Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
12 09 2023
12 09 2023
Historique:
received:
26
08
2022
accepted:
29
08
2023
medline:
14
9
2023
pubmed:
13
9
2023
entrez:
12
9
2023
Statut:
epublish
Résumé
Protrusions at the leading-edge of a cell play an important role in sensing the extracellular cues during cellular spreading and motility. Recent studies provided indications that these protrusions wrap (coil) around the extracellular fibers. However, the physics of this coiling process, and the mechanisms that drive it, are not well understood. We present a combined theoretical and experimental study of the coiling of cellular protrusions on fibers of different geometry. Our theoretical model describes membrane protrusions that are produced by curved membrane proteins that recruit the protrusive forces of actin polymerization, and identifies the role of bending and adhesion energies in orienting the leading-edges of the protrusions along the azimuthal (coiling) direction. Our model predicts that the cell's leading-edge coils on fibers with circular cross-section (above some critical radius), but the coiling ceases for flattened fibers of highly elliptical cross-section. These predictions are verified by 3D visualization and quantitation of coiling on suspended fibers using Dual-View light-sheet microscopy (diSPIM). Overall, we provide a theoretical framework, supported by experiments, which explains the physical origin of the coiling phenomenon.
Identifiants
pubmed: 37699891
doi: 10.1038/s41467-023-41273-y
pii: 10.1038/s41467-023-41273-y
pmc: PMC10497540
doi:
Substances chimiques
Membrane Proteins
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5612Informations de copyright
© 2023. Springer Nature Limited.
Références
Nat Rev Mol Cell Biol. 2009 Jul;10(7):445-57
pubmed: 19546857
Annu Rev Cell Dev Biol. 2014;30:503-33
pubmed: 25288117
Cell. 2014 Jan 16;156(1-2):277-90
pubmed: 24439382
Physiol Rev. 2019 Jul 1;99(3):1381-1431
pubmed: 31066630
Nat Biotechnol. 2013 Nov;31(11):1032-8
pubmed: 24108093
Cell. 2011 Jun 24;145(7):1012-22
pubmed: 21703446
Dev Neurobiol. 2021 Jul;81(5):464-489
pubmed: 32281247
Soft Matter. 2022 Dec 21;19(1):31-43
pubmed: 36472164
J Cell Sci. 2023 Jul 15;136(14):
pubmed: 37497740
Adv Sci (Weinh). 2022 Sep;9(25):e2203011
pubmed: 35863910
Soft Matter. 2015 Jul 7;11(25):5004-9
pubmed: 25909915
Sci Adv. 2017 Sep 06;3(9):e1700150
pubmed: 28913421
Cancer Metastasis Rev. 2009 Jun;28(1-2):137-49
pubmed: 19153671
Physiol Rev. 2014 Jan;94(1):235-63
pubmed: 24382887
Trends Cell Biol. 2018 Oct;28(10):823-834
pubmed: 29970282
Nat Biotechnol. 2020 Nov;38(11):1337-1346
pubmed: 32601431
Mol Cell Neurosci. 2006 Apr;31(4):613-27
pubmed: 16442810
Mol Biol Cell. 2022 May 15;33(6):ar55
pubmed: 34985924
Rev Sci Instrum. 2012 Sep;83(9):094302
pubmed: 23020396
Adv Sci (Weinh). 2023 Mar;10(7):e2207368
pubmed: 36698307
J Cell Biol. 2003 Aug 4;162(3):489-98
pubmed: 12900397
Adv Biosyst. 2019 Oct;3(10):e1900080
pubmed: 32648723
Phys Rev E. 2018 Mar;97(3-1):032408
pubmed: 29776029
J Cell Sci. 1995 Feb;108 ( Pt 2):735-45
pubmed: 7769015
ACS Nano. 2017 Dec 26;11(12):12037-12048
pubmed: 29144730
J Cell Biol. 2021 Aug 2;220(8):
pubmed: 34096975
Physiol Rev. 2008 Apr;88(2):489-513
pubmed: 18391171
Biophys J. 2014 Dec 2;107(11):2604-11
pubmed: 25468339
Nat Cell Biol. 2016 Apr 27;18(5):459-61
pubmed: 27117328
Phys Rev E. 2019 Aug;100(2-1):020401
pubmed: 31574594
J Neurosci Res. 2009 Nov 15;87(15):3480-91
pubmed: 19170162
Biophys J. 2008 Nov 1;95(9):4416-25
pubmed: 18658210
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Biol Methods. 2014;1(2):
pubmed: 25606571
Biophys J. 2017 May 9;112(9):1975-1983
pubmed: 28494967
Soft Matter. 2019 Jul 14;15(26):5319-5330
pubmed: 31237259
Open Biol. 2019 Oct 31;9(10):190155
pubmed: 31640476
J Cell Sci. 2022 Mar 15;135(6):
pubmed: 35285496
J Cell Biol. 2015 Nov 9;211(3):683-701
pubmed: 26553933
Commun Biol. 2020 Jul 21;3(1):390
pubmed: 32694539
Acta Biomater. 2017 Mar 1;50:41-55
pubmed: 28011142
Biomed Microdevices. 2009 Aug;11(4):739-46
pubmed: 19242806
FASEB J. 2019 Oct;33(10):10618-10632
pubmed: 31225977
iScience. 2019 Sep 27;19:905-915
pubmed: 31513975
Nat Rev Mol Cell Biol. 2008 Sep;9(9):730-6
pubmed: 18628785
Curr Opin Cell Biol. 2010 Oct;22(5):617-25
pubmed: 20817428
J R Soc Interface. 2018 Aug;15(145):
pubmed: 30089684
Dev Cell. 2009 Sep;17(3):307-9
pubmed: 19758555
J Invest Dermatol. 1982 Nov;79(5):264-9
pubmed: 6752288
PLoS Biol. 2010 Nov 30;8(11):e1000544
pubmed: 21151339
Arch Histol Cytol. 2002 Jun;65(2):109-26
pubmed: 12164335
Nat Protoc. 2014 Nov;9(11):2555-73
pubmed: 25299154
Biomaterials. 2020 Feb;232:119739
pubmed: 31911284