Literature DB >> 33593211

Cells exploit a phase transition to mechanically remodel the fibrous extracellular matrix.

Georgios Grekas1, Maria Proestaki2, Phoebus Rosakis3,4, Jacob Notbohm2, Charalambos Makridakis3,4,5, Guruswami Ravichandran6.   

Abstract

Through mechanical forces, biological cells remodel the surrounding collagen network, generating striking deformation patterns. Tethers-tracts of high densification and fibre alignment-form between cells, thinner bands emanate from cell clusters. While tethers facilitate cell migration and communication, how they form is unclear. Combining modelling, simulation and experiment, we show that tether formation is a densification phase transition of the extracellular matrix, caused by buckling instability of network fibres under cell-induced compression, featuring unexpected similarities with martensitic microstructures. Multiscale averaging yields a two-phase, bistable continuum energy landscape for fibrous collagen, with a densified/aligned second phase. Simulations predict strain discontinuities between the undensified and densified phase, which localizes within tethers as experimentally observed. In our experiments, active particles induce similar localized patterns as cells. This shows how cells exploit an instability to mechanically remodel the extracellular matrix simply by contracting, thereby facilitating mechanosensing, invasion and metastasis.

Entities:  

Keywords:  ECM remodelling; densification patterns; fibre alignment; fibre buckling; phase transition; tumour biomarkers

Mesh:

Substances:

Year:  2021        PMID: 33593211      PMCID: PMC8086878          DOI: 10.1098/rsif.2020.0823

Source DB:  PubMed          Journal:  J R Soc Interface        ISSN: 1742-5662            Impact factor:   4.118


  42 in total

1.  Structural hierarchy governs fibrin gel mechanics.

Authors:  Izabela K Piechocka; Rommel G Bacabac; Max Potters; Fred C Mackintosh; Gijsje H Koenderink
Journal:  Biophys J       Date:  2010-05-19       Impact factor: 4.033

Review 2.  Forcing form and function: biomechanical regulation of tumor evolution.

Authors:  Hongmei Yu; Janna Kay Mouw; Valerie M Weaver
Journal:  Trends Cell Biol       Date:  2010-10-01       Impact factor: 20.808

3.  Rapid disorganization of mechanically interacting systems of mammary acini.

Authors:  Quanming Shi; Rajarshi P Ghosh; Hanna Engelke; Chris H Rycroft; Luke Cassereau; James A Sethian; Valerie M Weaver; Jan T Liphardt
Journal:  Proc Natl Acad Sci U S A       Date:  2013-12-30       Impact factor: 11.205

4.  Mechanical Interaction between Cells Facilitates Molecular Transport.

Authors:  David Gomez; Sari Natan; Yair Shokef; Ayelet Lesman
Journal:  Adv Biosyst       Date:  2019-11-04

5.  Mechanical response of collagen networks to nonuniform microscale loads.

Authors:  Brian Burkel; Jacob Notbohm
Journal:  Soft Matter       Date:  2017-08-30       Impact factor: 3.679

6.  Force chains in cell-cell mechanical communication.

Authors:  Amots Mann; Ran S Sopher; Shahar Goren; Ortal Shelah; Oren Tchaicheeyan; Ayelet Lesman
Journal:  J R Soc Interface       Date:  2019-10-30       Impact factor: 4.118

7.  Micromechanical testing of individual collagen fibrils.

Authors:  Joost A J van der Rijt; Kees O van der Werf; Martin L Bennink; Pieter J Dijkstra; Jan Feijen
Journal:  Macromol Biosci       Date:  2006-09-15       Impact factor: 4.979

8.  Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization.

Authors:  Paolo P Provenzano; David R Inman; Kevin W Eliceiri; Steven M Trier; Patricia J Keely
Journal:  Biophys J       Date:  2008-09-05       Impact factor: 4.033

9.  Organization of associating or crosslinked actin filaments in confinement.

Authors:  Maral Adeli Koudehi; David M Rutkowski; Dimitrios Vavylonis
Journal:  Cytoskeleton (Hoboken)       Date:  2019-10-31

Review 10.  Semiflexible Biopolymers in Bundled Arrangements.

Authors:  Jörg Schnauß; Tina Händler; Josef A Käs
Journal:  Polymers (Basel)       Date:  2016-07-28       Impact factor: 4.329

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  4 in total

1.  Effect of hyaluronic acid on microscale deformations of collagen gels.

Authors:  Maria Proestaki; Mainak Sarkar; Brian M Burkel; Suzanne M Ponik; Jacob Notbohm
Journal:  J Mech Behav Biomed Mater       Date:  2022-09-14

2.  Percolation of collagen stress in a random network model of the alveolar wall.

Authors:  Dylan T Casey; Samer Bou Jawde; Jacob Herrmann; Vitor Mori; J Matthew Mahoney; Béla Suki; Jason H T Bates
Journal:  Sci Rep       Date:  2021-08-17       Impact factor: 4.379

3.  Effect of matrix heterogeneity on cell mechanosensing.

Authors:  Maria Proestaki; Brian M Burkel; Emmett E Galles; Suzanne M Ponik; Jacob Notbohm
Journal:  Soft Matter       Date:  2021-11-24       Impact factor: 3.679

4.  Collagen fibril assembly: New approaches to unanswered questions.

Authors:  Christopher K Revell; Oliver E Jensen; Tom Shearer; Yinhui Lu; David F Holmes; Karl E Kadler
Journal:  Matrix Biol Plus       Date:  2021-07-13
  4 in total

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