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  • Open Access

Morphological parameters capture emergent properties of dynamic disordered cytoskeletal networks

Soumik Ghosh1, Lilianna Houston2, Alejandra Vasquez1, Kingshuk Ghosh2, and Ashok Prasad1,*

  • *Contact author: ashok.prasad@colostate.edu
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APS Open Sci. 1, 000144 – Published 21 September, 2026

DOI: https://doi.org/10.1103/b8cz-s9ld

Abstract

The actin cytoskeleton is an inherently disordered active system. The actomyosin cortex and reconstituted actomyosin systems are globally disordered, yet undergo transitions between distinct disordered states as parameters like motor and crosslinker concentration and filament length and rigidity change. In cells, these changes are related to genetic mutations or differences in cell state and dictate fundamental biological processes. However, we do not have well-established methods to detect and classify differences in disordered polymer networks. Image-based morphology techniques provide a noninvasive, high-throughput method of extracting information about a system. In this work, we simulate biopolymer networks under varying conditions and develop and use morphological descriptors to construct trajectories in morphospace. Using statistical analysis, we find that morphological descriptors are able to distinguish between different trajectories of the system, including differences not apparent to the eye. However, no single descriptor alone is able to capture all the differences in the simulated trajectories. Nematic order parameters typically perform the worst for our simulations, while curvature and texture descriptors can collectively distinguish between dynamic trajectories. This work helps develop quantification of cytoskeleton dynamics for classification and data-driven modeling.

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References (50)

