Role of DNA-DNA sliding friction and nonequilibrium dynamics in viral genome ejection and packaging.
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
25 08 2023
25 08 2023
Historique:
accepted:
27
06
2023
revised:
17
06
2023
received:
04
04
2023
medline:
28
8
2023
pubmed:
14
7
2023
entrez:
14
7
2023
Statut:
ppublish
Résumé
Many viruses eject their DNA via a nanochannel in the viral shell, driven by internal forces arising from the high-density genome packing. The speed of DNA exit is controlled by friction forces that limit the molecular mobility, but the nature of this friction is unknown. We introduce a method to probe the mobility of the tightly confined DNA by measuring DNA exit from phage phi29 capsids with optical tweezers. We measure extremely low initial exit velocity, a regime of exponentially increasing velocity, stochastic pausing that dominates the kinetics and large dynamic heterogeneity. Measurements with variable applied force provide evidence that the initial velocity is controlled by DNA-DNA sliding friction, consistent with a Frenkel-Kontorova model for nanoscale friction. We confirm several aspects of the ejection dynamics predicted by theoretical models. Features of the pausing suggest that it is connected to the phenomenon of 'clogging' in soft matter systems. Our results provide evidence that DNA-DNA friction and clogging control the DNA exit dynamics, but that this friction does not significantly affect DNA packaging.
Identifiants
pubmed: 37449417
pii: 7224125
doi: 10.1093/nar/gkad582
pmc: PMC10450192
doi:
Substances chimiques
DNA, Viral
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
8060-8069Subventions
Organisme : NIH HHS
ID : T32 GM008326
Pays : United States
Commentaires et corrections
Type : UpdateOf
Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Methods Mol Biol. 2018;1805:393-422
pubmed: 29971729
Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):16868-73
pubmed: 17942694
Biophys J. 2008 Jun;94(11):4159-64
pubmed: 18192378
J Phys Chem B. 2016 Jul 7;120(26):5975-86
pubmed: 27152667
Polymers (Basel). 2019 Jan 07;11(1):
pubmed: 30960068
Phys Rev Lett. 2001 Jan 1;86(1):71-74
pubmed: 11136096
J Theor Biol. 1969 Jan;22(1):33-42
pubmed: 5797570
Biopolymers. 1978 Mar;17(3):785-94
pubmed: 638234
Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14675-80
pubmed: 25271319
Curr Biol. 2005 Mar 8;15(5):430-5
pubmed: 15753037
Biophys J. 2010 Jul 21;99(2):447-55
pubmed: 20643062
J Biomol Struct Dyn. 1992 Apr;9(5):911-20
pubmed: 1524706
Science. 2009 Mar 27;323(5922):1682-3
pubmed: 19325104
Nature. 2000 Dec 7;408(6813):745-50
pubmed: 11130079
Curr Opin Virol. 2011 Aug;1(2):134-41
pubmed: 22440623
Biophys J. 2006 Jul 15;91(2):411-20
pubmed: 16679360
Biophys J. 2003 Mar;84(3):1616-27
pubmed: 12609865
Curr Biol. 2012 Jul 24;22(14):1339-43
pubmed: 22727695
Phys Rev Lett. 2019 Dec 31;123(26):267801
pubmed: 31951464
Phys Rev E. 2021 Oct;104(4-1):044909
pubmed: 34781509
Phys Rev E Stat Nonlin Soft Matter Phys. 2014 Apr;89(4):042205
pubmed: 24827239
Cell. 1980 Sep;21(2):319-31
pubmed: 6447542
Nucleic Acids Res. 2016 Mar 18;44(5):2036-46
pubmed: 26883635
Biophys J. 2016 Oct 18;111(8):1604-1611
pubmed: 27760348
Biophys J. 2008 Jul;95(2):497-502
