Home LiteratureArticle Details
PMID: 19487681 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids.

Roos WH, Radtke K, Kniesmeijer E, Geertsema H, Sodeik B, Wuite GJ

Abstract

Herpes simplex virus type 1 (HSV1) capsids undergo extensive structural changes during maturation and DNA packaging. As a result, they become more stable and competent for nuclear egress. To further elucidate this stabilization process, we used biochemical and nanoindentation approaches to analyze the structural and mechanical properties of scaffold-containing (B), empty (A), and DNA-containing (C) nuclear capsids. Atomic force microscopy experiments revealed that A and C capsids were mechanically indistinguishable, indicating that the presence of DNA does not account for changes in mechanical properties during capsid maturation. Despite having the same rigidity, the scaffold-containing B capsids broke at significantly lower forces than A and C capsids. An extraction of pentons with guanidine hydrochloride (GuHCl) increased the flexibility of all capsids. Surprisingly, the breaking forces of the modified A and C capsids dropped to similar values as those of the GuHCl-treated B capsids, indicating that mechanical reinforcement occurs at the vertices. Nonetheless, it also showed that HSV1 capsids possess a remarkable structural integrity that was preserved after removal of pentons. We suggest that HSV1 capsids are stabilized after removal of the scaffold proteins, and that this stabilization is triggered by the packaging of DNA, but independent of the actual presence of DNA.