  1. M. Bornens, Organelle positioning and cell polarity, Nat. Rev. Mol. Cell Biol. 9, 874 (2008).
  2. L. Chang and R. D. Goldman, Intermediate filaments mediate cytoskeletal crosstalk, Nat. Rev. Mol. Cell Biol. 5, 601 (2004).
  3. R. Sanghvi-Shah and G. F. Weber, Intermediate filaments at the junction of mechanotransduction, migration, and development, Front. Cell Dev. Biol. 5, 81 (2017).
  4. J. Kroll and J. Renkawitz, Principles of organelle positioning in motile and non-motile cells, EMBO Rep. 25, 2172 (2024).
  5. D. A. Fletcher and R. D. Mullins, Cell mechanics and the cytoskeleton, Nature (London) 463, 485 (2010).
  6. B. Geinger, J. P. Spatz, and A. D. Bershadsky, Environment sensing through focal adhesions, Nat. Rev. Mol. Cell Biol. 10, 21 (2009).
  7. C. S. Janota, F. J. Calero-Cuenca, and E. R. Gomes, The role of the cell nucleus in mechanotransduction, Curr. Opin. Cell Biol. 63, 204 (2020).
  8. A. B. Ndiaye, G. H. Koenderink, and M. Shemesh, Intermediate filaments in cellular mechanoresponsiveness: Mediating cytoskeletal crosstalk from membrane to nucleus and back, Front. Cell Dev. Biol. 10, 882037 (2022).
  9. D. E. Discher, D. J. Mooney, and P. W. Zandstra, Growth factors, matrices, and forces combine and control stem cells, Science 324, 1673 (2009).
  10. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, and S. Piccolo, Role of YAP/TAZ in mechanotransduction, Nature (London) 474, 179 (2011).
  11. A. Elosegui-Artola, I. Andreu, A. E. M. Beedle, A. Lezamiz, M. Uroz, A. J. Kosmalska, R. Oria, J. Z. Kechagia, P. Rico-Lastres, A. L. Le Roux, C. M. Shanahan, X. Trepat, D. Navajas, S. Garcia-Manyes, and P. Roca-Cusachs, Force triggers YAP nuclear entry by regulating transport across nuclear pores, Cell 171, 1397 (2017).
  12. D. E. Jaalouk and J. Lammerding, Mechanotransduction gone awry, Nat. Rev. Mol. Cell Biol. 10, 63 (2009).
  13. M. H. Kim, J. Kim, H. Hong, S. H. Lee, J. K. Lee, E. Jung, and J. Kim, Actin remodeling confers BRAF inhibitor resistance to melanoma cells through YAP/TAZ activation, EMBO J. 35, 462 (2016).
  14. O. H. Akenuwa, J. Gu, A. Nebenführ, and S. M. Abel, Morphometric analysis of actin networks, Mol. Biol. Cell 35, ar146 (2024).
  15. S. Alderfer, J. Sun, L. Tahtamouni, and A. Prasad, Morphological signatures of actin organization in single cells accurately classify genetic perturbations using CNNs with transfer learning, Soft Matter 18, 8342 (2022).
  16. T. Andersen, D. Worthmuller, D. Probst, I. Wang, P. Moreau, V. Fitzpatrick, T. Boudou, U. S. Schwarz, and M. Balland, Cell size and actin architecture determine force generation in optogenetically activated cells, Biophys. J. 122, 684 (2023).
  17. N. S. Bryce, T. W. Failes, J. R. Stehn, K. Baker, S. Zahler, Y. Arzhaeva, L. Bischof, C. Lyons, I. Dedova, G. M. Arndt, K. Gaus, B. T. Goult, E. C. Hardeman, P. W. Gunning, and J. G. Lock, High-content imaging of unbiased chemical perturbations reveals that the phenotypic plasticity of the actin cytoskeleton is constrained, Cell Syst. 9, 496 (2019).
  18. W. H. Chou, M. Molaei, H. Wu, P. W. Oakes, J. R. Beach, and M. L. Gardel, Limiting pool and actin architecture controls myosin cluster sizes in adherent cells, Biophys. J. 123, 157 (2024).
  19. R. S. Kadzik, K. E. Homa, and D. R. Kovar, F-actin cytoskeleton network self-organization through competition and cooperation, Annu. Rev. Cell Dev. Biol. 36, 35 (2020).
  20. M. Y. Mollica, K. M. Beussman, A. Kandasamy, L. M. Rodriguez, F. R. Morales, J. Chen, K. Manohar, J. C. Del Alamo, J. A. Lopez, W. E. Thomas, and N. J. Sniadecki, Distinct platelet F-actin patterns and traction forces on von Willebrand factor versus fibrinogen, Biophys. J. 122, 3738 (2023).
  21. R. Sakamoto and M. P. Murrell, Composite branched and linear F-actin maximize myosin-induced membrane shape changes in a biomimetic cell model, Commun. Biol. 7, 840 (2024).
  22. R. Sakamoto and M. P. Murrell, F-actin architecture determines the conversion of chemical energy into mechanical work, Nat. Commun. 15, 3444 (2024).
  23. R. Sakamoto and M. P. Murrell, Mechanical power is maximized during contractile ring-like formation in a biomimetic dividing cell model, Nat. Commun. 15, 9731 (2024).
  24. K. Schakenraad, J. Ernst, W. Pomp, E. H. J. Danen, R. M. H. Merks, T. Schmidt, and L. Giomi, Mechanical interplay between cell shape and actin cytoskeleton organization, Soft Matter 16, 6328 (2020).
  25. J. Gao and F. Nakamura, Actin-associated proteins and small molecules targeting the actin cytoskeleton, Int. J. Mol. Sci. 23, 2118 (2022).