pubmed: 18487310
Annu Rev Virol. 2015 Nov;2(1):351-78
pubmed: 26958920
Adv Exp Med Biol. 2012;726:549-84
pubmed: 22297530
Appl Phys Lett. 2014 Apr 7;104(14):143701
pubmed: 25316922
Cell. 2014 Apr 24;157(3):702-713
pubmed: 24766813
Nucleic Acids Res. 2006 Feb 01;34(2):e15
pubmed: 16452295
Nat Mater. 2015 Jun;14(6):583-8
pubmed: 25730393
J Mol Biol. 2007 Nov 9;373(5):1113-22
pubmed: 17919653
Soft Matter. 2022 Sep 21;18(36):6987-6997
pubmed: 36069637
Nucleic Acids Res. 2017 Nov 2;45(19):11437-11448
pubmed: 28981683
Phys Rev E Stat Nonlin Soft Matter Phys. 2015 Dec;92(6):062715
pubmed: 26764735
Phys Rev Lett. 2009 Apr 10;102(14):148302
pubmed: 19392490
Proc Natl Acad Sci U S A. 2005 Jun 28;102(26):9165-9
pubmed: 15958528
Phys Rev Lett. 2021 Oct 1;127(14):148002
pubmed: 34652198
J Chem Phys. 2011 Sep 7;135(9):095101
pubmed: 21913781
Phys Rev E. 2017 May;95(5-1):052408
pubmed: 28618627
Langmuir. 2016 Feb 16;32(6):1478-88
pubmed: 26789199
Proc Natl Acad Sci U S A. 1981 Sep;78(9):5498-502
pubmed: 6272306
Soft Matter. 2016 Jun 14;12(22):5041-9
pubmed: 27181288
J Phys Chem B. 2016 Jul 7;120(26):6130-8
pubmed: 27063451
Phys Rev E. 2018 Feb;97(2-1):021102
pubmed: 29548190
Phys Rev Lett. 2009 Feb 27;102(8):088101
pubmed: 19257792
Proc Natl Acad Sci U S A. 2003 Mar 18;100(6):3173-8
pubmed: 12629206
Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13671-4
pubmed: 11707588
Methods Mol Biol. 2017;1486:343-355
pubmed: 27844435
Sci Rep. 2014 Dec 04;4:7324
pubmed: 25471601
J Mol Biol. 2008 Nov 14;383(3):520-8
pubmed: 18778713
Phys Rev Lett. 2000 Feb 7;84(6):1172-5
pubmed: 11017471
Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20081-6
pubmed: 24272939
J Am Chem Soc. 2022 Feb 2;144(4):1718-1728
pubmed: 35073489
Q Rev Biophys. 1978 May;11(2):179-246
pubmed: 353876
Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8345-50
pubmed: 24912187
Nature. 2001 Oct 18;413(6857):748-52
pubmed: 11607035
Nat Rev Microbiol. 2011 Aug 12;9(9):647-57
pubmed: 21836625
J Biol Phys. 2013 Mar;39(2):229-45
pubmed: 23860871
Phys Rev E. 2017 Nov;96(5-1):052402
pubmed: 29347730
Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5373-7
pubmed: 11959991
Proc Natl Acad Sci U S A. 1984 May;81(9):2621-5
pubmed: 6585818
Soft Matter. 2014 Sep 7;10(33):6303-15
pubmed: 25029591
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9292-5
pubmed: 12881484
Biochemistry. 1979 May 29;18(11):2192-6
pubmed: 444448
Philos Trans A Math Phys Eng Sci. 2004 Jul 15;362(1820):1497-517
pubmed: 15306463
Phys Rev Lett. 2011 Jan 14;106(2):028102
pubmed: 21405253
Biophys J. 2010 Aug 9;99(4):1101-9
pubmed: 20712993
Nucleic Acids Res. 2021 May 21;49(9):5143-5158
pubmed: 33905507
Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22269-74
pubmed: 20018693
Biophys J. 2015 Jan 20;108(2):315-24
pubmed: 25606680
Proc Natl Acad Sci U S A. 2018 Jul 31;115(31):7961-7966
pubmed: 30012596
Proc Natl Acad Sci U S A. 2007 Sep 11;104(37):14652-7
pubmed: 17804798
Phys Rev Lett. 2012 Dec 14;109(24):248105
pubmed: 23368388
Phys Rev Lett. 2012 Sep 14;109(11):118301
pubmed: 23005684
Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11245-50
pubmed: 17556543
Phys Rev Lett. 2006 May 26;96(20):208102
pubmed: 16803211
Elife. 2019 Aug 08;8:
pubmed: 31393262