Home LiteratureArticle Details
PMID: 8289400 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following herpes simplex virus infection.

Journal of virology ·Vol. 68 ·No. 2 ·1994-02-00 ·Pages 988-1001

Rice SA, Long MC, Lam V, Spencer CA

Abstract

During lytic infection, herpes simplex virus subverts the host cell RNA polymerase II transcription machinery to efficiently express its own genome while repressing the expression of most cellular genes. The mechanism by which RNA polymerase II is directed to the viral delayed-early and late genes is still unresolved. We report here that RNA polymerase II is preferentially localized to viral replication compartments early after infection with herpes simplex virus type 1. Concurrent with recruitment of RNA polymerase II into viral compartments is a rapid and aberrant phosphorylation of the large subunit carboxy-terminal domain (CTD). Aberrant phosphorylation of the CTD requires early viral gene expression but is not dependent on viral DNA replication or on the formation of viral replication compartments. Localization of RNA polymerase II and modifications to the CTD may be instrumental in favoring transcription of viral genes and repressing specific transcription of cellular genes.

MeSH Terms
Animals Biological Transport Cell Compartmentation Cell Nucleus/metabolism Cells, Cultured Gene Expression Regulation, Viral Herpesvirus 1, Human/enzymology,growth & development Humans Immunohistochemistry Phosphorylation Protein Processing, Post-Translational RNA Polymerase II/isolation & purification,metabolism Time Factors Transcription, Genetic Virus Replication
Chemicals
RNA Polymerase II
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rice S A
Department of Biochemistry, University of Alberta, Edmonton, Canada.
Long M C
Lam V
Spencer C A
References (94)
94 references, click to expand
  1. RNA polymerase II.
    Annu Rev Biochem. 1991;60:689-715 PMID: 1883205
  2. Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription.
    Nature. 1993 May 27;363(6427):371-4 PMID: 8497323
  3. RNA polymerase II transcription cycles.
    Curr Opin Genet Dev. 1993 Apr;3(2):213-8 PMID: 8504246
  4. Polysomes and protein synthesis in cells infected with a DNA virus.
    Science. 1966 Jul 1;153(3731):76-8 PMID: 4287165
  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. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  7. 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
  8. 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
  9. 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
  10. A herpes simplex virus type 1 function continuously required for early and late virus RNA synthesis.
    Nature. 1980 May 29;285(5763):329-30 PMID: 6246451
  11. Monoclonal antibody directed against RNA polymerase II of Drosophila melanogaster.
    Mol Gen Genet. 1980;180(1):193-9 PMID: 6777631
  12. The structure of herpes simplex virus type 1 DNA as probed by micrococcal nuclease digestion.
    J Gen Virol. 1980 Nov;51(Pt 1):45-59 PMID: 6257837
  13. Immunological relatedness of subunits of RNA polymerase II from insects and mammals.
    Eur J Biochem. 1981 Jul;117(3):449-55 PMID: 6793357
  14. Regulation of herpesvirus macromolecular synthesis: temporal order of transcription of alpha genes is not dependent on the stringency of inhibition of protein synthesis.
    J Virol. 1981 Oct;40(1):319-22 PMID: 6270385
  15. Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus.
    J Virol. 1982 Jul;43(1):314-24 PMID: 6287005
  16. 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
  17. Herpes simplex virus types 1 and 2 induce shutoff of host protein synthesis by different mechanisms in Friend erythroleukemia cells.
    J Virol. 1983 Jan;45(1):241-50 PMID: 6296433
  18. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication.
    Cell. 1984 Apr;36(4):857-68 PMID: 6323024
  19. 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
  20. Differential stability of host mRNAs in Friend erythroleukemia cells infected with herpes simplex virus type 1.
    J Virol. 1985 Jan;53(1):1-6 PMID: 2981326
  21. 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
  22. Herpes simplex virus type 1 ICP27 is an essential regulatory protein.
    J Virol. 1985 Sep;55(3):796-805 PMID: 2991596
  23. Virion component of herpes simplex virus type 1 KOS interferes with early shutoff of host protein synthesis induced by herpes simplex virus type 2 186.
    J Virol. 1985 Oct;56(1):312-6 PMID: 2993660
  24. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4.
    J Virol. 1985 Nov;56(2):558-70 PMID: 2997476
  25. Activation of cellular promoters during herpes virus infection of biochemically transformed cells.
    EMBO J. 1985 Aug;4(8):1973-80 PMID: 2998778
  26. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):7934-8 PMID: 2999785
  27. Transcriptional control of herpesvirus gene expression: gene functions required for positive and negative regulation.
    Proc Natl Acad Sci U S A. 1986 Jan;83(2):256-60 PMID: 3001729
