title: Subunit folds and maturation pathway of a dsRNA virus capsid.
abstract: The cystovirus ϕ6 shares several distinct features with other double-stranded RNA (dsRNA) viruses, including the human pathogen, rotavirus: segmented genomes, nonequivalent packing of 120 subunits in its icosahedral capsid, and capsids as compartments for transcription and replication. ϕ6 assembles as a dodecahedral procapsid that undergoes major conformational changes as it matures into the spherical capsid. We determined the crystal structure of the capsid protein, P1, revealing a flattened trapezoid subunit with an α-helical fold. We also solved the procapsid with cryo-electron microscopy to comparable resolution. Fitting the crystal structure into the procapsid disclosed substantial conformational differences between the two P1 conformers. Maturation via two intermediate states involves remodeling on a similar scale, besides huge rigid-body rotations. The capsid structure and its stepwise maturation that is coupled to sequential packaging of three RNA segments sets the cystoviruses apart from other dsRNA viruses as a dynamic molecular machine.
authors.affiliation: National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, 50 South Drive, Bethesda, MD 20892, USA.
authors.forename: Daniel
authors.initials: D
authors.lastname: Nemecek
authors.forename: Evzen
authors.initials: E
authors.lastname: Boura
authors.forename: Weimin
authors.initials: W
authors.lastname: Wu
authors.forename: Naiqian
authors.initials: N
authors.lastname: Cheng
authors.forename: Pavel
authors.initials: P
authors.lastname: Plevka
authors.forename: Jian
authors.initials: J
authors.lastname: Qiao
authors.forename: Leonard
authors.initials: L
authors.lastname: Mindich
authors.forename: J Bernard
authors.initials: JB
authors.lastname: Heymann
authors.forename: James H
authors.initials: JH
authors.lastname: Hurley
authors.forename: Alasdair C
authors.initials: AC
authors.lastname: Steven
mesh_terms: D017126:Bacteriophage phi 6 / Q000502:physiology / Q000648:ultrastructure*; D002213:Capsid / Q000648:ultrastructure; D036022:Capsid Proteins / Q000737:chemistry*; D020285:Cryoelectron Microscopy; D018360:Crystallography, X-Ray; D008958:Models, Molecular; D017510:Protein Folding; D020836:Protein Structure, Quaternary; D017433:Protein Structure, Secondary; D021122:Protein Subunits / Q000737:chemistry*; D019065:Virus Assembly
chemical_list: D036022:Capsid Proteins; D021122:Protein Subunits
references.citation: Structure. 2005 Mar;13(3):473-82
references.pmid: 15766548
references.citation: J Struct Biol. 1999 Dec 1;128(1):82-97
references.pmid: 10600563
references.citation: Proc Natl Acad Sci U S A. 1990 Dec;87(23):9173-7
references.pmid: 2251260
references.citation: Nature. 1998 Oct 1;395(6701):470-8
references.pmid: 9774103
references.citation: Science. 2000 Sep 22;289(5487):2129-33
references.pmid: 11000116
references.citation: Biochemistry. 2002 Oct 8;41(40):11946-53
references.pmid: 12356294
references.citation: J Virol. 1992 Aug;66(8):5013-7
references.pmid: 1629962
references.citation: Methods Mol Biol. 2010;673:157-73
references.pmid: 20835797
references.citation: J Mol Biol. 2008 Oct 3;382(2):402-22
references.pmid: 18647606
references.citation: J Mol Biol. 1999 Nov 26;294(2):357-72
references.pmid: 10610764
references.citation: Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4074-9
references.pmid: 9108107
references.citation: Nucleic Acids Res. 2010 Jul;38(Web Server issue):W545-9
references.pmid: 20457744
references.citation: Cell. 2004 Sep 17;118(6):743-55
references.pmid: 15369673
references.citation: J Struct Biol. 2013 Jan;181(1):53-60
references.pmid: 23079477
references.citation: J Virol. 2002 Oct;76(20):10122-7
references.pmid: 12239286
references.citation: Curr Opin Struct Biol. 2005 Dec;15(6):655-63
references.pmid: 16271469
references.citation: J Bacteriol. 2003 Aug;185(15):4572-7
references.pmid: 12867467
references.citation: J Bacteriol. 2003 Nov;185(21):6409-14
references.pmid: 14563876
references.citation: Methods. 2009 Oct;49(2):174-80
references.pmid: 19398010
references.citation: J Mol Biol. 2008 Nov 14;383(3):529-38
references.pmid: 18793644
references.citation: J Comput Chem. 2004 Oct;25(13):1605-12
references.pmid: 15264254
references.citation: J Struct Biol. 2010 Sep;171(3):389-96
references.pmid: 20538059
references.citation: Cell. 2005 Mar 25;120(6):761-72
references.pmid: 15797378
references.citation: EMBO J. 1997 Jul 16;16(14):4477-87
references.pmid: 9250692
references.citation: Virology. 1994 Jul;202(1):258-63
references.pmid: 8009837
references.citation: Methods Enzymol. 1997;276:307-26
references.pmid: 27754618
references.citation: J Virol. 2012 Nov;86(21):11616-24
references.pmid: 22896624
references.citation: Adv Exp Med Biol. 2012;726:379-402
references.pmid: 22297523
references.citation: Structure. 2007 Feb;15(2):157-67
references.pmid: 17292834
references.citation: J Biol Chem. 2008 May 2;283(18):12227-31
references.pmid: 18287088
references.citation: J Mol Biol. 1995 Feb 24;246(3):418-28
references.pmid: 7877165
references.citation: Nature. 2009 Apr 2;458(7238):646-50
references.pmid: 19204733
references.citation: Structure. 2003 Oct;11(10):1227-38
references.pmid: 14527391
references.citation: Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):233-4
references.pmid: 21460440
references.citation: Microbiol Mol Biol Rev. 1999 Mar;63(1):149-60
references.pmid: 10066834
references.citation: Nat Protoc. 2010 Sep;5(10):1697-708
references.pmid: 20885381
references.citation: Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):328-35
references.pmid: 22505253
references.citation: PLoS One. 2012;7(10):e47489
references.pmid: 23077625
references.citation: Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
references.pmid: 15572765
references.citation: J Virol. 2012 Nov;86(22):12208-16
references.pmid: 22933292
references.citation: Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
references.pmid: 20124702
references.citation: Science. 2001 Apr 27;292(5517):744-8
references.pmid: 11326105
references.citation: J Struct Biol. 2007 Jan;157(1):3-18
references.pmid: 17011211
references.citation: Nat Struct Biol. 2002 Oct;9(10):725-8
references.pmid: 12244300
references.citation: J Mol Biol. 2011 Nov 25;414(2):260-71
references.pmid: 22019738
references.citation: Nature. 2001 Mar 8;410(6825):235-40
references.pmid: 11242087
references.citation: Structure. 2006 Jun;14(6):1039-48
references.pmid: 16765897
references.citation: Adv Virus Res. 1999;53:341-53
references.pmid: 10582106
references.citation: Nature. 2000 Apr 27;404(6781):960-7
references.pmid: 10801118
references.citation: Curr Biol. 2006 Jan 10;16(1):R11-3
references.pmid: 16401408
references.citation: J Struct Biol. 2012 Jun;178(3):215-24
references.pmid: 22508104
references.citation: EMBO J. 2009 Jun 3;28(11):1655-65
references.pmid: 19407816
references.citation: Cell. 2000 Jan 21;100(2):253-63
references.pmid: 10660048