Rigidity of Epithelial Tissues as a Double Optimization Problem (2312.11683v5)
Abstract: How do cells tune emergent properties at the scale of tissues? One class of such emergent behaviors are rigidity transitions, in which a tissue changes from a solid-like to a fluid-like state or vice versa. Here, we introduce a new way for a tissue described by a vertex model to tune its rigidity, by using ``tunable degrees of freedom." We use the vertex model elastic energy as a cost function and the cell stiffnesses, target shapes, and target areas as different sets of degrees of freedom describing cell-cell interactions that can be tuned to minimize the cost function. We show that the rigidity transition is unaffected when cell stiffnesses are treated as tunable degrees of freedom. When preferred shapes or areas are treated as tunable degrees of freedom, however, induced spatial correlations in target cell shapes or areas shift the rigidity transition. These observations suggest that tissues can coordinate changes in cell-scale properties, treated here as tunable degrees of freedom, to achieve desired tissue-scale behaviors.
- Designing allostery-inspired response in mechanical networks. Proceedings of the National Academy of Sciences, 114(10):2520–2525, March 2017. Publisher: Proceedings of the National Academy of Sciences.
- The Principle of Independent Bond-Level Response: Tuning by Pruning to Exploit Disorder for Global Behavior. Physical Review Letters, 114(22):225501, June 2015. Publisher: American Physical Society.
- Role of local response in manipulating the elastic properties of disordered solids by bond removal. Soft Matter, 14(2):312–318, 2018.
- Linking microscopic and macroscopic response in disordered solids. Physical Review E, 97(6):063001, June 2018.
- Limits of multifunctionality in tunable networks. Proceedings of the National Academy of Sciences, 116(7):2506–2511, February 2019. Publisher: Proceedings of the National Academy of Sciences.
- Learning Without Neurons in Physical Systems. Annual Review of Condensed Matter Physics, 14(1):417–441, 2023. _eprint: https://doi.org/10.1146/annurev-conmatphys-040821-113439.
- Directed aging, memory, and nature’s greed. Science Advances, 5(12):eaax4215, December 2019. Publisher: American Association for the Advancement of Science.
- Effect of directed aging on nonlinear elasticity and memory formation in a material. Physical Review Research, 2(4):043231, November 2020. Publisher: American Physical Society.
- Periodic training of creeping solids. Proceedings of the National Academy of Sciences, 117(50):31690–31695, December 2020. Publisher: Proceedings of the National Academy of Sciences.
- Equilibrium Propagation: Bridging the Gap between Energy-Based Models and Backpropagation. Frontiers in Computational Neuroscience, 11, 2017.
- Supervised Learning in Physical Networks: From Machine Learning to Learning Machines. Physical Review X, 11(2):021045, May 2021. Publisher: American Physical Society.
- Demonstration of Decentralized Physics-Driven Learning. Physical Review Applied, 18(1):014040, July 2022. Publisher: American Physical Society.
- Desynchronous learning in a physics-driven learning network. The Journal of Chemical Physics, 156(14):144903, April 2022.
- Machine Learning Without a Processor: Emergent Learning in a Nonlinear Electronic Metamaterial, November 2023. arXiv:2311.00537 [cond-mat].
- On the mechanism of wing size determination in fly development. Proceedings of the National Academy of Sciences, 104(10):3835–3840, March 2007. Publisher: Proceedings of the National Academy of Sciences.
- The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing. Current Biology, 17(24):2095–2104, December 2007.
- Unjamming and cell shape in the asthmatic airway epithelium. Nature Materials, 14(10):1040–1048, October 2015. Number: 10 Publisher: Nature Publishing Group.
- A density-independent rigidity transition in biological tissues. Nature Physics, 11(12):1074–1079, December 2015. Number: 12 Publisher: Nature Publishing Group.
- Motility-Driven Glass and Jamming Transitions in Biological Tissues. Physical Review X, 6(2):021011, April 2016. Publisher: American Physical Society.
- M. Chiang and D. Marenduzzo. Glass transitions in the cellular Potts model. Europhysics Letters, 116(2):28009, December 2016. Publisher: EDP Sciences, IOP Publishing and Società Italiana di Fisica.
- A fluid-to-solid jamming transition underlies vertebrate body axis elongation. Nature, 561(7723):401–405, September 2018.
- Anisotropy links cell shapes to tissue flow during convergent extension. Proceedings of the National Academy of Sciences, 117(24):13541–13551, June 2020. Publisher: National Academy of Sciences Section: Biological Sciences.
- A Geometric Tension Dynamics Model of Epithelial Convergent Extension, November 2023. arXiv:2311.16384 [cond-mat, physics:physics, q-bio].
- Tissue Flow Induces Cell Shape Changes During Organogenesis. Biophysical Journal, 115(11):2259–2270, December 2018.
- 3D viscoelastic drag forces contribute to cell shape changes during organogenesis in the zebrafish embryo. Cells & Development, 168:203718, December 2021.
- Minimal vertex model explains how the amnioserosa avoids fluidization during Drosophila dorsal closure, December 2023. bioRxiv: Pages: 2023.12.20.572544 Section: New Results.
- Hisao Honda. Description of cellular patterns by Dirichlet domains: The two-dimensional case. Journal of Theoretical Biology, 72(3):523–543, June 1978.
- Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion. Physical Review Letters, 123(5):058101, July 2019.
- Daniel M. Sussman. cellGPU: Massively parallel simulations of dynamic vertex models. Computer Physics Communications, 219:400–406, October 2017.
- Structural Relaxation Made Simple. Physical Review Letters, 97(17):170201, October 2006.
- Transient learning degrees of freedom for introducing function in materials. Proceedings of the National Academy of Sciences, 119(19):e2117622119, May 2022. Publisher: Proceedings of the National Academy of Sciences.
- A minimal-length approach unifies rigidity in underconstrained materials. Proceedings of the National Academy of Sciences, 116(14):6560–6568, April 2019.
- A geometrically controlled rigidity transition in a model for confluent 3D tissues. New Journal of Physics, 20(2):022002, February 2018.
- Energetic rigidity. I. A unifying theory of mechanical stability. Physical Review E, 105(2):025003, February 2022.
- Bond-orientational order in liquids and glasses. Physical Review B, 28(2):784, 1983.
- Correlating cell shape and cellular stress in motile confluent tissues. Proceedings of the National Academy of Sciences, 114(48):12663–12668, November 2017. Publisher: National Academy of Sciences Section: Physical Sciences.
- Confluent and nonconfluent phases in a model of cell tissue. Physical Review E, 98(4):042418, October 2018. Publisher: American Physical Society.
- B. Pisanty. (private communication, 2023).
- Small-scale demixing in confluent biological tissues. Soft Matter, 16(13):3325–3337, 2020. Publisher: Royal Society of Chemistry.
- Mechanosensitive Junction Remodeling Promotes Robust Epithelial Morphogenesis. Biophysical Journal, 117(9):1739–1750, November 2019.
- Active tension network model suggests an exotic mechanical state realized in epithelial tissues. Nature Physics, 13(12):1221–1226, December 2017.