Home LiteratureArticle Details
PMID: 9971781 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

ATP depletion blocks herpes simplex virus DNA packaging and capsid maturation.

Journal of virology ·Vol. 73 ·No. 3 ·1999-03-00 ·Pages 2006-15

Dasgupta A, Wilson DW

Abstract

During herpes simplex virus (HSV) assembly, immature procapsids must expel their internal scaffold proteins, transform their outer shell to form mature polyhedrons, and become packaged with the viral double-stranded (ds) DNA genome. A large number of virally encoded proteins are required for successful completion of these events, but their molecular roles are poorly understood. By analogy with the dsDNA bacteriophage we reasoned that HSV DNA packaging might be an ATP-requiring process and tested this hypothesis by adding an ATP depletion cocktail to cells accumulating unpackaged procapsids due to the presence of a temperature-sensitive lesion in the HSV maturational protease UL26. Following return to permissive temperature, HSV capsids were found to be unable to package DNA, suggesting that this process is indeed ATP dependent. Surprisingly, however, the display of epitopes indicative of capsid maturation was also inhibited. We conclude that either formation of these epitopes directly requires ATP or capsid maturation is normally arrested by a proofreading mechanism until DNA packaging has been successfully completed.

MeSH Terms
Adenosine Triphosphate/physiology Animals Capsid/physiology Chlorocebus aethiops DNA, Viral/physiology Simplexvirus/physiology Vero Cells Virus Assembly
Chemicals
DNA, Viral Adenosine Triphosphate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Dasgupta A
Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, Bronx, New York 10461, USA.
Wilson D W
References (54)
54 references, click to expand
  1. Distinct monoclonal antibodies separately label the hexons or the pentons of herpes simplex virus capsid.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11508-12 PMID: 1280828
  2. Processing of the herpes simplex virus assembly protein ICP35 near its carboxy terminal end requires the product of the whole of the UL26 reading frame.
    Virology. 1992 Jan;186(1):87-98 PMID: 1309284
  3. Differentiation of multiple domains in the herpes simplex virus 1 protease encoded by the UL26 gene.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2076-80 PMID: 1312713
  4. Identification of genes encoding two capsid proteins (VP24 and VP26) of herpes simplex virus type 1.
    J Gen Virol. 1992 Oct;73 ( Pt 10):2709-13 PMID: 1328483
  5. The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate.
    J Virol. 1991 Oct;65(10):5149-56 PMID: 1654435
  6. Sequence analysis of the splice junction in the transcript of herpes simplex virus type 1 gene UL15.
    Virus Res. 1991 Jun;20(1):97-104 PMID: 1656627
  7. Channel catfish virus: a new type of herpesvirus.
    Virology. 1992 Jan;186(1):9-14 PMID: 1727613
  8. The herpes simplex virus UL33 gene product is required for the assembly of full capsids.
    Virology. 1991 Jan;180(1):380-8 PMID: 1845831
  9. 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
  10. Use of Ar+ plasma etching to localize structural proteins in the capsid of herpes simplex virus type 1.
    J Virol. 1989 Nov;63(11):4697-702 PMID: 2552147
  11. DNA packaging in dsDNA bacteriophages.
    Annu Rev Microbiol. 1989;43:267-92 PMID: 2679356
  12. The products of herpes simplex virus type 1 gene UL26 which are involved in DNA packaging are strongly associated with empty but not with full capsids.
    J Gen Virol. 1988 Nov;69 ( Pt 11):2879-91 PMID: 2846764
  13. Identification and characterization of a herpes simplex virus gene product required for encapsidation of virus DNA.
    J Virol. 1983 Mar;45(3):1056-64 PMID: 6300447
  14. Characterization of post-translational products of herpes simplex virus gene 35 proteins binding to the surfaces of full capsids but not empty capsids.
    J Virol. 1984 Jan;49(1):142-53 PMID: 6317887
  15. Release of the catalytic domain N(o) from the herpes simplex virus type 1 protease is required for viral growth.
    J Virol. 1995 Nov;69(11):7113-21 PMID: 7474131
  16. Herpes simplex virus capsids assembled in insect cells infected with recombinant baculoviruses: structural authenticity and localization of VP26.
    J Virol. 1995 Nov;69(11):7362-6 PMID: 7474170
  17. Assembly of the herpes simplex virus capsid: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes.
    J Virol. 1995 Jun;69(6):3690-703 PMID: 7745718
  18. Fusion of cationic liposomes with mammalian cells occurs after endocytosis.
    Biochim Biophys Acta. 1995 May 4;1235(2):296-304 PMID: 7756338
  19. The C-terminal 25 amino acids of the protease and its substrate ICP35 of herpes simplex virus type 1 are involved in the formation of sealed capsids.
    J Virol. 1995 Jul;69(7):4347-56 PMID: 7769696
  20. A eukaryotic cytosolic chaperonin is associated with a high molecular weight intermediate in the assembly of hepatitis B virus capsid, a multimeric particle.
    J Cell Biol. 1994 Apr;125(1):99-111 PMID: 7908022
  21. Protein subunit structures in the herpes simplex virus A-capsid determined from 400 kV spot-scan electron cryomicroscopy.
    J Mol Biol. 1994 Sep 30;242(4):456-69 PMID: 7932703
  22. The herpes simplex virus 1 UL15 gene encodes two proteins and is required for cleavage of genomic viral DNA.