  28. Chromosomal organization of the herpes simplex virus genome during acute infection of the mouse central nervous system.
    J Virol. 1986 Sep;59(3):764-7 PMID: 3016340
  29. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4.
    Mol Cell Biol. 1985 Aug;5(8):1997-2008 PMID: 3018543
  30. A genetic approach to promoter recognition during trans induction of viral gene expression.
    Science. 1986 Oct 3;234(4772):53-9 PMID: 3018926
  31. Transcriptional selectivity of viral genes in mammalian cells.
    Cell. 1986 Sep 12;46(6):795-805 PMID: 3530495
  32. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10004-8 PMID: 1946417
  33. RNA polymerase II carboxy-terminal domain contributes to the response to multiple acidic activators in vitro.
    Genes Dev. 1991 Dec;5(12B):2431-40 PMID: 1752437
  34. The ICP4 binding sites in the herpes simplex virus type 1 glycoprotein D (gD) promoter are not essential for efficient gD transcription during virus infection.
    J Virol. 1992 Feb;66(2):623-31 PMID: 1309905
  35. DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats.
    Genes Dev. 1992 Mar;6(3):426-38 PMID: 1547941
  36. Mechanism of assembly of the RNA polymerase II preinitiation complex. Evidence for a functional interaction between the carboxyl-terminal domain of the largest subunit of RNA polymerase II and a high molecular mass form of the TATA factor.
    J Biol Chem. 1992 Apr 25;267(12):8464-7 PMID: 1569096
  37. The HIP1 initiator element plays a role in determining the in vitro requirement of the dihydrofolate reductase gene promoter for the C-terminal domain of RNA polymerase II.
    Mol Cell Biol. 1992 May;12(5):2250-9 PMID: 1569952
  38. The interaction of RNA polymerase II with the adenovirus-2 major late promoter is precluded by phosphorylation of the C-terminal domain of subunit IIa.
    J Biol Chem. 1992 May 25;267(15):10500-6 PMID: 1316903
  39. Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein.
    Cell. 1992 May 29;69(5):871-81 PMID: 1591781
  40. A novel transcription factor reveals a functional link between the RNA polymerase II CTD and TFIID.
    Cell. 1992 May 29;69(5):883-94 PMID: 1591782
  41. Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II.
    Nature. 1992 Aug 20;358(6388):641-5 PMID: 1495560
  42. A carboxyl-terminal-domain kinase associated with RNA polymerase II transcription factor delta from rat liver.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7476-80 PMID: 1386928
  43. Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11920-4 PMID: 1465419
  44. Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxyl-terminal domain of RNA polymerase subunit IIa.
    J Biol Chem. 1993 Jan 5;268(1):80-7 PMID: 8416977
  45. The cell's nucleus shapes up.
    Science. 1993 Feb 26;259(5099):1257-9 PMID: 8446894
  46. Higher level organization of individual gene transcription and RNA splicing.
    Science. 1993 Feb 26;259(5099):1326-30 PMID: 8446901
  47. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism.
    Cell. 1993 Apr 9;73(1):47-59 PMID: 8462102
  48. Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three-dimensional wide-field microscopy.
    Cell. 1993 Apr 9;73(1):97-108 PMID: 8384932
  49. Visualization of replication factories attached to nucleoskeleton.
    Cell. 1993 Apr 23;73(2):361-73 PMID: 8097433
  50. Positive patches and negative noodles: linking RNA processing to transcription?
    Trends Biochem Sci. 1993 Apr;18(4):117-9 PMID: 8493720
  51. RNA contacts subunits IIo and IIc in HeLa RNA polymerase II transcription complexes.
    J Biol Chem. 1986 Oct 25;261(30):14226-31 PMID: 2429953
  52. The control of herpes simplex virus type-1 late gene transcription: a 'TATA-box'/cap site region is sufficient for fully efficient regulated activity.
    Nucleic Acids Res. 1986 Nov 11;14(21):8247-64 PMID: 3024102
  53. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4.
    J Virol. 1987 Feb;61(2):276-84 PMID: 3027360
  54. 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
  55. Expression of a cellular gene cloned in herpes simplex virus: rabbit beta-globin is regulated as an early viral gene in infected fibroblasts.
    J Virol. 1987 Aug;61(8):2368-77 PMID: 3037101
  56. Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II.
    J Biol Chem. 1987 Sep 15;262(26):12468-74 PMID: 3624268
  57. Transcriptional and post-transcriptional controls establish the cascade of herpes simplex virus protein synthesis.
    J Mol Biol. 1987 Jun 20;195(4):819-33 PMID: 2821283
  58. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function.
    Mol Cell Biol. 1988 Jan;8(1):321-9 PMID: 3122024
  59. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI.
    J Virol. 1988 Apr;62(4):1347-54 PMID: 2831396
  60. A specific 15-bp TATA box promoter element is required for expression of a herpes simplex virus type 1 late gene.
    Genes Dev. 1988 Jan;2(1):40-53 PMID: 2833425
  61. Transcriptional activation. Acid blobs and negative noodles.
    Nature. 1988 May 19;333(6170):210-2 PMID: 3367995
