MT1-MMP directs force-producing proteolytic contacts that drive tumor cell invasion.
Actin-Related Protein 2-3 Complex
/ metabolism
Actins
/ metabolism
Breast Neoplasms
/ pathology
Cell Line, Tumor
Collagen Type I
/ metabolism
Extracellular Matrix
Humans
Matrix Metalloproteinase 14
/ metabolism
Microscopy, Electron
Models, Theoretical
Neoplasm Invasiveness
Podosomes
/ metabolism
Polymerization
Proteolysis
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
25 10 2019
25 10 2019
Historique:
received:
15
04
2019
accepted:
04
10
2019
entrez:
27
10
2019
pubmed:
28
10
2019
medline:
12
2
2020
Statut:
epublish
Résumé
Unraveling the mechanisms that govern the formation and function of invadopodia is essential towards the prevention of cancer spread. Here, we characterize the ultrastructural organization, dynamics and mechanical properties of collagenotytic invadopodia forming at the interface between breast cancer cells and a physiologic fibrillary type I collagen matrix. Our study highlights an uncovered role for MT1-MMP in directing invadopodia assembly independent of its proteolytic activity. Electron microscopy analysis reveals a polymerized Arp2/3 actin network at the concave side of the curved invadopodia in association with the collagen fibers. Actin polymerization is shown to produce pushing forces that repel the confining matrix fibers, and requires MT1-MMP matrix-degradative activity to widen the matrix pores and generate the invasive pathway. A theoretical model is proposed whereby pushing forces result from actin assembly and frictional forces in the actin meshwork due to the curved geometry of the matrix fibers that counterbalance resisting forces by the collagen fibers.
Identifiants
pubmed: 31653854
doi: 10.1038/s41467-019-12930-y
pii: 10.1038/s41467-019-12930-y
pmc: PMC6814785
doi:
Substances chimiques
Actin-Related Protein 2-3 Complex
0
Actins
0
Collagen Type I
0
Matrix Metalloproteinase 14
EC 3.4.24.80
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4886Références
Nat Commun. 2014 Nov 11;5:5343
pubmed: 25385672
Genes Dev. 2018 Feb 1;32(3-4):244-257
pubmed: 29483153
Cancer Res. 2009 Apr 1;69(7):2792-800
pubmed: 19276357
Dev Cell. 2018 Oct 22;47(2):145-160.e6
pubmed: 30269950
Integr Biol (Camb). 2015 Oct;7(10):1186-95
pubmed: 26021600
J Biol Chem. 2001 Jul 13;276(28):25705-14
pubmed: 11335709
Annu Rev Cell Dev Biol. 2011;27:185-211
pubmed: 21801014
J Cell Biol. 2013 Dec 23;203(6):1063-79
pubmed: 24344185
J Cell Biol. 2015 Feb 2;208(3):331-50
pubmed: 25646088
J Cell Biol. 2018 Jul 2;217(7):2549-2564
pubmed: 29891722
Nat Rev Mol Cell Biol. 2011 Jun 23;12(7):413-26
pubmed: 21697900
Traffic. 2000 Jul;1(7):545-52
pubmed: 11208142
J Cell Biol. 2015 Oct 26;211(2):339-58
pubmed: 26504170
Nat Cell Biol. 2018 Jan;20(1):8-20
pubmed: 29269951
J Biol Chem. 2002 Oct 11;277(41):39005-14
pubmed: 12145314
Biophys J. 2011 Feb 2;100(3):573-582
pubmed: 21281571
Sci Rep. 2015 Mar 30;5:9466
pubmed: 25820462
J Cell Sci. 2018 Jan 8;131(1):
pubmed: 29311151
Nat Commun. 2018 Oct 8;9(1):4144
pubmed: 30297715
Acta Biomater. 2014 May;10(5):1886-96
pubmed: 24412623
Oncogene. 2016 Jan 21;35(3):344-57
pubmed: 25893299
Nature. 2009 Aug 20;460(7258):1031-4
pubmed: 19648907
Biochemistry. 2005 Jan 18;44(2):584-8
pubmed: 15641783
Science. 2003 Mar 14;299(5613):1743-7
pubmed: 12637748
Dev Cell. 2019 Feb 11;48(3):313-328.e8
pubmed: 30686527
Mol Biol Cell. 2010 Dec;21(23):4108-19
pubmed: 20926684
Cell. 2016 Jan 14;164(1-2):115-127
pubmed: 26771487
J Cell Biol. 2014 Nov 24;207(4):517-33
pubmed: 25422375
PLoS Biol. 2014 Nov 11;12(11):e1001995
pubmed: 25386698
Bio Protoc. 2016 Dec 20;6(24):
pubmed: 28191488
J Cell Biol. 2009 Apr 6;185(1):11-9
pubmed: 19332889
J Natl Cancer Inst. 2000 Jul 19;92(14):1185-6
pubmed: 10904098
Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):11537-11542
pubmed: 30348801
Trends Cell Biol. 2008 Nov;18(11):560-74
pubmed: 18848450
Nat Cell Biol. 2007 Aug;9(8):893-904
pubmed: 17618273
Nature. 1997 Oct 30;389(6654):990-4
pubmed: 9353125
Cold Spring Harb Perspect Biol. 2018 Jan 2;10(1):
pubmed: 29295889
J Cell Biol. 2001 Dec 24;155(7):1345-56
pubmed: 11756481
Genes Dev. 2006 Oct 1;20(19):2673-86
pubmed: 16983145
ACS Nano. 2017 Apr 25;11(4):4028-4040
pubmed: 28355484
Ultramicroscopy. 2011 Dec;111(12):1659-69
pubmed: 22094372
Mol Biol Cell. 2012 Jan;23(2):297-309
pubmed: 22114353
J Biol Chem. 2004 Oct 8;279(41):43336-44
pubmed: 15292230
J Cell Sci. 2009 Sep 1;122(Pt 17):3015-24
pubmed: 19692588
J Cell Biol. 2018 Jan 2;217(1):195-209
pubmed: 29133484
J Cell Biol. 2013 Jun 24;201(7):1069-84
pubmed: 23798731
Cancer Res. 2006 Mar 15;66(6):3034-43
pubmed: 16540652
J Cell Biol. 1987 Oct;105(4):1473-8
pubmed: 3312229
J Cell Biol. 2012 Oct 29;199(3):527-44
pubmed: 23091069
Oncogene. 2018 Dec;37(50):6425-6441
pubmed: 30065298
Dev Cell. 2010 Jul 20;19(1):13-26
pubmed: 20643347
J Cell Biol. 2016 Mar 28;212(7):763-6
pubmed: 27002174
J Cell Sci. 2016 Oct 1;129(19):3661-3674
pubmed: 27694340
Cancer Res. 2011 Jul 1;71(13):4527-38
pubmed: 21571860
Nat Commun. 2018 Jun 22;9(1):2443
pubmed: 29934494
Annu Rev Cell Dev Biol. 2016 Oct 6;32:555-576
pubmed: 27501444
Biomaterials. 2016 Apr;84:119-129
pubmed: 26826790
Curr Biol. 2008 Sep 9;18(17):1295-1299
pubmed: 18718759
Cell Rep. 2014 Sep 11;8(5):1558-70
pubmed: 25176655
ACS Appl Mater Interfaces. 2016 Aug 31;8(34):21946-55
pubmed: 27128771
Trends Cell Biol. 2017 Aug;27(8):595-607
pubmed: 28412099
Curr Biol. 2013 Nov 4;23(21):2079-89
pubmed: 24206842