The role of flow in the self-assembly of dragline spider silk proteins.
Journal
Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626
Informations de publication
Date de publication:
07 11 2023
07 11 2023
Historique:
received:
25
10
2022
revised:
14
07
2023
accepted:
29
09
2023
pmc-release:
07
11
2024
medline:
10
11
2023
pubmed:
7
10
2023
entrez:
7
10
2023
Statut:
ppublish
Résumé
Hydrodynamic flow in the spider duct induces conformational changes in dragline spider silk proteins (spidroins) and drives their assembly, but the underlying physical mechanisms are still elusive. Here we address this challenging multiscale problem with a complementary strategy of atomistic and coarse-grained molecular dynamics simulations with uniform flow. The conformational changes at the molecular level were analyzed for single-tethered spider silk peptides. Uniform flow leads to coiled-to-stretch transitions and pushes alanine residues into β sheet and poly-proline II conformations. Coarse-grained simulations of the assembly process of multiple semi-flexible block copolymers using multi-particle collision dynamics reveal that the spidroins aggregate faster but into low-order assemblies when they are less extended. At medium-to-large peptide extensions (50%-80%), assembly slows down and becomes reversible with frequent association and dissociation events, whereas spidroin alignment increases and alanine repeats form ordered regions. Our work highlights the role of flow in guiding silk self-assembly into tough fibers by enhancing alignment and kinetic reversibility, a mechanism likely relevant also for other proteins whose function depends on hydrodynamic flow.
Identifiants
pubmed: 37803828
pii: S0006-3495(23)00624-0
doi: 10.1016/j.bpj.2023.09.020
pmc: PMC10645567
pii:
doi:
Substances chimiques
Silk
0
Arthropod Proteins
0
Fibroins
9007-76-5
Peptides
0
Alanine
OF5P57N2ZX
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4241-4253Informations de copyright
Copyright © 2023 Biophysical Society. Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Proc Natl Acad Sci U S A. 2018 May 22;115(21):E4758-E4766
pubmed: 29735687
BMC Biophys. 2012 Dec 17;5:22
pubmed: 23244740
Nat Chem Biol. 2017 Mar;13(3):262-264
pubmed: 28068309
ACS Chem Neurosci. 2017 Nov 15;8(11):2558-2567
pubmed: 28759721
Annu Rev Phys Chem. 2015 Apr;66:217-39
pubmed: 25532951
J Chem Theory Comput. 2016 Jul 12;12(7):3407-15
pubmed: 27243806
Nat Commun. 2018 May 29;9(1):2121
pubmed: 29844575
Proc Natl Acad Sci U S A. 2017 Feb 7;114(6):1232-1237
pubmed: 28123065
J Phys Condens Matter. 2011 Jan 26;23(3):033102
pubmed: 21406855
Nat Commun. 2015 May 28;6:6892
pubmed: 26017575
Biomacromolecules. 2009 Jan 12;10(1):49-57
pubmed: 19053289
ACS Biomater Sci Eng. 2015 Jul 13;1(7):577-584
pubmed: 27064312
Sci Rep. 2017 Oct 27;7(1):14278
pubmed: 29079767
Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):11507-11512
pubmed: 30348773
Phys Rev E Stat Nonlin Soft Matter Phys. 2015 Jan;91(1):013310
pubmed: 25679742
Science. 1996 Jan 5;271(5245):84-7
pubmed: 8539605
Biophys J. 2008 Aug;95(3):1303-13
pubmed: 18441028
Nanotechnology. 2010 Jun 11;21(23):235101
pubmed: 20463391
Nat Chem Biol. 2015 May;11(5):309-15
pubmed: 25885958
J Chem Theory Comput. 2020 Apr 14;16(4):2494-2507
pubmed: 31914313
Blood. 2022 Dec 8;140(23):2490-2499
pubmed: 36040485
Nat Mater. 2010 Apr;9(4):359-67
pubmed: 20228820
Nature. 2003 Aug 28;424(6952):1057-61
pubmed: 12944968
Nature. 2001 Mar 29;410(6828):541-8
pubmed: 11279484
J R Soc Interface. 2010 Dec 6;7(53):1709-21
pubmed: 20519206
J Mech Behav Biomed Mater. 2020 Aug;108:103773
pubmed: 32310107
PLoS One. 2017 Aug 23;12(8):e0183397
pubmed: 28832627
Biophys J. 2009 May 20;96(10):3997-4005
pubmed: 19450471
J Exp Biol. 2006 Nov;209(Pt 21):4355-62
pubmed: 17050850
J Am Chem Soc. 2010 Dec 8;132(48):17277-81
pubmed: 21080669
Phys Rev Lett. 2006 Sep 29;97(13):138101
pubmed: 17026077
J Chem Phys. 2010 Oct 28;133(16):164905
pubmed: 21033821
Biophys J. 2019 May 7;116(9):1579-1585
pubmed: 30975453
J Phys Chem B. 2015 Aug 27;119(34):11358-70
pubmed: 26131594
Biophys J. 2010 Dec 15;99(12):3863-9
pubmed: 21156127
Biofabrication. 2017 May 31;9(2):025025
pubmed: 28471354
J Phys Chem B. 2015 Apr 23;119(16):5113-23
pubmed: 25764013
Adv Theory Simul. 2020 Dec;3(12):2000156
pubmed: 33173846
Proc Biol Sci. 2001 Nov 22;268(1483):2339-46
pubmed: 11703874
Proteins. 2003 May 1;51(2):224-35
pubmed: 12660991
Curr Biol. 2021 Nov 8;31(21):R1422-R1423
pubmed: 34752765
Protein Eng Des Sel. 2009 Dec;22(12):741-6
pubmed: 19850675
Proc Natl Acad Sci U S A. 2017 May 2;114(18):4673-4678
pubmed: 28416674
Biomacromolecules. 2016 Feb 8;17(2):427-36
pubmed: 26669270
Proc Natl Acad Sci U S A. 2008 May 6;105(18):6590-5
pubmed: 18445655
Proc Natl Acad Sci U S A. 2007 May 8;104(19):7899-903
pubmed: 17470810
Biophys J. 2006 Jul 1;91(1):42-54
pubmed: 16565055
Nat Commun. 2018 Nov 14;9(1):4779
pubmed: 30429482
Phys Rev E Stat Nonlin Soft Matter Phys. 2005 Jun;71(6 Pt 1):061804
pubmed: 16089758
Biomacromolecules. 2021 Aug 9;22(8):3377-3385
pubmed: 34251190
Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Mar;67(3 Pt 1):031910
pubmed: 12689104
J Chem Phys. 2007 Jan 7;126(1):014101
pubmed: 17212484
Nat Commun. 2017 Sep 19;8(1):594
pubmed: 28928362
Proc Natl Acad Sci U S A. 2002 Apr 30;99 Suppl 2:6460-5
pubmed: 11959907
Molecules. 2020 Jun 05;25(11):
pubmed: 32517041
Proteins. 2010 Jun;78(8):1950-8
pubmed: 20408171
J Thromb Haemost. 2009 Dec;7(12):2096-105
pubmed: 19817991
Nat Commun. 2013;4:1333
pubmed: 23299883