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

ECM remodelling densification patterns fibre alignment fibre buckling phase transition tumour biomarkers

Journal

Journal of the Royal Society, Interface
ISSN: 1742-5662
Titre abrégé: J R Soc Interface
Pays: England
ID NLM: 101217269

Informations de publication

Date de publication:
02 2021
Historique:
entrez: 17 2 2021
pubmed: 18 2 2021
medline: 22 6 2021
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 33593211
doi: 10.1098/rsif.2020.0823
pmc: PMC8086878
doi:

Substances chimiques

Collagen 9007-34-5

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

20200823

Références

Trends Cell Biol. 2011 Jan;21(1):47-56
pubmed: 20870407
Cytoskeleton (Hoboken). 2019 Nov;76(11-12):532-548
pubmed: 31525281
J R Soc Interface. 2019 Oct 31;16(159):20190348
pubmed: 31662075
Adv Biosyst. 2019 Dec;3(12):e1900192
pubmed: 32648678
Biophys J. 2010 May 19;98(10):2281-9
pubmed: 20483337
Macromol Biosci. 2006 Sep 15;6(9):697-702
pubmed: 16967482
Biophys J. 2008 Dec;95(11):5374-84
pubmed: 18775961
Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):658-63
pubmed: 24379367
Soft Matter. 2017 Aug 30;13(34):5749-5758
pubmed: 28759060
Polymers (Basel). 2016 Jul 28;8(8):
pubmed: 30974551
Am J Pathol. 2011 Mar;178(3):1221-32
pubmed: 21356373
Soft Matter. 2017 Dec 6;13(47):8886-8893
pubmed: 29057402
Biomech Model Mechanobiol. 2016 Feb;15(1):213-228
pubmed: 25982442
Sci Rep. 2019 Mar 8;9(1):3990
pubmed: 30850656
Acta Biomater. 2016 Jun;37:28-37
pubmed: 27015891
Phys Rev E. 2018 Nov;98(5):
pubmed: 30619988
Biophys J. 2010 Apr 21;98(8):1632-40
pubmed: 20409484
PLoS One. 2009 Jun 16;4(6):e5902
pubmed: 19529768
BMC Med. 2006 Dec 26;4(1):38
pubmed: 17190588
Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
pubmed: 21917992
Nature. 1981 Mar 19;290(5803):249-51
pubmed: 7207616
J Microsc. 2008 Dec;232(3):463-75
pubmed: 19094023
Cell Adh Migr. 2012 May-Jun;6(3):249-60
pubmed: 22568982
Sci Rep. 2019 Nov 20;9(1):17151
pubmed: 31748563
Cancer Epidemiol Biomarkers Prev. 2006 Jun;15(6):1159-69
pubmed: 16775176
PLoS Comput Biol. 2019 Apr 8;15(4):e1006684
pubmed: 30958816
Biophys J. 2013 Jul 2;105(1):11-20
pubmed: 23823219
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):2827-32
pubmed: 26921325
Cell Mol Bioeng. 2016 Oct 19;10(1):114-123
pubmed: 31719853
PLoS One. 2009 Jul 24;4(7):e6382
pubmed: 19629190
J R Soc Interface. 2015 Jul 6;12(108):20150320
pubmed: 26040601
J Cell Sci. 1999 Oct;112 ( Pt 19):3249-58
pubmed: 10504330
Dev Biol. 1982 Apr;90(2):383-98
pubmed: 7075867
BMC Med. 2008 Apr 28;6:11
pubmed: 18442412
Biomaterials. 2011 Mar;32(8):2043-51
pubmed: 21163521
Biomaterials. 2014 Aug;35(25):6739-49
pubmed: 24840618
Cytometry A. 2012 May;81(5):409-18
pubmed: 22411907
Biophys J. 2014 Dec 2;107(11):2592-603
pubmed: 25468338
Biomaterials. 2020 Mar;234:119756
pubmed: 31954229
Biophys J. 2018 Jan 23;114(2):450-461
pubmed: 29401442
Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12197-202
pubmed: 23754380
Acta Biomater. 2019 Jan 15;84:280-292
pubmed: 30500449

Auteurs

Georgios Grekas (G)

Aerospace Engineering and Mechanics, University of Minnesota, Minneapolis, MN, USA.

Maria Proestaki (M)

Department of Engineering Physics, University of Wisconsin-Madison, Madison, WI, USA.

Phoebus Rosakis (P)

Department of Mathematics and Applied Mathematics, University of Crete, Heraklion, Greece.
Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Greece.

Jacob Notbohm (J)

Department of Engineering Physics, University of Wisconsin-Madison, Madison, WI, USA.

Charalambos Makridakis (C)

Department of Mathematics and Applied Mathematics, University of Crete, Heraklion, Greece.
Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Greece.
Department of Mathematics, MPS, University of Sussex, Brighton, UK.

Guruswami Ravichandran (G)

Division of Engineering and Applied Science, California Institute of Technology, Pasadena, CA, USA.

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Classifications MeSH