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PMID: 16216585 Published · ppublish English Comparative Study 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. Research Support, U.S. Gov't, P.H.S.

Features of reovirus outer capsid protein mu1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Angstrom resolution.

Structure (London, England : 1993) ·Vol. 13 ·No. 10 ·2005-10-00 ·Pages 1545-57

Zhang X, Ji Y, Zhang L, Harrison SC, Marinescu DC, Nibert ML, Baker TS

Abstract

Reovirus is a useful model for addressing the molecular basis of membrane penetration by one of the larger nonenveloped animal viruses. We now report the structure of the reovirus virion at approximately 7.0 A resolution as obtained by electron cryomicroscopy and three-dimensional image reconstruction. Several features of the myristoylated outer capsid protein mu1, not seen in a previous X-ray crystal structure of the mu1-sigma3 heterohexamer, are evident in the virion. These features appear to be important for stabilizing the outer capsid, regulating the conformational changes in mu1 that accompany perforation of target membranes, and contributing directly to membrane penetration during cell entry.

MeSH Terms
Algorithms Amino Acid Sequence Animals Capsid Proteins/chemistry,isolation & purification,ultrastructure Cryoelectron Microscopy Crystallography, X-Ray Fourier Analysis L Cells Mice Models, Chemical Models, Molecular Molecular Sequence Data Myristic Acid/metabolism Orthoreovirus/chemistry,genetics,ultrastructure Protein Conformation Protein Structure, Secondary Sequence Homology, Amino Acid Virion/growth & development,ultrastructure
Chemicals
Capsid Proteins Myristic Acid
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Zhang Xing
Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, USA.
Ji Yongchang
Zhang Lan
Harrison Stephen C
Marinescu Dan C
Nibert Max L
Baker Timothy S
References (52)
52 references, click to expand
  1. Sequences of avian reovirus M1, M2 and M3 genes and predicted structure/function of the encoded mu proteins.
    Virus Res. 2006 Mar;116(1-2):45-57 PMID: 16297481
  2. Digestion pattern of reovirus outer capsid protein sigma3 determined by mass spectrometry.
    Virology. 2003 Jul 5;311(2):289-304 PMID: 12842619
  3. Characterization of anti-reovirus immunoglobulins secreted by cloned hybridoma cell lines.
    Virology. 1981 Jan 15;108(1):134-46 PMID: 7269233
  4. Multi-resolution contour-based fitting of macromolecular structures.
    J Mol Biol. 2002 Mar 29;317(3):375-84 PMID: 11922671
  5. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction.
    J Cell Biol. 1993 Sep;122(5):1023-41 PMID: 8394844
  6. Disulfide bonding among micro 1 trimers in mammalian reovirus outer capsid: a late and reversible step in virion morphogenesis.
    J Virol. 2003 May;77(9):5389-400 PMID: 12692241
  7. Animal cell invasion by a large nonenveloped virus: reovirus delivers the goods.
    Trends Microbiol. 2003 Aug;11(8):374-82 PMID: 12915095
  8. Transcriptional activities of reovirus RNA polymerase in recoated cores. Initiation and elongation are regulated by separate mechanisms.
    J Biol Chem. 2000 Dec 15;275(50):39693-701 PMID: 11007773
  9. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy.
    J Mol Biol. 2003 Oct 31;333(4):721-45 PMID: 14568533
  10. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles.
    J Virol. 1988 Jan;62(1):246-56 PMID: 3275434
  11. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption.
    J Virol. 2002 Oct;76(19):9920-33 PMID: 12208969
  12. Pathogenesis of viral infections. Basic concepts derived from the reovirus model.
    N Engl J Med. 1985 Feb 21;312(8):486-97 PMID: 2982096
  13. Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae).
    J Gen Virol. 2002 Aug;83(Pt 8):1941-51 PMID: 12124458
  14. Combining electron microscopic with x-ray crystallographic structures.
    J Struct Biol. 2001 Dec;136(3):190-200 PMID: 12051899
  15. Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses.
    J Virol. 2001 Dec;75(24):11943-7 PMID: 11711584
  16. Seeing the herpesvirus capsid at 8.5 A.
    Science. 2000 May 5;288(5467):877-80 PMID: 10797014
  17. A model-based parallel origin and orientation refinement algorithm for cryoTEM and its application to the study of virus structures.
    J Struct Biol. 2006 Apr;154(1):1-19 PMID: 16459100
  18. Mammalian reoviruses contain a myristoylated structural protein.
    J Virol. 1991 Apr;65(4):1960-7 PMID: 2002551
  19. Putative autocleavage of outer capsid protein micro1, allowing release of myristoylated peptide micro1N during particle uncoating, is critical for cell entry by reovirus.
    J Virol. 2004 Aug;78(16):8732-45 PMID: 15280481
  20. Reovirus receptors and pathogenesis.
    J Virol. 2003 Sep;77(17):9109-15 PMID: 12915527
  21. Loss of activities for mRNA synthesis accompanies loss of lambda2 spikes from reovirus cores: an effect of lambda2 on lambda1 shell structure.
    Virology. 2002 Apr 25;296(1):24-38 PMID: 12036315
  22. Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization.
    J Mol Biol. 2005 Jan 21;345(3):461-74 PMID: 15581891
