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Cells exploit a phase transition to establish interconnections in fibrous extracellular matrices

Grekas, Georgios and Proestaki, Maria and Rosakis, Phoebus and Notbohm, Jacob and Makridakis, Charalambos and Ravichandran, Guruswami (2019) Cells exploit a phase transition to establish interconnections in fibrous extracellular matrices. . (Unpublished)

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By exerting mechanical forces, biological cells generate striking spatial patterns of localised deformation in the surrounding collagen network. Tethers-paths of high densification and fiber alignment-form between cells, and radial hair-like bands emanate from cell clusters. While tethers facilitate cell communication, the mechanism for their formation is unclear. Here we combine modelling, simulation and experiment, and explore unexpected similarities with martensitic microstructures in shape memory alloys; we show that tether formation is a densification phase transition of the fibrous extracellular matrix, caused by buckling instability of network fibers under cell-induced compression. Our model uses multiscale averaging over fiber orientations to obtain a two-phase, bistable continuum strain energy density for fibrous collagen, with a densified second phase. Simulations predict strain discontinuities between the undensified and the densified phase, which localises within intercellular tethers and radial emanations from cell clusters, as experimentally observed. Ruling out biochemical factors, our experiments use contracting active hydrogel particles to produce similar-but controlled-localised deformations as contractile cells. Our results reveal subtle connections with martensitic phase transitions that demonstrate how, by exploiting a special instability, cells spontaneously generate pathways to each other in a 3D complex medium simply by contracting, with implications on intercellular mechanosensing and the remodelling of matrix mechanical properties by tether networks.

Item Type:Report or Paper (Discussion Paper)
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URLURL TypeDescription Paper
Ravichandran, Guruswami0000-0002-2912-0001
Additional Information:The work of PR, CG and GG was partially supported by the EU Horizon 2020 Research and Innovation Programme under the Marie Sklodowska-Curie project ModComp-Shock ( agreement No 642768. The work of JN and MP and was partially supported by National Science Foundation grant number CMMI-1749400. GR acknowledges the support of the National Science Foundation (DMR No. 0520565) through the Center for Science and Engineering of Materials at the California Institute of Technology. We thank Brian Burkel for assistance in microscopy. Author Contributions: PR, GR and JN planned the research. GG and PR developed the model. GG and CG developed the numerical method. GG performed the simulations. MP and JN designed the experiments. MP performed the experiments; MP and JN analysed the data. All authors discussed and analyzed the results and contributed to writing the manuscript.
Funding AgencyGrant Number
Marie Curie Fellowship642768
Record Number:CaltechAUTHORS:20200122-131403095
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100843
Deposited By: Tony Diaz
Deposited On:22 Jan 2020 23:16
Last Modified:09 Mar 2020 13:19

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