Bursts of activity in collective cell migration.
Dense monolayers of living cells display intriguing relaxation dynamics, reminiscent of soft and glassy materials close to the jamming transition, and migrate collectively when space is available, as in wound healing or in cancer invasion. Here we show that collective cell migration occurs in bursts that are similar to those recorded in the propagation of cracks, fluid fronts in porous media, and ferromagnetic domain walls. In analogy with these systems, the distribution of activity bursts displays scaling laws that are universal in different cell types and for cells moving on different substrates. The main features of the invasion dynamics are quantitatively captured by a model of interacting active particles moving in a disordered landscape. Our results illustrate that collective motion of living cells is analogous to the corresponding dynamics in driven, but inanimate, systems.
Department of Applied Physics, Aalto University, FIN-00076 Aalto, Espoo, Finland.
Oleksandr
O
Chepizhko
Department of Biosciences, Center for Complexity and Biosystems, University of Milan, 20133 Milan, Italy.
Costanza
C
Giampietro
Department of Biosciences, University of Milan, 20133 Milan, Italy.
Eleonora
E
Mastrapasqua
Department of Applied Physics, Aalto University, FIN-00076 Aalto, Espoo, Finland.
Mehdi
M
Nourazar
Department of Biosciences, University of Milan, 20133 Milan, Italy.
Miriam
M
Ascagni
Department of Biosciences, Center for Complexity and Biosystems, University of Milan, 20133 Milan, Italy.
Michela
M
Sugni
Department of Biosciences, University of Milan, 20133 Milan, Italy.
Umberto
U
Fascio
Department of Biosciences, University of Milan, 20133 Milan, Italy.
Livio
L
Leggio
Dipartimento di Scienze della Salute, San Paolo, University of Milan, 20122 Milan, Italy.
Chiara
C
Malinverno
Dipartimento di Scienze della Salute, San Paolo, University of Milan, 20122 Milan, Italy.
Giorgio
G
Scita
Laboratoire de Physique de l'École Normale Supérieure de Lyon, UMR CNRS 5672, Université de Lyon, 69364 Lyon, France.
Stéphane
S
Santucci
Department of Applied Physics, Aalto University, FIN-00076 Aalto, Espoo, Finland.
Mikko J
MJ
Alava
Department of Applied Physics, Aalto University, FIN-00076 Aalto, Espoo, Finland; Department of Physics, Center for Complexity and Biosystems, University of Milan, 20133 Milan, Italy; Institute for Scientific Interchange Foundation, 10126 Torino, Italy; Istituto di Chimica della Materia Condensata e di Tecnologie per l'Energia, Consiglio Nazionale delle Ricerche, 20125 Milan, Italy.
Stefano
S
Zapperi
Department of Biosciences, Center for Complexity and Biosystems, University of Milan, 20133 Milan, Italy; caterina.laporta@unimi.it.
Caterina A M
CA
La Porta
D000818:Animals; D015703:Antigens, CD / Q000378:metabolism; D001696:Biomechanical Phenomena; D015820:Cadherins / Q000378:metabolism; D002417:Cattle; D002460:Cell Line; D002465:Cell Movement / Q000187:drug effects; D003094:Collagen / Q000494:pharmacology; D003198:Computer Simulation; D055785:Gene Knockdown Techniques; D006801:Humans; D051379:Mice; D008954:Models, Biological; D059008:Time-Lapse Imaging; D000099152:Cadherin 5
D015703:Antigens, CD; D015820:Cadherins; D003094:Collagen; D000099152:Cadherin 5
avalanches; collagen substrate; collective cell migration; universality; vascular endothelial cadherin
Proc Natl Acad Sci U S A. 2007 Oct 9;104(41):15988-93
17905871
Mol Biol Cell. 2002 Apr;13(4):1175-89
11950930
J Mol Histol. 2004 Nov;35(8-9):839-44
15609097
Blood. 2009 Aug 13;114(7):1387-95
19491394
Biochim Biophys Acta. 2014 Aug;1840(8):2386-95
24721714
Nature. 2001 Mar 8;410(6825):242-50
11258379
Phys Rev E Stat Nonlin Soft Matter Phys. 2006 Dec;74(6 Pt 1):061908
17280097
J R Soc Interface. 2014 Aug 6;11(97):20140325
24850906
PLoS One. 2012;7(3):e33476
22479403
Phys Rev Lett. 2006 Feb 3;96(4):045501
16486839
Arterioscler Thromb Vasc Biol. 2000 Jun;20(6):1443-51
10845856
PLoS Comput Biol. 2013;9(3):e1002944
23505356
Physiology (Bethesda). 2013 Nov;28(6):370-9
24186932
Annu Rev Cell Dev Biol. 2003;19:207-35
14570569
Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):10703-7
26261319
Phys Rev E Stat Nonlin Soft Matter Phys. 2009 May;79(5 Pt 1):051106
19518415
PLoS One. 2013 Jun 24;8(6):e67389
23826283
Phys Rev Lett. 2015 Jun 5;114(22):228101
26196647
Nat Phys. 2014 Sep;10(9):683-690
27340423
Phys Rev B Condens Matter. 1992 Nov 1;46(18):11520-11549
10003040
Phys Rev Lett. 2001 Feb 26;86(9):1785-8
11290248
J Cell Biol. 2015 Dec 21;211(6):1177-92
26668327
Nat Mater. 2011 Jun;10(6):469-75
21602808
Exp Cell Res. 2013 Oct 1;319(16):2418-23
23664834
Nat Mater. 2015 Oct;14(10):1040-8
26237129
Nat Commun. 2015 Jun 25;6:7516
26108639
Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12729-34
26417082
Soft Matter. 2014 Apr 14;10(14):2397-404
24623049
Biophys J. 2005 Mar;88(3):2250-6
15596493
Annu Rev Biomed Eng. 2003;5:251-84
12730082
Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4714-9
21321233
J Cell Biol. 2012 Oct 29;199(3):545-63
23091067
Blood. 2012 Mar 1;119(9):2159-70
22246030
Phys Rev Lett. 2014 Aug 15;113(7):074501
25170710
Phys Rev E Stat Nonlin Soft Matter Phys. 2011 Apr;83(4 Pt 2):046108
21599241
Proc Natl Acad Sci U S A. 2007 May 15;104(20):8281-6
17488828
Phys Rev Lett. 2000 May 15;84(20):4705-8
10990776