MeSH Terms
Animals Blotting, Western Capsid Cell Line Cricetinae DNA, Viral/genetics Electrophoresis, Polyacrylamide Gel Genome, Viral Herpesvirus 1, Human/genetics Microscopy, Atomic Force Polymerase Chain Reaction Virus Assembly
Chemicals
DNA, Viral
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Roos Wouter H
Natuur en Sterrenkunde, Vrije Universiteit, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands.
Radtke Kerstin
Kniesmeijer Edward
Geertsema Hylkje
Sodeik Beate
Wuite Gijs J L
References (52)
52 references, click to expand
  1. Forces during bacteriophage DNA packaging and ejection.
    Biophys J. 2005 Feb;88(2):851-66 PMID: 15556983
  2. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  3. Rapid quantitative PCR assays for the simultaneous detection of herpes simplex virus, varicella zoster virus, cytomegalovirus, Epstein-Barr virus, and human herpesvirus 6 DNA in blood and other clinical specimens.
    J Med Virol. 2008 Mar;80(3):467-77 PMID: 18205230
  4. Biochemical studies of the maturation of herpesvirus nucleocapsid species.
    Virology. 1976 Oct 1;74(1):194-208 PMID: 18625460
  5. Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro.
    Mol Cell Biol. 2000 Jul;20(13):4922-31 PMID: 10848617
  6. Capsid assembly and DNA packaging in herpes simplex virus.
    Rev Med Virol. 1997 Jul;7(2):107-122 PMID: 10398476
  7. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids.
    Mol Cell. 2007 May 25;26(4):479-89 PMID: 17531807
  8. Characterization of three species of nucleocapsids of equine herpesvirus type-1 (EHV-1).
    Virology. 1975 Mar;64(1):187-204 PMID: 1167720
  9. The pseudorabies virus UL28 protein enters the nucleus after coexpression with the herpes simplex virus UL15 protein.
    J Virol. 1997 Dec;71(12):9118-23 PMID: 9371568
  10. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid.
    J Virol. 2001 Nov;75(22):10923-32 PMID: 11602732
  11. Manipulation of the mechanical properties of a virus by protein engineering.
    Proc Natl Acad Sci U S A. 2008 Mar 18;105(11):4150-5 PMID: 18334651
  12. Common ancestry of herpesviruses and tailed DNA bacteriophages.
    J Virol. 2005 Dec;79(23):14967-70 PMID: 16282496
  13. Hexavalent capsomers of herpes simplex virus type 2: symmetry, shape, dimensions, and oligomeric status.
    J Virol. 1986 Feb;57(2):578-84 PMID: 3003389
  14. Structural transitions during maturation of bacteriophage lambda capsids.
    J Mol Biol. 1993 Oct 20;233(4):682-94 PMID: 8411174
  15. Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices.
    J Virol. 2006 Jul;80(13):6286-94 PMID: 16775316
  16. Structural analysis of the capsid polypeptides of herpes simplex virus types 1 and 2.
    J Virol. 1980 May;34(2):521-31 PMID: 6154808
  17. Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus.
    Cell. 1991 Mar 8;64(5):1007-15 PMID: 1848156
  18. Bacteriophage capsids: tough nanoshells with complex elastic properties.
    Proc Natl Acad Sci U S A. 2004 May 18;101(20):7600-5 PMID: 15133147
  19. Structure of the herpes simplex virus capsid. Molecular composition of the pentons and the triplexes.
    J Mol Biol. 1993 Jul 20;232(2):499-511 PMID: 8393939
  20. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro.
    Traffic. 2006 Feb;7(2):227-37 PMID: 16420530
  21. Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid.
    J Virol. 1998 Sep;72(9):7563-8 PMID: 9696854
  22. Influence of nonuniform geometry on nanoindentation of viral capsids.
    Biophys J. 2008 Oct;95(8):3640-9 PMID: 18621831
  23. Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS.
    J Virol. 2001 Nov;75(22):10755-65 PMID: 11602717
  24. Partial functional complementation of a pseudorabies virus UL25 deletion mutant by herpes simplex virus type 1 pUL25 indicates overlapping functions of alphaherpesvirus pUL25 proteins.
    J Virol. 2008 Jun;82(12):5725-34 PMID: 18400859
  25. Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms.
    Cell Mol Life Sci. 2007 Jun;64(12):1484-97 PMID: 17440680
  26. Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice.
    Virology. 1998 Jul 20;247(1):115-24 PMID: 9683577
  27. pH reduction as a trigger for dissociation of herpes simplex virus type 1 scaffolds.
    J Virol. 2002 Aug;76(15):7407-17 PMID: 12097553
  28. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity.
    Curr Opin Struct Biol. 2005 Apr;15(2):227-36 PMID: 15837183
  29. Induced extrusion of DNA from the capsid of herpes simplex virus type 1.
    J Virol. 1994 Jan;68(1):433-40 PMID: 8254753
  30. Characterization of intranuclear capsids made by ts morphogenic mutants of HSV-1.
    Virology. 1988 Apr;163(2):471-80 PMID: 2833020
  31. Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids.
    Nat Struct Biol. 1995 Nov;2(11):1026-30 PMID: 7583656
  32. The herpes simplex virus type 1 DNA packaging protein UL17 is a virion protein that is present in both the capsid and the tegument compartments.
    J Virol. 2005 Jan;79(1):150-8 PMID: 15596811
  33. DNA-mediated anisotropic mechanical reinforcement of a virus.
    Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13706-11 PMID: 16945903
  34. Mechanical properties of murine leukemia virus particles: effect of maturation.
    Biophys J. 2006 Jul 15;91(2):767-74 PMID: 16632508
  35. Identification, subviral localization, and functional characterization of the pseudorabies virus UL17 protein.
    J Virol. 2005 Nov;79(21):13442-53 PMID: 16227265
  36. Herpes simplex virus type 1 tegument proteins VP1/2 and UL37 are associated with intranuclear capsids.
    Virology. 2007 May 10;361(2):316-24 PMID: 17223150
  37. Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids.
    J Virol. 1991 Feb;65(2):613-20 PMID: 1846187
  38. Eclipse phase of herpes simplex virus type 1 infection: Efficient dynein-mediated capsid transport without the small capsid protein VP26.
    J Virol. 2006 Aug;80(16):8211-24 PMID: 16873277
  39. Identification and characterization of the herpes simplex virus type 1 virion protein encoded by the UL35 open reading frame.
    J Virol. 1992 May;66(5):2653-63 PMID: 1313892
  40. Topics in herpesvirus genomics and evolution.
    Virus Res. 2006 Apr;117(1):90-104 PMID: 16490275
  41. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids.
    Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9216-20 PMID: 18587050
  42. Internal DNA pressure modifies stability of WT phage.
    Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9603-8 PMID: 17535894
  43. Nonlinear finite-element analysis of nanoindentation of viral capsids.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2007 Mar;75(3 Pt 1):031901 PMID: 17500720
  44. Finding a needle in a haystack: detection of a small protein (the 12-kDa VP26) in a large complex (the 200-MDa capsid of herpes simplex virus).
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5652-6 PMID: 8202543
  45. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA.
    J Virol. 1998 Feb;72(2):1060-70 PMID: 9445000
  46. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength.
    Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6184-9 PMID: 16606825
  47. A stiffness switch in human immunodeficiency virus.
    Biophys J. 2007 Mar 1;92(5):1777-83 PMID: 17158573
  48. Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids.
    J Virol. 2006 Mar;80(5):2118-26 PMID: 16474120
  49. Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy.
    Nat Struct Biol. 2003 May;10(5):334-41 PMID: 12704429
  50. Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation.
    J Mol Biol. 1996 Nov 1;263(3):432-46 PMID: 8918599
  51. The herpes simplex virus type 1 U(L)17 gene encodes virion tegument proteins that are required for cleavage and packaging of viral DNA.
    J Virol. 1998 May;72(5):3779-88 PMID: 9557660
  52. Exceptional mechanical and structural stability of HSV-1 unveiled with fluid atomic force microscopy.
    J Cell Sci. 2008 Jul 15;121(Pt 14):2287-92 PMID: 18559888
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-06-16
Epub
2009-00-01
Pages
9673-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2700990
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com