  23. RNA synthesis in a cage--structural studies of reovirus polymerase lambda3.
    Cell. 2002 Nov 27;111(5):733-45 PMID: 12464184
  24. Thermostability of reovirus disassembly intermediates (ISVPs) correlates with genetic, biochemical, and thermodynamic properties of major surface protein mu1.
    J Virol. 2002 Feb;76(3):1051-61 PMID: 11773381
  25. Polypeptide components of virions, top component and cores of reovirus type 3.
    Virology. 1969 Dec;39(4):791-810 PMID: 4311639
  26. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  27. Not your average density.
    Structure. 1997 Dec 15;5(12):1557-69 PMID: 9438862
  28. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs.
    Microbiol Mol Biol Rev. 1999 Dec;63(4):862-922, table of contents PMID: 10585969
  29. Assembly of the reovirus outer capsid requires mu 1/sigma 3 interactions which are prevented by misfolded sigma 3 protein in temperature-sensitive mutant tsG453.
    Virus Res. 1996 Dec;46(1-2):19-29 PMID: 9029774
  30. Structure of the reovirus membrane-penetration protein, Mu1, in a complex with is protector protein, Sigma3.
    Cell. 2002 Jan 25;108(2):283-95 PMID: 11832217
  31. Crystal structure of reovirus attachment protein sigma1 reveals evolutionary relationship to adenovirus fiber.
    EMBO J. 2002 Jan 15;21(1-2):1-11 PMID: 11782420
  32. Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus.
    Nat Struct Biol. 2001 Oct;8(10):868-73 PMID: 11573092
  33. Three-dimensional structure of halorhodopsin at 7 A resolution.
    J Mol Biol. 1995 Apr 7;247(4):726-38 PMID: 7723027
  34. Software for handling macromolecular envelopes.
    Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):941-4 PMID: 10089342
  35. In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins mu1 and sigma3.
    J Virol. 1999 May;73(5):3941-50 PMID: 10196289
  36. Structure of the reovirus core at 3.6 A resolution.
    Nature. 2000 Apr 27;404(6781):960-7 PMID: 10801118
  37. The delta region of outer-capsid protein micro 1 undergoes conformational change and release from reovirus particles during cell entry.
    J Virol. 2003 Dec;77(24):13361-75 PMID: 14645591
  38. Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 A.
    Nat Struct Biol. 2003 Dec;10(12):1011-8 PMID: 14608373
  39. A single mutation in the carboxy terminus of reovirus outer-capsid protein sigma 3 confers enhanced kinetics of sigma 3 proteolysis, resistance to inhibitors of viral disassembly, and alterations in sigma 3 structure.
    J Virol. 2002 Oct;76(19):9832-43 PMID: 12208961
  40. Complete in vitro assembly of the reovirus outer capsid produces highly infectious particles suitable for genetic studies of the receptor-binding protein.
    J Virol. 2001 Jun;75(11):5335-42 PMID: 11333914
  41. Reovirus polypeptide sigma 3 and N-terminal myristoylation of polypeptide mu 1 are required for site-specific cleavage to mu 1C in transfected cells.
    J Virol. 1992 Apr;66(4):2180-6 PMID: 1548757
  42. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  43. Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein-protein interfaces.
    Virus Res. 2004 Apr;101(1):15-28 PMID: 15010214
  44. The three-dimensional structure of reovirus obtained by cryo-electron microscopy.
    EMBO J. 1991 Nov;10(11):3129-36 PMID: 1915287
  45. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions.
    Nat Struct Biol. 2003 Feb;10(2):131-5 PMID: 12536205
  46. Realizing the potential of electron cryo-microscopy.
    Q Rev Biophys. 2004 Feb;37(1):3-13 PMID: 17390603
  47. Molecular model for a complete clathrin lattice from electron cryomicroscopy.
    Nature. 2004 Dec 2;432(7017):573-9 PMID: 15502812
  48. Reoviruses and the host cell.
    Trends Microbiol. 2001 Nov;9(11):560-4 PMID: 11825717
  49. Internal/structures containing transcriptase-related proteins in top component particles of mammalian orthoreovirus.
    Virology. 1998 May 25;245(1):33-46 PMID: 9614865
  50. A monoclonal antibody specific for reovirus outer-capsid protein sigma3 inhibits sigma1-mediated hemagglutination by steric hindrance.
    J Virol. 2001 Jul;75(14):6625-34 PMID: 11413330
  51. Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host.
    J Clin Invest. 1991 Sep;88(3):727-34 PMID: 1885768
  52. Viral and cellular mRNA capping: past and prospects.
    Adv Virus Res. 2000;55:135-84 PMID: 11050942
Article Info
Journal
Structure (London, England : 1993)
Abbr.
Structure
ISSN
0969-2126
Published
2005-10-00
Pages
1545-57
Language
English
Region
United States
NLM ID
101087697
PMCID
PMC4126556
Subset
IM
Grants
NIGMS NIH HHS · R37 GM033050 · United States
NIGMS NIH HHS · P01 GM062580 · United States
NIGMS NIH HHS · R01 GM033050 · United States
NCI NIH HHS · R37 CA013202 · United States
NIAID NIH HHS · P01 AI045976 · United States
NIAID NIH HHS · R01 AI046440 · United States
NIAID NIH HHS · R01 AI47904 · United States
NIGMS NIH HHS · R01 GM33050 · United States
NIAID NIH HHS · R01 AI46440 · United States
NCI NIH HHS · R01 CA013202 · United States
NIAID NIH HHS · R01 AI047904 · United States
NIGMS NIH HHS · R01 GM62580 · United States
NCI NIH HHS · R01 CA13202 · United States
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