  26. Y. Aratyn-Schaus, P. W. Oakes, and M. L. Gardel, Dynamic and structural signatures of lamellar actomyosin force generation, Mol. Biol. Cell 22, 1330 (2011).
  27. N. A. McDonald, A. L. Lind, S. E. Smith, R. Li, and K. L. Gould, Nanoscale architecture of the Schizosaccharomyces pombe contractile ring, eLife 6, e28865 (2017).
  28. 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).
  29. C. P. Brangwynne, F. C. MacKintosh, S. Kumar, N. A. Geisse, J. Talbot, L. Mahadevan, K. K. Parker, D. E. Ingber, and D. A. Weitz, Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement, J. Cell Biol. 173, 733 (2006).
  30. S. H. Shabbir, M. M. Cleland, R. D. Goldman, and M. Mrksich, Geometric control of vimentin intermediate filaments, Biomaterials 35, 1359 (2014).
  31. E. Terriac, S. Schutz, and F. Lautenschlager, Vimentin intermediate filament rings deform the nucleus during the first steps of adhesion, Front. Cell Dev. Biol. 7, 106 (2019).
  32. C. Schwayer, M. Sikora, J. Slovakova, R. Kardos, and C. P. Heisenberg, Actin rings of power, Dev. Cell 37, 493 (2016).
  33. M. J. Reynolds, C. Hachicho, A. G. Carl, R. Gong, and G. M. Alushin, Bending forces and nucleotide state jointly regulate F-actin structure, Nature (London) 611, 380 (2022).
  34. M. Nakamura, J. Hui, and S. M. Parkhurst, Bending actin filaments: Twists of fate, Fac. Rev. 12, 7 (2023).
  35. R. M. Haralick, K. Shanmugam, and Its’Hak Dinstein, Textural features for image classification, IEEE Trans. Syst. Man Cybern. SMC-3, 610 (1973).
  36. E. Alizadeh, J. Castle, A. Quirk, C. D. L. Taylor, W. Xu, and A. Prasad, Cellular morphological features are predictive markers of cancer cell state, Comput. Biol. Med. 126, 104044 (2020).
  37. J. Hui, R. Nakamura, J. Dubrulle, and S. M. Parkhurst, Coordinated efforts of different actin filament populations are needed for optimal cell wound repair, Mol. Biol. Cell 34, ar15 (2023).
  38. W. Liu, E. Ralston, N. Raben, and E. Ralston, A new directionality tool for assessing microtubule pattern alterations, J. Biomed. Opt. 19, 056001 (2014).
  39. D. Borin et al., Altered microtubule structure, hemichannel localization and beating activity in cardiomyocytes expressing pathologic nuclear lamin A/C, Heliyon 6, e03175 (2020).
  40. Y. Wang et al., Live-cell imaging and analysis reveal cell phenotypic transition dynamics inherently missing in snapshot data, Sci. Adv. 6, eaba9319 (2020).
  41. Q. Chen, A. Sriram, A. Das, K. Matic, M. Hendija, K. Tonry, J. L. Ross, M. Das, R. J. McGorty, R. M. Robertson-Anderson, and M. T. Valentine, BARCODE: High throughput screening and analysis of soft active materials, Nat. Commun. 17, 1192 (2025).
  42. F. Nédélec and D. Foethke, Collective Langevin dynamics of flexible cytoskeletal fibers, New J. Phys. 9, 427 (2007).
  43. J. M. Belmonte, M. Leptin, and F. Nédélec, A theory that predicts behaviors of disordered cytoskeletal networks, Mol. Syst. Biol. 13, MSB177796 (2017).
  44. V. Wollrab, J. M. Belmonte, L. Baldauf, M. Leptin, F. Nédélec, and G. H. Koenderink, Polarity sorting drives remodeling of actin–myosin networks, J. Cell Sci. 132, jcs219717 (2019).
  45. L. Hauke, A. Primeßnig, B. Eltzner, J. Radwitz, S. F. Huckemann, and F. Rehfeldt, FilamentSensor 2.0: An open-source modular toolbox for 2D/3D cytoskeletal filament tracking, PLoS ONE 18, e0279336 (2023).
  46. S. L. Madison, M. L. Buchanan, J. D. Glass, T. F. McClain, E. Park, and A. Nebenführ, Class XI myosins move specific organelles in pollen tubes and are required for normal fertility and pollen tube growth in Arabidopsis, Plant Physiol. 169, 1946 (2015).
  47. H. Ueda, E. Yokota, N. Kutsuna, T. Shimada, K. Tamura, T. Shimmen, S. Hasezawa, V. V. Dolja, and I. Hara-Nishimura, Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells, Proc. Natl. Acad. Sci. USA 107, 6894 (2010).
  48. See Supplemental Material at http://link.aps.org/supplemental/10.1103/b8cz-s9ld for additional figures.
  49. https://github.com/prasadlabcsu/CytoskeletonMorphology/releases/tag/paper-ghosh2026.
  50. S. Ghosh, L. Houston, A. Vasquez, K. Ghosh, and A. Prasad, CytoskeletonMorphology: Code associated with “Morphological parameters capture emergent properties of dynamic disordered cytoskeletal networks” [Computer software], Zenodo, 2026, https://doi.org/10.5281/zenodo.22770374.

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APS Open Sci. 1, 000144– Published 21 September, 2026
Vol. 1
  • Received 27 May 2026
  • Revised 26 August 2026
  • Accepted 2 September 2026
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Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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