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PMID: 10438802 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts.

Journal of virology ·Vol. 73 ·No. 9 ·1999-09-00 ·Pages 7153-64

Elgadi MM, Hayes CE, Smiley JR

Abstract

The herpes simplex virus virion host shutoff (vhs) protein (UL41 gene product) is a component of the HSV virion tegument that triggers shutoff of host protein synthesis and accelerated mRNA degradation during the early stages of HSV infection. Previous studies have demonstrated that extracts from HSV-infected cells and partially purified HSV virions display vhs-dependent RNase activity and that vhs is sufficient to trigger accelerated RNA degradation when expressed as the only HSV protein in an in vitro translation system derived from rabbit reticulocytes. We have used the rabbit reticulocyte translation system to characterize the mode of vhs-induced RNA decay in more detail. We report here that vhs-dependent RNA decay proceeds through endoribonucleolytic cleavage, is not affected by the presence of a 5' cap or a 3' poly(A) tail in the RNA substrate, requires Mg(2+), and occurs in the absence of ribosomes. Intriguingly, sites of preferential initial cleavage were clustered over the 5' quadrant of one RNA substrate that was characterized in detail. The vhs homologue of pseudorabies virus also induced accelerated RNA decay in this in vitro system.

MeSH Terms
Animals Base Sequence Dogs Endoribonucleases/genetics,metabolism HeLa Cells Herpesvirus 1, Suid Humans Magnesium Molecular Sequence Data Protein Biosynthesis RNA Caps/metabolism RNA, Messenger/metabolism Rabbits Ribonucleases Ribosomes Signal Recognition Particle/metabolism Substrate Specificity Viral Proteins/genetics,metabolism
Chemicals
RNA Caps RNA, Messenger Signal Recognition Particle Ul41 protein, Human herpesvirus 1 Viral Proteins virion host shutoff protein, Simplexvirus Endoribonucleases Ribonucleases Magnesium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Elgadi M M
Departments of Biology, McMaster University, Hamilton, Ontario, Canada L8N 3Z5.
Hayes C E
Smiley J R
References (52)
52 references, click to expand
  1. Herpes simplex virus VP16 forms a complex with the virion host shutoff protein vhs.
    J Virol. 1994 Apr;68(4):2339-46 PMID: 8139019
  2. Control of mRNA stability by the virion host shutoff function of herpes simplex virus.
    J Virol. 1989 May;63(5):1897-906 PMID: 2539493
  3. Transcription of the herpes simplex virus genome during productive and latent infection.
    Prog Nucleic Acid Res Mol Biol. 1995;51:123-65 PMID: 7659774
  4. Degradation of cellular mRNA during infection by herpes simplex virus.
    Proc Natl Acad Sci U S A. 1977 Jun;74(6):2370-4 PMID: 196289
  5. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  6. Picornavirus internal ribosome entry site elements target RNA cleavage events induced by the herpes simplex virus virion host shutoff protein.
    J Virol. 1999 Nov;73(11):9222-31 PMID: 10516030
  7. Macromolecular synthesis in cells infected with herpes simplex virus.
    Nature. 1965 Jun 26;206(991):1374-5 PMID: 4284477
  8. In vitro mRNA degradation system to study the virion host shutoff function of herpes simplex virus.
    J Virol. 1991 Jan;65(1):112-22 PMID: 1845879
  9. The virion host shutoff protein of herpes simplex virus inhibits reporter gene expression in the absence of other viral gene products.
    Virology. 1995 Aug 20;211(2):491-506 PMID: 7645253
  10. Genomic sequencing.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991-5 PMID: 6326095
  11. The virion host shutoff protein of herpes simplex virus type 1: messenger ribonucleolytic activity in vitro.
    J Virol. 1996 Apr;70(4):2411-9 PMID: 8642669
  12. Effects of herpes simplex virus on mRNA stability.
    J Virol. 1987 Jul;61(7):2198-207 PMID: 3035220
  13. On the control of immediate early (alpha) mRNA survival in cells infected with herpes simplex virus.
    J Gen Virol. 1988 Nov;69 ( Pt 11):2869-77 PMID: 2846763
  14. Analysis of herpes simplex virus-induced mRNA destabilizing activity using an in vitro mRNA decay system.
    Nucleic Acids Res. 1991 Aug 25;19(16):4459-65 PMID: 1653415
  15. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3' UTR and does not involve poly(A) tail shortening.
    EMBO J. 1994 Apr 15;13(8):1969-80 PMID: 7909515
  16. Polysomes and protein synthesis in cells infected with a DNA virus.
    Science. 1966 Jul 1;153(3731):76-8 PMID: 4287165
  17. Early virion-associated suppression of cellular protein synthesis by herpes simplex virus is accompanied by inactivation of mRNA.
    J Gen Virol. 1984 Jul;65 ( Pt 7):1225-8 PMID: 6086815
  18. Herpes simplex virus virion host shutoff function.
    J Virol. 1988 Mar;62(3):912-21 PMID: 2828686
  19. Early and delayed shut-off of host protein synthesis in cells infected with herpes simplex virus.
    J Gen Virol. 1982 Jul;61 (Pt l):121-5 PMID: 6288847
  20. Endonucleolytic cleavage of RNA at 5' endogenous stem structures by human flap endonuclease 1.
    Biochem Biophys Res Commun. 1998 Oct 20;251(2):501-8 PMID: 9792803
  21. Degradation of mRNA in eukaryotes.
