Actin bundle architecture and mechanics regulate myosin II force generation.
Journal
Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626
Informations de publication
Date de publication:
18 05 2021
18 05 2021
Historique:
received:
20
07
2020
revised:
01
03
2021
accepted:
12
03
2021
pubmed:
3
4
2021
medline:
3
7
2021
entrez:
2
4
2021
Statut:
ppublish
Résumé
The actin cytoskeleton is a soft, structural material that underlies biological processes such as cell division, motility, and cargo transport. The cross-linked actin filaments self-organize into a myriad of architectures, from disordered meshworks to ordered bundles, which are hypothesized to control the actomyosin force generation that regulates cell migration, shape, and adhesion. Here, we use fluorescence microscopy and simulations to investigate how actin bundle architectures with varying polarity, spacing, and rigidity impact myosin II dynamics and force generation. Microscopy reveals that mixed-polarity bundles formed by rigid cross-linkers support slow, bidirectional myosin II filament motion, punctuated by periods of stalled motion. Simulations reveal that these locations of stalled myosin motion correspond to sustained, high forces in regions of balanced actin filament polarity. By contrast, mixed-polarity bundles formed by compliant, large cross-linkers support fast, bidirectional motion with no traps. Simulations indicate that trap duration is directly related to force magnitude and that the observed increased velocity corresponds to lower forces resulting from both the increased bundle compliance and filament spacing. Our results indicate that the microstructures of actin assemblies regulate the dynamics and magnitude of myosin II forces, highlighting the importance of architecture and mechanics in regulating forces in biological materials.
Identifiants
pubmed: 33798565
pii: S0006-3495(21)00256-3
doi: 10.1016/j.bpj.2021.03.026
pmc: PMC8204393
pii:
doi:
Substances chimiques
Actins
0
Actomyosin
9013-26-7
Myosin Type II
EC 3.6.1.-
Myosins
EC 3.6.4.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
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
1957-1970Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM098441
Pays : United States
Organisme : NIBIB NIH HHS
ID : T32 EB009412
Pays : United States
Informations de copyright
Copyright © 2021 Biophysical Society. Published by Elsevier Inc. All rights reserved.
Références
Physiol Rev. 2014 Jan;94(1):235-63
pubmed: 24382887
Trends Cell Biol. 2012 Feb;22(2):61-81
pubmed: 22119497
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18243-8
pubmed: 19805036
Prog Biophys Biophys Chem. 1957;7:255-318
pubmed: 13485191
Curr Biol. 2016 Oct 24;26(20):2697-2706
pubmed: 27666967
Mol Biol Cell. 2014 Jun 15;25(12):1845-53
pubmed: 24760970
Elife. 2018 Feb 08;7:
pubmed: 29419377
J Cell Biol. 2006 Sep 11;174(6):863-75
pubmed: 16966425
Proc Natl Acad Sci U S A. 2019 Aug 13;116(33):16192-16197
pubmed: 31346091
Curr Opin Cell Biol. 2000 Feb;12(1):72-8
pubmed: 10679353
J Physiol. 1974 Nov;243(1):1-43
pubmed: 4449057
Soft Matter. 2020 Feb 26;16(8):2135-2140
pubmed: 32016200
Biophys J. 2015 Apr 21;108(8):1997-2006
pubmed: 25902439
J Cell Biol. 2007 Dec 3;179(5):1011-25
pubmed: 18056414
J Biol Chem. 1971 Aug 10;246(15):4866-71
pubmed: 4254541
Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7757-62
pubmed: 20385838
Biochem J. 2014 Apr 1;459(1):1-13
pubmed: 24627985
Nature. 1985 Jun 13-19;315(6020):584-6
pubmed: 3925346
Biochemistry. 1997 Sep 30;36(39):11828-36
pubmed: 9305974
Nat Rev Mol Cell Biol. 2015 Aug;16(8):486-98
pubmed: 26130009
Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9844-9
pubmed: 16785439
Biophys J. 2015 Oct 20;109(8):1574-82
pubmed: 26488648
Curr Biol. 2010 Aug 24;20(16):1415-22
pubmed: 20705466
Biochemistry. 1982 Mar 16;21(6):1284-94
pubmed: 7074085
Biochim Biophys Acta. 2001 Apr 23;1538(2-3):99-117
pubmed: 11336782
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9685-90
pubmed: 19478066
Proc Natl Acad Sci U S A. 2017 Nov 21;114(47):E10037-E10045
pubmed: 29114058
Phys Rev Lett. 2003 Oct 3;91(14):148102
pubmed: 14611558
Curr Opin Cell Biol. 2018 Feb;50:79-85
pubmed: 29482169
Mol Biol Cell. 2016 Jun 1;27(11):1821-33
pubmed: 27075176
J Cell Sci. 1994 Nov;107 ( Pt 11):3077-90
pubmed: 7699007
Proc Natl Acad Sci U S A. 1986 Sep;83(17):6272-6
pubmed: 3462694
Curr Biol. 2011 Jul 26;21(14):R560-9
pubmed: 21783039
Cytoskeleton (Hoboken). 2014 Nov;71(11):595-610
pubmed: 25382100
Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9616-20
pubmed: 18599451
Nat Cell Biol. 2003 Nov;5(11):980-6
pubmed: 14578909
Traffic. 2013 Jan;14(1):70-81
pubmed: 23046080
Cell Adh Migr. 2011 Mar-Apr;5(2):160-9
pubmed: 21169733
Science. 2012 Jun 8;336(6086):1310-4
pubmed: 22679097
Proc Natl Acad Sci U S A. 1981 Nov;78(11):6849-53
pubmed: 6947259
Phys Rev Lett. 2012 May 4;108(18):188101
pubmed: 22681120
Curr Biol. 2009 Jun 9;19(11):967-73
pubmed: 19398338
Methods Enzymol. 1982;85 Pt B:55-71
pubmed: 6214692
PLoS One. 2012;7(11):e49174
pubmed: 23139838
Annu Rev Biophys Biomol Struct. 2006;35:361-87
pubmed: 16689641
Biophys J. 2013 Feb 5;104(3):655-65
pubmed: 23442916
Methods Enzymol. 1982;85 Pt B:316-21
pubmed: 7121272
Biophys J. 2016 Nov 15;111(10):2228-2240
pubmed: 27851945
J Cell Biol. 2020 May 4;219(5):
pubmed: 32294157
J Cell Biol. 1993 Nov;123(3):637-52
pubmed: 8227130
Curr Biol. 2016 Mar 7;26(5):616-26
pubmed: 26898468
Biophys J. 2011 Sep 7;101(5):1231-7
pubmed: 21889461
J Gen Physiol. 2016 Dec;148(6):459-488
pubmed: 27864330
Trends Cell Biol. 2019 Feb;29(2):150-163
pubmed: 30385150