  62. The C-terminal repeat domain of RNA polymerase II largest subunit is essential in vivo but is not required for accurate transcription initiation in vitro.
    Proc Natl Acad Sci U S A. 1988 Jun;85(11):3698-702 PMID: 3131761
  63. Gene-specific transactivation by herpes simplex virus type 1 alpha protein ICP27.
    J Virol. 1988 Oct;62(10):3814-23 PMID: 2843677
  64. 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
  65. 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
  66. Purification of RNA polymerase IIO from calf thymus.
    J Biol Chem. 1988 Dec 15;263(35):18880-5 PMID: 3198603
  67. The regions of the herpes simplex virus type 1 immediate early protein Vmw175 required for site specific DNA binding closely correspond to those involved in transcriptional regulation.
    Nucleic Acids Res. 1988 Dec 9;16(23):11005-25 PMID: 2849757
  68. During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure.
    J Virol. 1989 Feb;63(2):943-7 PMID: 2536115
  69. The major late promoter of adenovirus-2 is accurately transcribed by RNA polymerases IIO, IIA, and IIB.
    J Biol Chem. 1989 Feb 25;264(6):3169-76 PMID: 2914948
  70. Mutations in RNA polymerase II enhance or suppress mutations in GAL4.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2794-8 PMID: 2495535
  71. A protein kinase that phosphorylates the C-terminal repeat domain of the largest subunit of RNA polymerase II.
    Proc Natl Acad Sci U S A. 1989 May;86(10):3624-8 PMID: 2657724
  72. Herpes simplex virus alpha protein ICP27 can inhibit or augment viral gene transactivation.
    Virology. 1989 Jun;170(2):496-504 PMID: 2543126
  73. Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II.
    J Biol Chem. 1989 Jul 5;264(19):11511-20 PMID: 2472398
  74. Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2.
    Nature. 1989 Jun 29;339(6227):679-84 PMID: 2662013
  75. Separation of primary structural components conferring autoregulation, transactivation, and DNA-binding properties to the herpes simplex virus transcriptional regulatory protein ICP4.
    J Virol. 1989 Sep;63(9):3714-28 PMID: 2760981
  76. The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa.
    J Biol Chem. 1989 Nov 25;264(33):19621-9 PMID: 2584185
  77. Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein.
    J Virol. 1989 Dec;63(12):5258-67 PMID: 2555553
  78. Intragenic and extragenic suppressors of mutations in the heptapeptide repeat domain of Saccharomyces cerevisiae RNA polymerase II.
    Genetics. 1989 Dec;123(4):715-24 PMID: 2693207
  79. Purification of eukaryotic RNA polymerase II by immunoaffinity chromatography. Elution of active enzyme with protein stabilizing agents from a polyol-responsive monoclonal antibody.
    J Biol Chem. 1990 Apr 25;265(12):7069-77 PMID: 2324114
  80. Intranuclear localization of herpes simplex virus immediate-early and delayed-early proteins: evidence that ICP 4 is associated with progeny virus DNA.
    J Gen Virol. 1986 Oct;67 ( Pt 10):2163-77 PMID: 3020158
  81. Immunochemical analysis of mammalian RNA polymerase II subspecies. Stability and relative in vivo concentration.
    J Biol Chem. 1986 Oct 25;261(30):14219-25 PMID: 3095316
  82. RNA polymerase II subunit composition, stoichiometry, and phosphorylation.
    Mol Cell Biol. 1990 May;10(5):1915-20 PMID: 2183013
  83. The carboxyl-terminal repeat domain of RNA polymerase II is not required for transcription factor Sp1 to function in vitro.
    J Biol Chem. 1990 May 25;265(15):8351-3 PMID: 2187861
  84. 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
  85. RNA polymerase B (II) and general transcription factors.
    Annu Rev Biochem. 1990;59:711-54 PMID: 2197989
  86. Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription.
    J Biol Chem. 1990 Aug 5;265(22):13165-73 PMID: 2376591
  87. Transcription initiation complexes and upstream activation with RNA polymerase II lacking the C-terminal domain of the largest subunit.
    Mol Cell Biol. 1990 Oct;10(10):5562-4 PMID: 2398901
  88. RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals.
    Nature. 1990 Oct 4;347(6292):491-4 PMID: 2215664
  89. RNA polymerase II: subunit structure and function.
    Trends Biochem Sci. 1990 Sep;15(9):347-51 PMID: 1700503
  90. Tails of RNA polymerase II.
    Trends Biochem Sci. 1990 Oct;15(10):383-7 PMID: 2251729
  91. Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit.
    J Biol Chem. 1991 Feb 5;266(4):2290-6 PMID: 1899239
  92. Phosphorylation causes a conformational change in the carboxyl-terminal domain of the mouse RNA polymerase II largest subunit.
    J Biol Chem. 1991 Feb 5;266(4):2297-302 PMID: 1989983
  93. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells.
    Nature. 1991 Jan 31;349(6308):429-31 PMID: 1671528
  94. A functional interaction between the C-terminal domain of RNA polymerase II and the negative regulator SIN1.
    Cell. 1991 Mar 22;64(6):1135-43 PMID: 2004420
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1994-02-00
Pages
988-1001
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC236537
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