    Cell. 1995 Apr 21;81(2):179-83 PMID: 7736570
  22. Identification and characterization of the virion-induced host shutoff product of herpes simplex virus gene UL41.
    J Gen Virol. 1992 Feb;73 ( Pt 2):467-70 PMID: 1311370
  23. Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies.
    J Virol. 1991 Nov;65(11):5886-94 PMID: 1656077
  24. Preparation of a cell-free translation system with minimal loss of initiation factor eIF-2/eIF-2B activity.
    Anal Biochem. 1993 Jul;212(1):17-23 PMID: 8368492
  25. Differential regulation of endogenous and transduced beta-globin genes during infection of erythroid cells with a herpes simplex virus type 1 recombinant.
    J Virol. 1990 Aug;64(8):3882-94 PMID: 1695257
  26. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1.
    J Gen Virol. 1988 Jul;69 ( Pt 7):1531-74 PMID: 2839594
  27. Transfer of UL41, the gene controlling virion-associated host cell shutoff, between different strains of herpes simplex virus.
    J Gen Virol. 1990 Feb;71 ( Pt 2):411-8 PMID: 2155295
  28. An amino-terminal domain containing hydrophobic and hydrophilic sequences binds the signal recognition particle receptor alpha subunit to the beta subunit on the endoplasmic reticulum membrane.
    J Biol Chem. 1995 Jun 30;270(26):15650-7 PMID: 7797564
  29. The pseudorabies virus host-shutoff homolog gene: nucleotide sequence and comparison with alphaherpesvirus protein counterparts.
    Virology. 1993 Apr;193(2):1028-32 PMID: 8384744
  30. Both the 5' untranslated region and the sequences surrounding the start site contribute to efficient initiation of translation in vitro.
    Mol Cell Biol. 1991 May;11(5):2656-64 PMID: 2017171
  31. Multiple regulatory steps control histone mRNA concentrations.
    Trends Biochem Sci. 1988 Feb;13(2):49-52 PMID: 3070846
  32. Requirement of protein synthesis for the degradation of host mRNA in Friend erythroleukemia cells infected wtih herpes simplex virus type 1.
    J Virol. 1978 Sep;27(3):619-27 PMID: 212585
  33. Sequence-specific endonucleolytic cleavage and protection of mRNA in Xenopus and Drosophila.
    Genes Dev. 1993 Aug;7(8):1620-31 PMID: 8339937
  34. Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function.
    EMBO J. 1996 May 15;15(10):2575-81 PMID: 8665865
  35. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1926-30 PMID: 3031658
  36. A mutant of herpes simplex virus type 1 exhibits increased stability of immediate-early (alpha) mRNAs.
    J Virol. 1987 Feb;61(2):604-6 PMID: 3027388
  37. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA.
    Nature. 1988 Jul 28;334(6180):320-5 PMID: 2839775
  38. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins.
    J Virol. 1974 Jul;14(1):8-19 PMID: 4365321
  39. Degradation of cellular mRNAs induced by a virion-associated factor during herpes simplex virus infection of Vero cells.
    J Virol. 1985 Sep;55(3):601-10 PMID: 4020960
  40. Mutational analysis of the herpes simplex virus virion host shutoff protein: evidence that vhs functions in the absence of other viral proteins.
    J Virol. 1995 Aug;69(8):4863-71 PMID: 7609054
  41. Isolation of a herpes simplex virus type 1 mutant with a deletion in the virion host shutoff gene and identification of multiple forms of the vhs (UL41) polypeptide.
    J Virol. 1993 Dec;67(12):7149-60 PMID: 8230437
  42. Characterization of the immediate-early functions of pseudorabies virus.
    Virology. 1983 Dec;131(2):437-54 PMID: 6318440
  43. The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair.
    Bioessays. 1997 Mar;19(3):233-40 PMID: 9080773
  44. Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of alpha (immediate early) viral polypeptides.
    J Virol. 1983 May;46(2):498-512 PMID: 6302315
  45. Suppression of the synthesis of cellular macromolecules by herpes simplex virus.
    J Gen Virol. 1978 Oct;41(1):37-51 PMID: 212520
  46. The disaggregation of host polyribosomes in productive and abortive infection with herpes simplex virus.
    Virology. 1967 Aug;32(4):678-86 PMID: 18614067
  47. Starting at the beginning, middle, and end: translation initiation in eukaryotes.
    Cell. 1997 Jun 13;89(6):831-8 PMID: 9200601
  48. Early functions of the genome of herpesvirus. II. Inhibition of the formation of cell-specific polysomes.
    Virology. 1971 Dec;46(3):890-9 PMID: 5167662
  49. Inactivation of the shutoff gene (UL41) of herpes simplex virus types 1 and 2.
    J Gen Virol. 1990 Dec;71 ( Pt 12):2961-7 PMID: 2177088
  50. The sedimentation profiles of cytoplasmic polyribosomes in mammalian cells productively and abortively infected with herpes simplex virus.
    Virology. 1968 Mar;34(3):562-5 PMID: 4297165
  51. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA.
    Nucleic Acids Res. 1996 Jul 1;24(13):2488-97 PMID: 8692686
  52. Role of the virion host shutoff (vhs) of herpes simplex virus type 1 in latency and pathogenesis.
    J Virol. 1995 Nov;69(11):6779-86 PMID: 7474089
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1999-09-00
Pages
7153-64
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC104239
Subset
IM
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