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  • Letter
  • Open Access

Building rigid networks with prestress and selective pruning

Marco A. Galvani Cunha1,*, John C. Crocker2, and Andrea J. Liu1,3

  • 1Department of Physics & Astronomy, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA
  • 2Department of Chemical and Biomolecular Engineering, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA
  • 3Santa Fe Institute, Santa Fe, New Mexico 87501, USA

  • *Contact author: mgalvani@sas.upenn.edu

Phys. Rev. Research 6, L042020 – Published 22 October, 2024

DOI: https://doi.org/10.1103/PhysRevResearch.6.L042020

Abstract

Biopolymer networks from the intracellular to tissue scale display high rigidity and tensile stress while having coordinations well below the normal threshold for mechanical rigidity. The elastic filaments in these networks are often severed by enzymes in a tension-inhibited manner. The effects of such pruning on the mechanics of prestressed networks have not been studied. We show that networks pruned by a tension-inhibited method remain rigid at much lower coordinations than randomly pruned ones. These findings suggest a possible reason for the repeated evolution of tension-inhibited filament-severing proteins.

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References (46)

  1. J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, Fibroblast adaptation and stiffness matching to soft elastic substrates, Biophys. J. 93, 4453 (2007).
  2. D. Mizuno, C. Tardin, C. F. Schmidt, and F. C. MacKintosh, Nonequilibrium mechanics of active cytoskeletal networks, Science 315, 370 (2007).
  3. B. D. Hoffman and J. C. Crocker, Cell mechanics: Dissecting the physical responses of cells to force, Annu. Rev. Biomed. Eng. 11, 259 (2009).
  4. S.-Y. Tee, J. Fu, C. S. Chen, and P. A. Janmey, Cell shape and substrate rigidity both regulate cell stiffness, Biophys. J. 100, L25 (2011).
  5. R. Vargas-Pinto, H. Gong, A. Vahabikashi, and M. Johnson, The effect of the endothelial cell cortex on atomic force microscopy measurements, Biophys. J. 105, 300 (2013).
  6. A. Rigato, A. Miyagi, S. Scheuring, and F. Rico, High-frequency microrheology reveals cytoskeleton dynamics in living cells, Nat. Phys. 13, 771 (2017).
  7. S. Arzash, J. L. Shivers, and F. C. MacKintosh, Shear-induced phase transition and critical exponents in three-dimensional fiber networks, Phys. Rev. E 104, L022402 (2021).
  8. S. Arzash, J. L. Shivers, and F. C. MacKintosh, Finite size effects in critical fiber networks, Soft Matter 16, 6784 (2020).
  9. A. Sharma, A. J. Licup, K. A. Jansen, R. Rens, M. Sheinman, G. H. Koenderink, and F. C. MacKintosh, Strain-controlled criticality governs the nonlinear mechanics of fibre networks, Nat. Phys. 12, 584 (2016).
  10. A. J. Licup, S. Münster, A. Sharma, M. Sheinman, L. M. Jawerth, B. Fabry, D. A. Weitz, and F. C. MacKintosh, Stress controls the mechanics of collagen networks, Proc. Natl. Acad. Sci. USA 112, 9573 (2015).
  11. A. Bose, M. F. J. Vermeulen, C. Storm, and W. G. Ellenbroek, Self-stresses control stiffness and stability in overconstrained disordered networks, Phys. Rev. E 99, 023001 (2019).
  12. S. Alexander, Amorphous solids: Their structure, lattice dynamics and elasticity, Phys. Rep. 296, 65 (1998).
  13. O. K. Damavandi, V. F. Hagh, C. D. Santangelo, and M. L. Manning, Energetic rigidity. I. A unifying theory of mechanical stability, Phys. Rev. E 105, 025003 (2022).
  14. O. K. Damavandi, V. F. Hagh, C. D. Santangelo, and M. L. Manning, Energetic rigidity. II. Applications in examples of biological and underconstrained materials, Phys. Rev. E 105, 025004 (2022).
  15. M. Merkel, K. Baumgarten, B. P. Tighe, and M. L. Manning, A minimal-length approach unifies rigidity in underconstrained materials, Proc. Natl. Acad. Sci. USA 116, 6560 (2019).
  16. B. Cui, G. Ruocco, and A. Zaccone, Theory of elastic constants of athermal amorphous solids with internal stresses, Granular Matter 21, 69 (2019).
  17. 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).
  18. S. Mukhina, Y.-L. Wang, and M. Murata-Hori, α-actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis, Develop. Cell 13, 554 (2007).
  19. C. A. Wilson, M. A. Tsuchida, G. M. Allen, E. L. Barnhart, K. T. Applegate, P. T. Yam, L. Ji, K. Keren, G. Danuser, and J. A. Theriot, Myosin II contributes to cell-scale actin network treadmilling through network disassembly, Nature (London) 465, 373 (2010).
  20. P. M. McCall, F. C. MacKintosh, D. R. Kovar, and M. L. Gardel, Cofilin drives rapid turnover and fluidization of entangled F-actin, Proc. Natl. Acad. Sci. USA 116, 12629 (2019).
  21. V. E. Galkin, A. Orlova, and E. H. Egelman, Actin filaments as tension sensors, Curr. Biol. 22, R96 (2012).
