys. 15, 1295 (2019).
  34. 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).
  35. M. C. Wigbers, T. H. Tan, F. Brauns, J. Liu, S. Z. Swartz, E. Frey, and N. Fakhri, A hierarchy of protein patterns robustly decodes cell shape information, Nat. Phys. 17, 578 (2021).
  36. K. Hara, Cinematographic observation of “surface contraction waves” (SCW) during the early cleavage of axolotl eggs, Wilhelm Roux Arch. Entwickl. Mech. Org. 167, 183 (1971).
  37. N. Satoh, ‘Metachronous’ cleavage and initiation of gastrulation in amphibian embryos, Dev. Growth Differ. 19, 111 (1977).
  38. C. A. Lewis, Ultrastructure of a fertilized barnacle egg (Pollicipes polymerus) with peristaltic constrictions, Wilhelm Roux Arch. Entwickl. Mech. Org. 181, 333 (1977).
  39. C. Sardet, J. Speksnijder, S. Inoue, and L. Jaffe, Fertilization and ooplasmic movements in the ascidian egg, Development 105, 237 (1989).
  40. J. Liu, T. Burkart, A. Ziepke, J. Reinhard, Y.-C. Chao, T. H. Tan, S. Z. Swartz, E. Frey, and N. Fakhri, Light-induced cortical excitability reveals programmable shape dynamics in starfish oocytes, Nat. Phys. 21, 846 (2025).
  41. S. Narumiya, M. Tanji, and T. Ishizaki, Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion, Cancer Metastasis Rev. 28, 65 (2009).
  42. See Supplemental Material at http://link.aps.org/supplemental/10.1103/k71r-5zgm for materials and methods, details on the active surface deformation model, active fluid model, Bayesian parameter inference, supplemental figures, and supplementary videos, which includes Refs. [31, 32, 33, 34, 44, 46, 47, 48, 49, 50, 51, 56, 57, 58, 64, 65, 66, 67, 68, 69, 70].
  43. M. R. Bubb, A. M. Senderowicz, E. A. Sausville, K. L. Duncan, and E. D. Korn, Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin, J. Biol. Chem. 269, 14869 (1994).
  44. M. Mori, K. Somogyi, H. Kondo, N. Monnier, H. J. Falk, P. Machado, M. Bathe, F. Nédélec, and P. Lénárt, An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes, Curr. Biol. 24, 1421 (2014).
  45. N. Wesolowska, I. Avilov, P. Machado, C. Geiss, H. Kondo, M. Mori, and P. Lenart, Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes, eLife 9, e49774 (2020).
  46. A. Mietke, F. Jülicher, and I. F. Sbalzarini, Self-organized shape dynamics of active surfaces, Proc. Natl. Acad. Sci. USA 116, 29 (2019).
  47. C. Bächer, D. Khoromskaia, G. Salbreux, and S. Gekle, A three-dimensional numerical model of an active cell cortex in the viscous limit, Front. Phys. 9, 753230 (2021).
  48. H. Borja da Rocha, J. Bleyer, and H. Turlier, A viscous active shell theory of the cell cortex, J. Mech. Phys. Solids 164, 104876 (2022).
  49. L. D. Wittwer and S. Aland, A computational model of self-organized shape dynamics of active surfaces in fluids, J. Comput. Phys.: X 17, 100126 (2023).
  50. M. Fritzsche, A. Lewalle, T. Duke, K. Kruse, and G. Charras, Analysis of turnover dynamics of the submembranous actin cortex, Mol. Biol. Cell 24, 757 (2013).
  51. D. S. Banerjee, A. Munjal, T. Lecuit, and M. Rao, Actomyosin pulsation and flows in an active elastomer with turnover and network remodeling, Nat. Commun. 8, 1121 (2017).
  52. O. Esue, E. S. Harris, H. N. Higgs, and D. Wirtz, The filamentous actin cross-linking/bundling activity of mammalian formins, J. Mol. Biol. 384, 324 (2008).
  53. J. Roostalu, J. Rickman, C. Thomas, F. Nédélec, and T. Surrey, Determinants of polar versus nematic organization in networks of dynamic microtubules and mitotic motors, Cell 175, 796 (2018).
  54. P. Chugh and E. K. Paluch, The actin cortex at a glance, J. Cell Sci. 131, jcs186254 (2018).
  55. T. H. Tan, G. A. Watson, Y.-C. Chao, J. Li, T. R. Gingrich, N. Horowitz, and J. M Fakhri, Scale-dependent irreversibility in living matter, arXiv:2107.05701.
  56. T. Hiraiwa and G. Salbreux, Role of turnover in active stress generation in a filament network, Phys. Rev. Lett. 116, 188101 (2016).
  57. C. Barutel and S. Fürthauer, Entropic, active, and frictional forces in cytoskeletal crosslinking, Phys. Rev. Res. 8, 033122 (2026).
  58. R. Sakamoto, Z. G. Sun, and M. P. Murrell, Crosslinked F-actin networks regulate load-dependent energy conversion, Commun. Biol. 9, 572 (2026).
  59. L. W. Janson, J. Kolega, and D. L. Taylor, Modulation of contraction by gelation/solation in a reconstituted motile model, J. Cell Biol. 114, 1005 (1991).
  60. M. Murrell and M. L. Gardel, Actomyosin sliding is attenuated in contractile biomimetic cortices, Mol. Biol. Cell 25, 1845 (2014).
  61. J. M. Belmonte, M. Leptin, and F. Nédélec, A theory that predicts behaviors of disordered cytoskeletal networks, Mol. Syst. Biol. 13, MSB177796 (2017).
  62. M. L. Gardel, J. H. Shin, F. C. MacKintosh, L. Mahadevan, P. Matsudaira, and D. A. Weitz, Elastic behavior of cross-linked and bundled actin networks, Science 304, 1301 (2004).
  63. X. Yang, M. Heinemann, J. Howard, G. Huber, S. Iyer-Biswas, G. Le Treut, M. Lynch, K. L. Montooth, D. J. Needleman, S. Pigolotti, J. Rodenfels, P. Ronceray, S. Shankar, I. Tavassoly, S. Thutupalli, D. V. Titov, J. Wang, and P. J. Foster, Physical bioenergetics: Energy fluxes, budgets, and constraints in cells, Proc. Natl. Acad. Sci. USA 118, e2026786118 (2021).
  64. T. H. Tan, J. Liu, P. W. Miller, M. Tekant, J. Dunkel, and N. Fakhri, Topological turbulence in the membrane of a living cell, Nat. Phys. 16, 657 (2020).
  65. A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, Advanced methods of microscope control using µManager software, JBM 1, 1 (2014).
  66. 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).
  67. T. Y. Hou, J. S. Lowengrub, and M. J. Shelley, Removing the stiffness from interfacial flows with surface tension, J. Comput. Phys. 114, 312 (1994).
  68. S. Banerjee and M. C. Marchetti, Instabilities and oscillations in isotropic active gels, Soft Matter 7, 463 (2011).
  69. J. Clarke, F. Cavanna, A. Marne, A. Davolio, and J. Alvarado, Nonlinear contractile response of actomyosin active gels to control signals, Phys. Rev. Res. 7, 043181 (2025).
  70. A. Gelman, B. Goodrich, J. Gabry, and A. Vehtari, R-squared for Bayesian regression models, Am. Stat. 73, 307 (2019).
  71. https://github.com/foster61012/Starfish_SCW.

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Phys. Rev. Research 8, 043103– Published 29 October, 2026
  • Received 10 April 2026
  • Accepted 24 September 2026
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