    J Virol. 1994 Dec;68(12):8118-24 PMID: 7966602
  23. Phenotype of the herpes simplex virus type 1 protease substrate ICP35 mutant virus.
    J Virol. 1994 Sep;68(9):5384-94 PMID: 8057422
  24. Cell-free assembly of the herpes simplex virus capsid.
    J Virol. 1994 Sep;68(9):6059-63 PMID: 8057482
  25. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins.
    J Virol. 1994 Apr;68(4):2442-57 PMID: 8139029
  26. Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses.
    J Gen Virol. 1994 May;75 ( Pt 5):1101-13 PMID: 8176371
  27. The protease of herpes simplex virus type 1 is essential for functional capsid formation and viral growth.
    J Virol. 1994 Jun;68(6):3702-12 PMID: 8189508
  28. 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
  29. Kinetic characterization of the ATPase activity of the DNA packaging enzyme from bacteriophage lambda.
    Biochemistry. 1993 Nov 16;32(45):11992-7 PMID: 8218275
  30. Characterization of a temperature-sensitive mutant of the UL15 open reading frame of herpes simplex virus 1.
    J Virol. 1993 Aug;67(8):4497-503 PMID: 8331721
  31. Characterization of the protease and other products of amino-terminus-proximal cleavage of the herpes simplex virus 1 UL26 protein.
    J Virol. 1993 Mar;67(3):1300-9 PMID: 8382296
  32. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA.
    J Virol. 1993 Mar;67(3):1357-64 PMID: 8382300
  33. Herpes simplex virus type 1 DNA cleavage and encapsidation require the product of the UL28 gene: isolation and characterization of two UL28 deletion mutants.
    J Virol. 1993 Jun;67(6):3470-80 PMID: 8388510
  34. Herpes simplex virus type 1 capsid protein, VP21, originates within the UL26 open reading frame.
    J Gen Virol. 1993 Oct;74 ( Pt 10):2269-73 PMID: 8409950
  35. Virus DNA packaging: the strategy used by phage lambda.
    Mol Microbiol. 1995 Jun;16(6):1075-86 PMID: 8577244
  36. Isolation and characterization of herpes simplex virus type 1 mutants defective in the UL6 gene.
    Virology. 1996 Mar 1;217(1):111-23 PMID: 8599195
  37. The distal pathway of lipoprotein-induced cholesterol esterification, but not sphingomyelinase-induced cholesterol esterification, is energy-dependent.
    J Biol Chem. 1996 Jun 7;271(23):13392-400 PMID: 8662777
  38. Separate functional domains of the herpes simplex virus type 1 protease: evidence for cleavage inside capsids.
    J Virol. 1996 Jul;70(7):4317-28 PMID: 8676454
  39. 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
  40. The herpes simplex virus procapsid: structure, conformational changes upon maturation, and roles of the triplex proteins VP19c and VP23 in assembly.
    J Mol Biol. 1996 Nov 1;263(3):447-62 PMID: 8918600
  41. The herpes simplex virus type 1 UL6 protein is essential for cleavage and packaging but not for genomic inversion.
    Virology. 1996 Dec 15;226(2):403-7 PMID: 8955060
  42. Characterization of ICP6::lacZ insertion mutants of the UL15 gene of herpes simplex virus type 1 reveals the translation of two proteins.
    J Virol. 1997 Apr;71(4):2656-65 PMID: 9060618
  43. The U(L)15 gene of herpes simplex virus type 1 contains within its second exon a novel open reading frame that is translated in frame with the U(L)15 gene product.
    J Virol. 1997 Apr;71(4):2666-73 PMID: 9060619
  44. Study of herpes simplex virus maturation during a synchronous wave of assembly.
    J Virol. 1997 May;71(5):3603-12 PMID: 9094633
  45. Structure of the herpes simplex virus capsid: peptide A862-H880 of the major capsid protein is displayed on the rim of the capsomer protrusions.
    Virology. 1997 Feb 17;228(2):229-35 PMID: 9123829
  46. Hexon-only binding of VP26 reflects differences between the hexon and penton conformations of VP5, the major capsid protein of herpes simplex virus.
    J Virol. 1997 Dec;71(12):8955-61 PMID: 9371551
  47. 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
  48. The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments.
    J Virol. 1998 Mar;72(3):2463-73 PMID: 9499108
  49. Herpes simplex virus DNA packaging without measurable DNA synthesis.
    J Virol. 1998 Apr;72(4):2745-51 PMID: 9525593
  50. Herpes simplex virus DNA cleavage and packaging: association of multiple forms of U(L)15-encoded proteins with B capsids requires at least the U(L)6, U(L)17, and U(L)28 genes.
    J Virol. 1998 Apr;72(4):3045-50 PMID: 9525627
  51. Type D retrovirus capsid assembly and release are active events requiring ATP.
    J Virol. 1998 Apr;72(4):3098-106 PMID: 9525635
  52. Genetic analysis of the UL 15 gene locus for the putative terminase of herpes simplex virus type 1.
    Virology. 1998 Mar 30;243(1):32-44 PMID: 9527913
  53. 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
  54. Herpes simplex virus type 1 cleavage and packaging proteins UL15 and UL28 are associated with B but not C capsids during packaging.
    J Virol. 1998 Sep;72(9):7428-39 PMID: 9696839
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/JVI.73.3.2006-2015.1999
Published
1999-03-00
Pages
2006-15
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC104443
Subset
IM
Grants
NCI NIH HHS · P30 CA013330 · United States
NIAID NIH HHS · R01 AI038265 · United States
NIAID NIH HHS · AI38265 · United States
NCI NIH HHS · P30-CA13330 · United States
External Links
PubMed source DOI: 10.1128/JVI.73.3.2006-2015.1999 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2