  22. D. Pavlov, A. Muhlrad, J. Cooper, M. Wear, and E. Reisler, Actin filament severing by cofilin, J. Mol. Biol. 365, 1350 (2007).
  23. A. C. Schramm, G. M. Hocky, G. A. Voth, L. Blanchoin, J.-L. Martiel, and E. M. De La Cruz, Actin filament strain promotes severing and cofilin dissociation, Biophys. J. 112, 2624 (2017).
  24. K. Hayakawa, H. Tatsumi, and M. Sokabe, Actin filaments function as a tension sensor by tension-dependent binding of cofilin to the filament, J. Cell Biol. 195, 721 (2011).
  25. Y. Nabeshima, E. S. Grood, A. Sakurai, and J. H. Herman, Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro, J. Orthop. Res. 14, 123 (1996).
  26. E. Yi, S. Sato, A. Takahashi, H. Parameswaran, T. A. Blute, E. Bartolák-Suki, and B. Suki, Mechanical forces accelerate collagen digestion by bacterial collagenase in lung tissue strips, Front. Physiol. 7, 287 (2016).
  27. K. Saini, S. Cho, L. J. Dooling, and D. E. Discher, Tension in fibrils suppresses their enzymatic degradation–a molecular mechanism for ‘use it or lose it’, Matrix Biol. 85–86, 34 (2020).
  28. S. J. Cone, A. T. Fuquay, J. M. Litofsky, T. C. Dement, C. A. Carolan, and N. E. Hudson, Inherent fibrin fiber tension propels mechanisms of network clearance during fibrinolysis, Acta Biomater. 107, 164 (2020).
  29. M. Stern and A. Murugan, Learning without neurons in physical systems, Annu. Rev. Condens. Matter Phys. 14, 417 (2023).
  30. J. Guénolé, W. G. Nöhring, A. Vaid, F. Houllé, Z. Xie, A. Prakash, and E. Bitzek, Assessment and optimization of the fast inertial relaxation engine (fire) for energy minimization in atomistic simulations and its implementation in lammps, Comput. Mater. Sci. 175, 109584 (2020).
  31. C. P. Goodrich, A. J. Liu, and S. R. Nagel, The principle of independent bond-level response: tuning by pruning to exploit disorder for global behavior, Phys. Rev. Lett. 114, 225501 (2015).
  32. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevResearch.6.L042020 for details on the calculation of the bond-level contributions to the elastic moduli based on linear response.
  33. D. Hexner, A. J. Liu, and S. R. Nagel, Linking microscopic and macroscopic response in disordered solids, Phys. Rev. E 97, 063001 (2018).
  34. D. Hexner, A. J. Liu, and S. R. Nagel, Role of local response in manipulating the elastic properties of disordered solids by bond removal, Soft Matter 14, 312 (2018).
  35. S. Arzash, J. L. Shivers, A. J. Licup, A. Sharma, and F. C. MacKintosh, Stress-stabilized subisostatic fiber networks in a ropelike limit, Phys. Rev. E 99, 042412 (2019).
  36. S. Arzash, A. Sharma, and F. C. MacKintosh, Mechanics of fiber networks under a bulk strain, Phys. Rev. E 106, L062403 (2022).
  37. M. Sheinman, C. P. Broedersz, and F. C. MacKintosh, Actively stressed marginal networks, Phys. Rev. Lett. 109, 238101 (2012).
  38. M. Baity-Jesi, C. P. Goodrich, A. J. Liu, S. R. Nagel, and J. P. Sethna, Emergent SO(3) symmetry of the frictionless shear jamming transition, J. Stat. Phys. 167, 735 (2017).
  39. Y. Mulla, M. J. Avellaneda, A. Roland, L. Baldauf, W. Jung, T. Kim, S. J. Tans, and G. H. Koenderink, Weak catch bonds make strong networks, Nat. Mater. 21, 1019 (2022).
  40. H. Kojima, A. Ishijima, and T. Yanagida, Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation, Proc. Natl. Acad. Sci. USA 91, 12962 (1994).
  41. X. Liu and G. H. Pollack, Mechanics of F-actin characterized with microfabricated cantilevers, Biophys. J. 83, 2705 (2002).
  42. S. Matsushita, T. Adachi, Y. Inoue, M. Hojo, and M. Sokabe, Evaluation of extensional and torsional stiffness of single actin filaments by molecular dynamics analysis, J. Biomech. 43, 3162 (2010).
  43. Y.-S. Kee and D. N. Robinson, Micropipette aspiration for studying cellular mechanosensory responses and mechanics, in Dictyostelium Discoideum Protocols, edited by L. Eichinger and F. Rivero, Methods in Molecular Biology Vol. 983 (Humana Press, Totowa, NJ, 2013), pp 367–382.
  44. A. X. Cartagena-Rivera, J. S. Logue, C. M. Waterman, and R. S. Chadwick, Actomyosin cortical mechanical properties in nonadherent cells determined by atomic force microscopy, Biophys. J. 110, 2528 (2016).
  45. Y. Tsuda, H. Yasutake, A. Ishijima, and T. Yanagida, Torsional rigidity of single actin filaments and actin–actin bond breaking force under torsion measured directly by in vitro micromanipulation, Proc. Natl. Acad. Sci. USA 93, 12937 (1996).
  46. S. Sivarajan, Y. Shi, K. M. Xiang, C. Rodríguez-Cruz, C. L. Porter, G. M. Kostecki, L. Tung, J. C. Crocker, and D. H. Reich, Lévy distributed fluctuations in the living cell cortex, arXiv:2309.06226.

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