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PMID: 10516054 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle.

Journal of virology ·Vol. 73 ·No. 11 ·1999-11-00 ·Pages 9456-67

Lomonte P, Everett RD

Abstract

Herpes simplex virus type 1 (HSV-1) immediate-early protein Vmw110 stimulates the onset of virus infection in a multiplicity-dependent manner and is required for efficient reactivation from latency. Recent work has shown that Vmw110 is able to interact with or modify the stability of several cellular proteins. In this report we analyze the ability of Vmw110 to inhibit the progression of cells through the cell cycle. We show by fluorescence-activated cell sorter and/or confocal microscopy analysis that an enhanced green fluorescent protein-tagged Vmw110 possesses the abilities both to prevent transfected cells moving from G(1) into S phase and to block infected cells at an unusual stage of mitosis defined as pseudo-prometaphase. The latter property correlates with the Vmw110-induced proteasome-dependent degradation of CENP-C, a centromeric protein component of the inner plate of human kinetochores. We also show that whereas Vmw110 is not the only viral product implicated in the block of infected cells at the G(1)/S border, the mitotic block is a specific property of Vmw110 and more particularly of its RING finger domain. These data explain the toxicity of Vmw110 when expressed alone in transfected cells and provide an explanation for the remaining toxicity of replication-defective mutants of HSV-1 expressing Vmw110. In addition to contributing to our understanding of the effects of Vmw110 on the cell, our results demonstrate that Vmw110 expression is incompatible with the proliferation of a dividing cell population. This factor is of obvious importance to the design of gene therapy vectors based on HSV-1.

MeSH Terms
Blotting, Western Cell Line Defective Viruses Flow Cytometry Fluorescent Antibody Technique G1 Phase Green Fluorescent Proteins Herpesvirus 1, Human/physiology Humans Immediate-Early Proteins/genetics,metabolism,physiology Luminescent Proteins/genetics,metabolism Microscopy, Confocal Mitosis Plasmids/genetics Recombinant Fusion Proteins S Phase Transfection Ubiquitin-Protein Ligases Virus Replication
Chemicals
Immediate-Early Proteins Luminescent Proteins Recombinant Fusion Proteins Green Fluorescent Proteins Ubiquitin-Protein Ligases Vmw110 protein, Human herpesvirus 1
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lomonte P
MRC Virology Unit, Glasgow G11 5JR, Scotland, United Kingdom. p.lomonte@vir.gla.ac.uk
Everett R D
References (53)
53 references, click to expand
  1. Characterization of transcription-deficient temperature-sensitive mutants of herpes simplex virus type 1.
    Virology. 1978 Dec;91(2):364-79 PMID: 217153
  2. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110.
    EMBO J. 1999 Mar 15;18(6):1526-38 PMID: 10075924
  3. Fine-structure mapping and functional analysis of temperature-sensitive mutants in the gene encoding the herpes simplex virus type 1 immediate early protein VP175.
    J Virol. 1980 Oct;36(1):189-203 PMID: 6255206
  4. A generalized technique for deletion of specific genes in large genomes: alpha gene 22 of herpes simplex virus 1 is not essential for growth.
    Cell. 1981 Jul;25(1):227-32 PMID: 6268303
  5. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4.
    Infect Immun. 1981 Dec;34(3):684-92 PMID: 6277788
  6. Temperature-sensitive mutants in herpes simplex virus type 1 ICP4 permissive for early gene expression.
    J Virol. 1984 Dec;52(3):767-76 PMID: 6092709
  7. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma.
    Chromosoma. 1985;91(3-4):313-21 PMID: 2579778
  8. Herpes simplex virus 1 mutant deleted in the alpha 22 gene: growth and gene expression in permissive and restrictive cells and establishment of latency in mice.
    J Virol. 1985 Aug;55(2):338-46 PMID: 2991560
  9. Herpes simplex virus type 1 ICP27 is an essential regulatory protein.
    J Virol. 1985 Sep;55(3):796-805 PMID: 2991596
  10. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110.
    J Gen Virol. 1986 Dec;67 ( Pt 12):2571-85 PMID: 3025339
  11. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture.
    J Virol. 1987 Mar;61(3):829-39 PMID: 3027408
  12. Formation of DNA replication structures in herpes virus-infected cells requires a viral DNA binding protein.
    Cell. 1988 Dec 2;55(5):857-68 PMID: 2847874
  13. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient.
    J Virol. 1989 Jan;63(1):18-27 PMID: 2535723
  14. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency.
    J Virol. 1989 Feb;63(2):759-68 PMID: 2536101
  15. Construction and characterization of a herpes simplex virus type 1 mutant unable to transinduce immediate-early gene expression.
    J Virol. 1989 May;63(5):2260-9 PMID: 2539517
  16. Construction and characterization of herpes simplex virus type 1 mutants with defined lesions in immediate early gene 1.
    J Gen Virol. 1989 May;70 ( Pt 5):1185-202 PMID: 2543774
  17. Herpes simplex virus type 1 immediate-early protein Vmw110 reactivates latent herpes simplex virus type 2 in an in vitro latency system.
    J Virol. 1989 Aug;63(8):3513-5 PMID: 2545921
  18. A herpes simplex virus type 1 mutant containing a deletion within immediate early gene 1 is latency-competent in mice.
    J Gen Virol. 1989 Sep;70 ( Pt 9):2501-6 PMID: 2550578
  19. Reactivation of latent herpes simplex virus by adenovirus recombinants encoding mutant IE-0 gene products.
    J Virol. 1990 Sep;64(9):4489-98 PMID: 2166826
  20. Injection of anticentromere antibodies in interphase disrupts events required for chromosome movement at mitosis.
    J Cell Biol. 1990 Oct;111(4):1519-33 PMID: 2211824
  21. Identification of a novel nuclear domain.
    J Cell Biol. 1991 Mar;112(5):785-95 PMID: 1999457
  22. Disruption of centromere assembly during interphase inhibits kinetochore morphogenesis and function in mitosis.
    Cell. 1991 Sep 20;66(6):1229-38 PMID: 1913807
  23. Cytotoxicity of a replication-defective mutant of herpes simplex virus type 1.
    J Virol. 1992 May;66(5):2952-65 PMID: 1373198
  24. CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate.
    Cell. 1992 Jul 10;70(1):115-25 PMID: 1339310
  25. The latency-associated transcripts of herpes simplex virus: RNA in search of function.
    Virology. 1992 Nov;191(1):1-8 PMID: 1329311
  26. The herpes simplex virus type 1 regulatory protein ICP0 enhances virus replication during acute infection and reactivation from latency.
    J Virol. 1993 Dec;67(12):7501-12 PMID: 8230470
  27. A truncated form of herpes simplex virus type 1 immediate-early protein Vmw110 is expressed in a cell type dependent manner.
    Virology. 1993 Dec;197(2):751-6 PMID: 7504367
  28. CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase.
    J Cell Biol. 1994 May;125(3):531-45 PMID: 8175879
  29. Herpes simplex virus type 1 immediate-early protein Vmw110 binds strongly and specifically to a 135-kDa cellular protein.
    Virology. 1994 May 1;200(2):457-69 PMID: 8178435
  30. DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control.
    Trends Biochem Sci. 1994 Mar;19(3):108-14 PMID: 8203017
  31. Improved cell survival by the reduction of immediate-early gene expression in replication-defective mutants of herpes simplex virus type 1 but not by mutation of the virion host shutoff function.
    J Virol. 1994 Oct;68(10):6347-62 PMID: 8083974
  32. G1 phase progression: cycling on cue.
    Cell. 1994 Nov 18;79(4):551-5 PMID: 7954821
  33. Cyclins and cancer. II: Cyclin D and CDK inhibitors come of age.
    Cell. 1994 Nov 18;79(4):573-82 PMID: 7954824
  34. DP and E2F proteins: coordinating transcription with cell cycle progression.
    Curr Opin Cell Biol. 1994 Dec;6(6):859-66 PMID: 7880534
  35. The retinoblastoma protein and cell cycle control.
    Cell. 1995 May 5;81(3):323-30 PMID: 7736585
  36. Induction by herpes simplex virus of free and heteromeric forms of E2F transcription factor.
    Virology. 1995 Nov 10;213(2):624-38 PMID: 7491786
  37. Prolonged gene expression and cell survival after infection by a herpes simplex virus mutant defective in the immediate-early genes encoding ICP4, ICP27, and ICP22.
    J Virol. 1996 Sep;70(9):6358-69 PMID: 8709264
  38. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0.
    J Virol. 1996 Nov;70(11):7471-7 PMID: 8892865
  39. Interaction of herpes simplex virus 1 alpha regulatory protein ICP0 with elongation factor 1delta: ICP0 affects translational machinery.
    J Virol. 1997 Feb;71(2):1019-24 PMID: 8995621
  40. Construction and characterization of herpes simplex virus type 1 mutants with conditional defects in immediate early gene expression.
    Virology. 1997 Mar 3;229(1):228-39 PMID: 9123865
  41. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein.
    EMBO J. 1997 Apr 1;16(7):1519-30 PMID: 9130697
  42. The herpes simplex virus immediate-early protein ICP0 affects transcription from the viral genome and infected-cell survival in the absence of ICP4 and ICP27.
    J Virol. 1997 Jun;71(6):4614-25 PMID: 9151855
  43. The herpes simplex virus type 1 immediate-early protein ICP0 is necessary for the efficient establishment of latent infection.
    J Virol. 1997 Sep;71(9):6777-85 PMID: 9261402
  44. Herpes simplex virus 1 alpha regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3.
    J Virol. 1997 Oct;71(10):7328-36 PMID: 9311810
  45. Repression of gene expression upon infection of cells with herpes simplex virus type 1 mutants impaired for immediate-early protein synthesis.
    J Virol. 1997 Oct;71(10):7807-13 PMID: 9311867
  46. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins.
    J Virol. 1998 Apr;72(4):3307-20 PMID: 9525658
  47. Requirement for cellular cyclin-dependent kinases in herpes simplex virus replication and transcription.
    J Virol. 1998 Jul;72(7):5626-37 PMID: 9621021
  48. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms.
    J Virol. 1998 Aug;72(8):6581-91 PMID: 9658103
  49. The vertebrate cell kinetochore and its roles during mitosis.
    Trends Cell Biol. 1998 Aug;8(8):310-8 PMID: 9704407
  50. A viral activator of gene expression functions via the ubiquitin-proteasome pathway.
    EMBO J. 1998 Dec 15;17(24):7161-9 PMID: 9857173
  51. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase.
    J Virol. 1999 Jan;73(1):650-7 PMID: 9847370
  52. Transcription of herpes simplex virus immediate-early and early genes is inhibited by roscovitine, an inhibitor specific for cellular cyclin-dependent kinases.
    J Virol. 1999 Mar;73(3):2161-72 PMID: 9971799
  53. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature-sensitive mutant tsK.
    J Virol. 1979 Jan;29(1):275-84 PMID: 219222
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1999-11-00
Pages
9456-67
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC112980
Subset
IM
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